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Biosystems & Biorobotics

Winnie Jensen
Ole Kæseler Andersen
Metin Akay Editors

Replace, Repair,
Restore, Relieve –
Bridging Clinical and
Engineering Solutions
in Neurorehabilitation
Proceedings of the 2nd International Conference
on NeuroRehabilitation (ICNR2014),
Aalborg, 24–26 June, 2014
Biosystems & Biorobotics

Volume 7

Series editor
Eugenio Guglielmelli, Campus Bio-Medico University of Rome, Rome, Italy
e-mail: e.guglielmelli@unicampus.it

Editorial Board
Dino Accoto, Campus Bio-Medico University of Rome, Rome, Italy
Sunil Agrawal, University of Delaware, Newark DE, USA
Fabio Babiloni, Sapienza University of Rome, Rome, Italy
Jose M. Carmena, University of California, Berkeley CA, USA
Maria Chiara Carrozza, Scuola Superiore Sant’Anna, Pisa, Italy
Paolo Dario, Scuola Superiore Sant’Anna, Pisa, Italy
Arturo Forner-Cordero, University of Sao Paolo, São Paulo, Brazil
Masakatsu G. Fujie, Waseda University, Tokyo, Japan
Nicolas Garcia, Miguel Hernández University of Elche, Elche, Spain
Neville Hogan, Massachusetts Institute of Technology, Cambridge MA, USA
Hermano Igo Krebs, Massachusetts Institute of Technology, Cambridge MA, USA
Dirk Lefeber, Vrije Universiteit Brussel, Brussels, Belgium
Rui Loureiro, Middlesex University, London, UK
Marko Munih, University of Ljubljana, Ljubljana, Slovenia
Paolo M. Rossini, University Cattolica del Sacro Cuore, Rome, Italy
Atsuo Takanishi, Waseda University, Tokyo, Japan
Russell H. Taylor, The Johns Hopkins University, Baltimore, MD, USA
David A. Weitz, Harvard University, Cambridge MA, USA
Loredana Zollo, Campus Bio-Medico University of Rome, Rome, Italy

For further volumes:


http://www.springer.com/series/10421
Aims & Scope

Biosystems & Biorobotics publishes the latest research developments in three main areas:
1) understanding biological systems from a bioengineering point of view, i.e. the study of
biosystems by exploiting engineering methods and tools to unveil their functioning principles
and unrivalled performance; 2) design and development of biologically inspired machines
and systems to be used for different purposes and in a variety of application contexts. The
series welcomes contributions on novel design approaches, methods and tools as well as
case studies on specific bioinspired systems; 3) design and developments of nano-, micro-,
macro- devices and systems for biomedical applications, i.e. technologies that can improve
modern healthcare and welfare by enabling novel solutions for prevention, diagnosis, surgery,
prosthetics, rehabilitation and independent living.
On one side, the series focuses on recent methods and technologies which allow multi-
scale, multi-physics, high-resolution analysis and modeling of biological systems. A special
emphasis on this side is given to the use of mechatronic and robotic systems as a tool for
basic research in biology. On the other side, the series authoritatively reports on current theo-
retical and experimental challenges and developments related to the “biomechatronic” design
of novel biorobotic machines. A special emphasis on this side is given to human-machine
interaction and interfacing, and also to the ethical and social implications of this emerging
research area, as key challenges for the acceptability and sustainability of biorobotics tech-
nology.
The main target of the series are engineers interested in biology and medicine, and specif-
ically bioengineers and bioroboticists. Volume published in the series comprise monographs,
edited volumes, lecture notes, as well as selected conference proceedings and PhD theses.
The series also publishes books purposely devoted to support education in bioengineering,
biomedical engineering, biomechatronics and biorobotics at graduate and post-graduate lev-
els.

About the Cover


The cover of the book series Biosystems & Biorobotics features a robotic hand prosthesis.
This looks like a natural hand and is ready to be implanted on a human amputee to help them
recover their physical capabilities. This picture was chosen to represent a variety of concepts
and disciplines: from the understanding of biological systems to biomechatronics, bioinspira-
tion and biomimetics; and from the concept of human-robot and human-machine interaction
to the use of robots and, more generally, of engineering techniques for biological research and
in healthcare. The picture also points to the social impact of bioengineering research and to its
potential for improving human health and the quality of life of all individuals, including those
with special needs. The picture was taken during the LIFEHAND experimental trials run at
Università Campus Bio-Medico of Rome (Italy) in 2008. The LIFEHAND project tested the
ability of an amputee patient to control the Cyberhand, a robotic prosthesis developed at
Scuola Superiore Sant’Anna in Pisa (Italy), using the tf-LIFE electrodes developed at the
Fraunhofer Institute for Biomedical Engineering (IBMT, Germany), which were implanted
in the patient’s arm. The implanted tf-LIFE electrodes were shown to enable bidirectional
communication (from brain to hand and vice versa) between the brain and the Cyberhand. As
a result, the patient was able to control complex movements of the prosthesis, while receiving
sensory feedback in the form of direct neurostimulation. For more information please visit
http://www.biorobotics.it or contact the Series Editor.
Winnie Jensen · Ole Kæseler Andersen
Metin Akay
Editors

Replace, Repair, Restore,


Relieve – Bridging Clinical
and Engineering Solutions
in Neurorehabilitation
Proceedings of the 2nd International
Conference on NeuroRehabilitation
(ICNR2014), Aalborg, 24–26 June, 2014

ABC
Editors
Winnie Jensen Metin Akay
Center for Sensory-Motor Interaction Biomedical Engineering Department
Aalborg University University of Houston
Aalborg Houston Texas
Denmark USA

Ole Kæseler Andersen


Center for Sensory-Motor Interaction
Aalborg University
Aalborg
Denmark

ISSN 2195-3562 ISSN 2195-3570 (electronic)


ISBN 978-3-319-08071-0 ISBN 978-3-319-08072-7 (eBook)
DOI 10.1007/978-3-319-08072-7
Springer Cham Heidelberg New York Dordrecht London

Library of Congress Control Number: 2014942266

c Springer International Publishing Switzerland 2014


This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of
the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation,
broadcasting, reproduction on microfilms or in any other physical way, and transmission or information
storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology
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with reviews or scholarly analysis or material supplied specifically for the purpose of being entered
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The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication
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Springer is part of Springer Science+Business Media (www.springer.com)


Preface

Replace, Repair, Restore, Relieve – Bridging Clinical and Engineering Solutions in


Neurorehabilitation
Neural rehabilitation engineering is an emerging interdisciplinary research area
that aims to bridge neuroscience and engineering methods, and the present book fo-
cuses on developing novel solutions and therapies for people suffering from various
motor disabilities. Despite neural engineering is a relatively new research area, the
field is rapidly developing. This development requires continuously updated mate-
rial available for the increasing number of researchers and students in neural reha-
bilitation engineering.
The 2nd International Conference on NeuroRehabilitation took place on 24th -
th
26 June 2014 in Aalborg, Denmark, with participation of rehabilitation medicine
specialists, engineers, physiotherapists, exercise physiologists, neurophysiologists,
and other professionals involved in neuromuscular rehabilitation research.
The main themes of the conference were; neurorehabilitation applications and so-
lutions to restore or repair impaired neurological functions, techniques and methods
in neurorehabilitation, and translational challenges in neurorehabilitation. In addi-
tion, the conference hosted a commercially oriented track with emphasis on bringing
cutting-edge innovative technologies and research in neurorehabilitation from bench
to bedside.
This book contains the original conference contributions presented and discussed
at the conference.
The book is organized in four parts related to the main activities of the confer-
ence; 1) Plenary lectures, 2) Special sessions covering a range of specific topics
within neurorehabilitation, 3) Regular conference contributions, and 4) Innovation
session contributions. Each of the contribution parts are placed in alphabetical order
by the surname of the first author.
VI Preface

We would like to thank the scientific program committee for their invaluable
help to review the enclosed material and assist in securing high quality manuscripts.
We believe that this book presents the state-of-the-art within neurorehabilitation
research, and we do hope that many students and young researchers will find inspi-
ration within these pages.

Winnie Jensen
Ole Kæseler Andersen
Metin Akay
Contents

Keynote Papers
Role of Cortical Reorganization in the Rehabilitation of Chronic
Pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
Herta Flor
Induction of Cortical Plasticity: Clinical Applications . . . . . . . . . . . . . . . . 3
Min-Fang Kuo, Walter Paulus, Michael A. Nitsche
Miniaturized Neural Interfaces and Implants in Neurological
Rehabilitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
Thomas Stieglitz
Neuroprosthetics: Past, Present and Future . . . . . . . . . . . . . . . . . . . . . . . . . 15
Nitish V. Thakor

Special-Session Papers
Neuroplasticity in Constraint-Induced Movement Therapy . . . . . . . . . . . 23
Jakob Udby Blicher, Jamie Near, Erhard Næss-Schmidt, Leif Østergaard,
Heidi Johansen-Berg, Charlotte J. Stagg, Jørgen Feldbæk Nielsen,
Yi-Ching Lynn Ho
Advanced Prosthetic Control in Transhumeral Amputees Using
Osseointegration and Bidirectional Neuromuscular Interfaces . . . . . . . . . 25
Rickard Brånemark
The Control of Interlimb Coordination during Left-Right and
Transverse Split-Belt Locomotion in Intact and Spinal Cord-Injured
Cats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
Alain Frigon, Yann Thibaudier, Marie-France Hurteau,
Alessandro Telonio, Charline Dambreville, Victoria Kuczynski
VIII Contents

Chiropractic Alters TMS Induced Motor Neuronal Excitability:


Preliminary Findings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35
Heidi Haavik, Imran Khan Niazi, Jens Duehr, Mat Kinget,
Paulius Ugincius, Oğuz Sebik, Gizem Yılmaz, Kemal S. Türker
Strength and Motor Function after Arm Training with an Exoskeleton
Robot . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
Verena Klamroth-Marganska, Georg Rauter, Robert Riener
Tongue Motor Training – Behavioral and Neurophysiological
Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
M. Kothari, P. Svensson, J. Jensen, A. Kjaersgaard, L. Baad-Hansen,
Jørgen Feldbæk Nielsen
Functional Electrical Stimulation, Clinical Perspective
and Implications for Future Neurorehabilitation . . . . . . . . . . . . . . . . . . . . 49
P.T. Birgit Larsen
Fully Implantable Multichannel EMG Measurement System:
First Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51
Sören Lewis, Michael Russold, Marie Hahn, Oskar C. Aszmann

Does Computerized Cognitive Rehabilitation Generalize? . . . . . . . . . . . . . 61


Jonas Lindeløv
Clinical Rationale and Guidelines for Rehabilitation at Home . . . . . . . . . 63
Andreas Luft
The Learning Benefits of Haptic Guidance Are Age-Dependent . . . . . . . . 65
Laura Marchal-Crespo, Mark van Raai, Georg Rauter, Peter Wolf,
Robert Riener
Robot Supported Gait Rehabilitation: Clinical Needs, Current State
of the Art and Future . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
Zlatko Matjačić, Andrej Olenšek, Matjaž Zadravec
Spinal Cord Stimulation: Background and Clinical Application . . . . . . . . 81
Kaare Meier
Clinical Evaluation of Training System for Recovery of Motor
Function after Stroke in Patients with Hemiplegia . . . . . . . . . . . . . . . . . . . 83
Yoshifumi Morita, Noritaka Sato, Hiroyuki Ukai, Hirofumi Tanabe,
Toru Nagao, Rumi Tanemura, Yoshiaki Takagi, Yoshitaka Aoki
Exotendon Glove System for Finger Rehabilitation after Stroke . . . . . . . . 93
Shunji Moromugi, Toshio Higashi, Ryo Ishikawa, Seiya Kudo, Naoki Iso,
Shirou Ooso, Takeaki Shirotani, Murray J. Lawn, Takakazu Ishimatsu
Contents IX

Stretch Reflex Conditioning in Humans – Implications for Function . . . . 103


Natalie Mrachacz-Kersting, Priscila de Brito Silva, Yukiko Makihara,
Lars Arendt-Nielsen, Thomas Sinkjær, Uwe G. Kersting
The Role of Spinal Manipulation in Modulating Neuroplasticity
and Sensorimotor Integration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113
Bernadette Murphy, Heidi Haavik
Mathematical Modeling in Neuromodulation for Pain Relief . . . . . . . . . . 117
Carsten Dahl Mørch
Chiropractic, Cortical Excitability and BCI . . . . . . . . . . . . . . . . . . . . . . . . 121
Imran Khan Niazi, Mads Jochumsen, Jens Duehra, Mat Kingett,
Kim Dremstrup, Heidi Haavik
Abstract: Technical Device for Measurement of Spasticity, Developed
for Bedside Use . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
Tue Hvass Petersen
Game Engines and Exergames to Guide Rehabilitation at Home . . . . . . . 129
Michele Pirovano, Renato Mainetti, Pier Luca Lanzi,
Nunzio Alberto Borghese
Mechanism of Spinal Cord and Peripheral Nerve Stimulation:
More than the Gate Control Theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
Louis Vera-Portocarrero
Lokomat: Clinical Training and Experience in a Neurorehabiltation
Hospital . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137
Christian Gunge Riberholt

CORBYS Project Overview: Approach and Achieved Results . . . . . . . . . 139


Danijela Ristić-Durrant, Siniša Slavnić, Cornelius Glackin
Rehabilitation Robot in Primary Walking Pattern Training for SCI
Patient . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149
Taisuke Sakaki, Nobuhiro Ushimi, Koji Murakami,
Yong-Kwun Lee, Kazuhiro Tsuruta, Kanta Aoki, Kaoru Fujiie,
Ryuji Katamoto, Atsushi Sugyo, Yoshimitsu Kihara, Kenji Tateishi
Effect of Transcranial and Spinal Direct Current Stimulation on
Gait . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159
Giorgio Sandrini, C. Mondino
Adaptive Behavior of the Spinal Cord in the Transition from Quiet
Stance to Walking: The Use of Widthrawal Reflexes to Support Gait
Initiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161
Mariano Serrao
X Contents

Using Painful Sensory Stimulation to Improve the Hemiparetic Gait . . . . 165


Erika Geraldina Spaich, Ole Kæseler Andersen
Advanced Rehabilitation for Amputees after Selective Nerve
Transfers: EMG-Guided Training and Testing . . . . . . . . . . . . . . . . . . . . . . 169
Agnes Sturma, Peter Göbel, Malvina Herceg, Nan Gee, Aidan Roche,
Veronika Fialka-Moser, Oskar C. Aszmann
Learning to Change a Reflex to Improve Locomotion . . . . . . . . . . . . . . . . 179
Aiko K. Thompson
Advances in Robotic Gait Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187
Herman van der Kooij, Edwin H.F. van Asseldonk, Bram Koopman,
Gijs van Oort, Jos Meuleman, H. Carsten van Voort, S.M. Behrens
Assessing of Motor Performance in Stroke Using Body Worn Sensing . . . 191
Fokke B. van Meulen, Jasper Reenalda, Peter H. Veltink
Improving Interlimb Coordination Following Stroke: How Can We
Change How People Walk (and Why Should We)? . . . . . . . . . . . . . . . . . . . 195
Erin V. Vasudevan, Eileen M. Kirk
Exoskeletons Supporting Postural Balance – The BALANCE Project . . . 203
Jan F. Veneman
Spinal Reflex Conditioning: Mechanisms and Implications . . . . . . . . . . . . 209
Jonathan R. Wolpaw
Neuromechanical Interlimb Interactions and Rehabilitation of
Walking after Stroke . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 219
E. Paul Zehr, Trevor S. Barss, Chelsea Kaupp, Taryn Klarner,
Rinaldo A. Mezzarane, Tsuyoshi Nakajima, Yao Sun,
Tomoyoshi Komiyama

Conference Papers
Feature and Channel Selection Using Correlation Based Method for
Hand Posture Classification in Multiple Arm Positions . . . . . . . . . . . . . . . 227
Haitham M. Al-Angari, Gunter Kanitz, Sergio Tarantino, Jacopo Rigosa,
Christian Cipriani
Detection of Movement Intention from Movement-Related Cortical
Potentials with Different Paradigms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 237
Susan Aliakbaryhosseinabadi, Ning Jiang, Aleksandra Vuckovic,
Romulus Lontis, Kim Dremstrup, Dario Farina,
Natalie Mrachacz-Kersting
Contents XI

Muscle Synergy Features in Behavior Adaptation and Recovery . . . . . . . 245


Fady S. Alnajjar, Vincent Berenz, Ozaki Ken-ichi, Kensuke Ohno,
Hitoshi Yamada, Izumi Kondo, Shingo Shimoda
Human Cutaneous Reflexes Evoked with Simultaneous Multiple
Nerve Stimulation during Rhythmic Locomotor-Like Arm and Leg
Cycling in Stroke Subjects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 255
Ole Kæseler Andersen, Marc Klimstra, Evan Thomas,
Pamela M. Loadman, Sandra R. Hundza, E. Paul Zehr
Towards Establishing Clinical Guidelines for an Arm Rehabilitation
Virtual Reality System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263
Philippe S. Archambault, Nahid Gheidari Norouzi, Dahlia Kairy,
John M. Solomon, Mindy F. Levin
Modulatory Effect on Spinal and Supraspinal Responses during
Cognitive Attentional and Distraction Tasks . . . . . . . . . . . . . . . . . . . . . . . . 271
Federico Gabriel Arguissain, José Alberto Biurrun Manresa,
Carsten Dahl Mørch, Ole Kæseler Andersen
Equivalent Bilateral Early Latency Cutaneous Reflex Amplitudes
during Graded Contractions in Right Handers . . . . . . . . . . . . . . . . . . . . . . 279
Trevor S. Barss, Taryn Klarner, E. Paul Zehr
The Use of Ecological Sounds in Facilitation of Tool Use in Apraxia . . . . 289
Marta M.N. Bieńkiewicz, Philipp Gulde, Andrea Schlegel,
Joachim Hermsdörfer
Longitudinal Estimation of Intramuscular Tibialis Anterior
Coherence during Subacute Spinal Cord Injury: Relationship with
Neurophysiological, Clinical and Functional Measures . . . . . . . . . . . . . . . 295
Elisabeth Bravo-Esteban, Julian Taylor, Manuel Aleixandre,
Cristina Simon-Martínez, Diego Torricelli, José Luis Pons,
Julio Gómez-Soriano
Online Intramuscular EMG Decomposition with Varying Number of
Active Motor Units . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303
Eric Le Carpentier, Yannick Aoustin, Jonathan Monsifrot, Dario Farina

Inter-session Reliability of Robot-Measured Parameters for the


Evaluation of Upper Limb Recovery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 313
Ivana Cusmano, Roberto Colombo, Irma Sterpi, Alessandra Mazzone,
Carmen Delconte, Fabrizio Pisano
Reducing the False Positives Rate in a BCI System to Detect
Error-Related EEG Potentials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 321
Álvaro Costa, Enrique Hortal, Andrés Úbeda, Eduardo Iáñez,
José María Azorín
XII Contents

A Tool to Address Movement Quality Outcomes of Post-stroke


Patients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 329
Vincent Crocher, Justin Fong, Marlena Klaic, Denny Oetomo, Ying Tan
Characterization of a Dual PID-ILC FES Controller for FES-Robot
Control of Swing Phase of Walking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 341
Antonio J. del-Ama, Ángel Gil-Agudo, José Luis Pons, Juan C. Moreno
Physiological Recruitment of Large Populations of Motor Units Using
Electrical Stimulation of Afferent Pathways . . . . . . . . . . . . . . . . . . . . . . . . 351
Jakob Lund Dideriksen, Silvia Muceli, Strahinja Dosen, Dario Farina
Extending a Dynamic Muscle Model for Usage with Amputees . . . . . . . . . 361
Stefan Erber, Markus Schachinger, Thomas Mandl, Peter Michael Goebel
Measuring the Effectiveness of an Intensive Rehabilitation Treatment
on Balance Parameters in Patients with Parkinson’s Disease through
a Stabilometric Platform . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 369
Davide Ferrazzoli, Rossana Bera, Roberto Maestri, Gloria Perini,
Letizia Spina, Roberto Gargantini, Gianni Pezzoli, Giuseppe Frazzitta
Detection of Common Synaptic Inputs Shared by Populations of
Motor Neurons Innervating Different Muscles: Methodology and
Considerations for Neuroprosthetic Treatment of Tremor . . . . . . . . . . . . . 373
Juan Álvaro Gallego, Jakob Lund Dideriksen, Ales Holobar,
Juan Pablo Romero, Julián Benito-León, Félix Bermejo-Pareja,
José Luis Pons, Eduardo Rocon, Dario Farina
A Novel Robot-Aided Therapy for Shoulder Rehabilitation after
Stroke: Active-Assisted Control of the RehaArm Robot Using
Electromyographic Signals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 383
Clara Genna, Strahinja Dosen, Liliana Paredes, Andrea Turolla,
Bernhard Graimann, Dario Farina
Analysis of Eye Movements, Kinematics and Dynamic Aspects of
Performance during Activities of Daily Living in Stroke Patients . . . . . . . 393
Philipp Gulde, Charmayne Hughes, Manish Parekh, Martin Russel,
Manuel Ferre, Alan Wing, Marta M.N. Bieńkiewicz, Joachim Hermsdörfer

Historical Background from 1986 – 2005 for the Development of the


ActiGait System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 403
Jens Peter Haase, Morten Haugland, Thomas Sinkjær
Impact of Problem Solving Therapy on Brain Networks Associated
with Depressive Symptoms in Poststroke Older Adults . . . . . . . . . . . . . . . 405
Niloufar Niakosari Hadidi, Leah Jappe, Kathryn Cullen, Kay Savik
Contents XIII

Improved Detection and Force Decoding through Combined


Near-Infrared Spectroscopy and Electroencephalographic
Measurements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 411
Mia H. Hansen, Eric Kassebaum, Marlena A. Plocharska,
Mads Jochumsen, Ernest N. Kamavuako
Modeling the Functional Dependence of Stroke Patients:
The Outcome of an Improved Gait Training . . . . . . . . . . . . . . . . . . . . . . . . 421
Kristian Hennings, Sabata Gervasio, Ole Kæseler Andersen,
Erika Geraldina Spaich
Startling Acoustic Stimuli Elicit Rapid Hand Extension Following
Stroke . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 431
Claire F. Honeycutt, Ursina A. Tresch, Eric J. Perreault
Detection of the Onset of Voluntary Movements Based on the
Combination of ERD and BP Cortical Patterns . . . . . . . . . . . . . . . . . . . . . 437
Jaime Ibáñez, J. Ignacio Serrano, M. Dolores del Castillo,
Esther Monge, Francisco Molina, Francisco Rivas, Isabela Alguacil,
J. Miangolarra-Page, José Luis Pons
Flexible Thread-like Electrical Stimulation Implants Based on
Rectification of Epidermically Applied Currents Which Perform
Charge Balance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 447
Antoni Ivorra, Laura Becerra-Fajardo
High-Frequency Oscillations in Chemically Induced Spike-and-Wave
Epileptic Seizures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 457
Jianhang Jiao, Cristian Sevcencu, Kristian Rauhe Harreby, Winnie Jensen
Detection of Movement Intentions through a Single Channel of
Electroencephalography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 465
Mads Jochumsen, Imran Khan Niazi, Helene Rovsing,
Cecilie Rovsing, Gebbie A.R. Nielsen, Tina K. Andersen, Nhung P.T. Dong,
Marina E. Sørensen, Natalie Mrachacz-Kersting, Ning Jiang,
Dario Farina, Kim Dremstrup
A Standard Low-Cost Worldwide Accessible Nintendo Wii Balance
Test Can Differentiate Older Fallers from Non-fallers . . . . . . . . . . . . . . . . 473
Martin G. Jørgensen, Nicolas B. Hansen, Alberto L.R. Perez,
Erika Geraldina Spaich
Reliability of Multiple Baseline Measures for Locomotor Retraining
after Stroke . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 479
Taryn Klarner, Trevor S. Barss, Yao Sun, Chelsea Kaupp, Simone Beattie,
E. Paul Zehr
XIV Contents

Continuous Monitoring of Respiration during Rehabilitation . . . . . . . . . . 487


Marketa Kotova, Ludek Zalud, Jana Kolarova, Petr Dobsak
The Effects of Neuromuscular Electrical Stimulation on
Corticomuscular Coherence in Patients with Stroke . . . . . . . . . . . . . . . . . . 493
Meei-I Lai, Li-Ling Pan, Chung-Lan Kao, Mei-Wun Tsai, Shun-Hwa Wei,
Li-Wei Chou
Exercising the Tibialis Anterior Muscle of Children with Cerebral
Palsy for Improved Neuroplasticity Using an Electrical Guitar . . . . . . . . . 501
Jeppe V. Larsen, Thomas B. Moeslund, Dan Overholt
Feedback Strategies for BCI Based Stroke Rehabilitation: Evaluation
of Different Approaches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 507
Alexander Lechner, Rupert Ortner, Christoph Guger
A System for Real-Time Estimation of Joint Torque with Evoked
EMG under Electrical Stimulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 513
Zhan Li, Mitsuhiro Hayashibe, David Andreu, David Guiraud
Wheelchair Control with the Tip of the Tongue . . . . . . . . . . . . . . . . . . . . . 521
Eugen Romulus Lontis, Bo Bentsen, Michael Gaihede,
Lotte N.S. Andreasen Struijk
Information on Ankle Angle from Intramuscular EMG Signals
during Development of Muscle Fatigue in an Open-Loop Functional
Electrical Stimulation System in Rats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 529
Line E. Lykholt, Sahana Ganeswarathas, Anil K. Thota,
Kristian Rauhe Harreby, Ranu Jung
Frailty Assessment Based on Trunk Accelerometry during Walking . . . . 537
Ion Martinikorena, Alicia Martínez-Ramírez, Pablo Lecumberri,
Nora Millor, Marisol Gómez, Mikel Izquierdo
Increasing Voltage Transients Using Implanted Titanium Nitride
Neural Stimulation Electrodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 543
Suzan Meijs, Morten Fjorback, Søren Sørensen, Kristian Rechendorff,
Nico J.M. Rijkhoff
Frailty Detection Using the Instrumented Version of the 30-s Chair
Stand Test . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 553
Nora Millor, Pablo Lecumberri, Marisol Gómez, Alicia Martínez-Ramírez,
Mikel Izquierdo
Contents XV

An EMG Pattern Comparison of Exoskeleton vs. End-Effector


Robotic Device for Assisted Walking Training . . . . . . . . . . . . . . . . . . . . . . . 563
Giovanni Morone, Marco Iosa, Federica Tamburella, Luca Muzzioli,
Iolanda Pisotta, Juan C. Moreno, José Luis Pons, Stefano Paolucci,
Febo Cincotti, Marco Molinari
Effectiveness of Robotic Assisted Walking Therapy: The Role of Age
and Sex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 569
Giovanni Morone, Marco Iosa, Franco Marinozzi, Erika D’Antonio,
Patrizia Poli, Stefano Masiero, Marco Molinari, Stefano Paolucci
Cortical Contribution to Crossed Reflexes in Walking Humans . . . . . . . . 575
Natalie Mrachacz-Kersting, Sabata Gervasio, Dario Farina,
Thomas Sinkjær
On Electrode Configuration for Low-Back Peripheral Nerve Field
Stimulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 585
Carsten Dahl Mørch, Louis Vera-Portocarrero, Ken Steffen Frahm
Novel Approach for Investigation of Neuronal Alterations Following
Ischemic Stroke in a Rat Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 591
Rasmus Kragh Nielsen, Winnie Jensen
Modular Control of Gait in Incomplete Spinal Cord Injury:
Preliminary Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 601
Soraya Pérez-Nombela, Filipe Barroso, Diego Torricelli,
Julio Gómez Soriano, Ana de los Reyes-Guzmán,
Antonio J. del-Ama, José Luis Pons, Ángel Gil-Agudo
EEG-Based Classification of Imagined Arm Trajectories . . . . . . . . . . . . . 611
Patrick Ofner, Gernot R. Müller-Putz
Investigate the Changes of Motor Unit Recruitment Pattern after
Stroke Using Surface EMG . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 621
Pan Li-Ling, Lai Meei-I, Kao Chung-Lan, Tsai Mei-Wun, Wei Shun-Hwa,
Chou Li-Wei
Using Human-Computer Interface for Rehabilitation of Activities
of Daily Living (ADL) in Stroke Patients: Lessons from the First
Prototype . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 629
Johannes Pflügler, Andrea Schlegel, Emilie Jean-Baptiste,
Pia Rotshtein, Matteo Pastorino, Javier Rojo, Jose Maria Cogollor,
Maria Teresa Arredondo, Marta M.N. Bieńkiewicz, Joachim Hermsdörfer
Evaluation of a New Exoskeleton for Upper Limb Post-stroke
Neuro-rehabilitation: Preliminary Results . . . . . . . . . . . . . . . . . . . . . . . . . . 637
Elvira Pirondini, Martina Coscia, Simone Marcheschi, Gianluca Roas,
Fabio Salsedo, Antonio Frisoli, Massimo Bergamasco, Silvestro Micera
XVI Contents

Experimental Architecture to Analyse Brain Signals during Walking . . . 647


Daniel Planelles, Álvaro Costa, Andrés Úbeda, Eduardo Iáñez,
José María Azorín
Processing EEG Signals to Detect Intention of Upper Limb
Movement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 655
Daniel Planelles, Enrique Hortal, Eduardo Iáñez, Álvaro Costa,
José María Azorín
Preliminary Findings of Feasibility and Compliance of
Technology-Supported Distal Arm Training at Home after
Stroke . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 665
Gerdienke B. Prange, Sharon M. Nijenhuis, Patrizio Sale, Alfredo Cesario,
Nasrin Nasr, Gail Mountain, Farshid Amirabdollahian, Jaap H. Buurke
Exploring Relations between Functional Task Kinematics and Clinical
Assessment of Arm Function and Dexterity Post-stroke . . . . . . . . . . . . . . . 675
Gerdienke B. Prange, Sharon M. Nijenhuis, Stefanie M. Kersten,
Arno H.A. Stienen, J.S. Rietman
A Combined Interfascicular-Cuff Electrode (ICE) for Selective
Recruitment of Polyfascicular Peripheral Nerves Using Transversal
Stimulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 685
Alessandro Ranieri, Rasmus Elbæk Andersen, Mette Vandborg Lauridsen,
Kristian Rauhe Harreby
Integration of Neurodynamics into Neurorehabilitation . . . . . . . . . . . . . . 695
Carlos Rodríguez-López, Bibiana Da Rocha-Souto, Nora Kern
Movement Related Cortical Potentials and Sensory Motor Rhythms
during Self Initiated and Cued Movements . . . . . . . . . . . . . . . . . . . . . . . . . 701
Andrej Savić, Romulus Lontis, Ning Jiang, Mirjana Popović,
Dario Farina, Kim Dremstrup, Natalie Mrachacz-Kersting
Use of Dynamic Movement Orthoses as Rehabilitative Method to
Improve Gait Stability in Ataxic Patients . . . . . . . . . . . . . . . . . . . . . . . . . . . 709
Mariano Serrao, Alberto Ranavolo, Carlo Casali, Silvia Mari,
Carmela Conte, Francesco Draicchio, Giorgio Sandrini,
Francesco Pierelli
A Blood Pressure-Related Profile Extracted from Pig Left Vagus
Nerves Using Cuff Electrodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 717
Cristian Sevcencu, Thomas Nørgaard Nielsen, Johannes J. Struijk
Patient Satisfaction of Using the ActiGaitR
Drop Foot Stimulator
System and Effect of Treatment on Walking . . . . . . . . . . . . . . . . . . . . . . . . 725
Kaare Severinsen, Kurt Grey, Anne Juhl, Preben Soerensen, L. Oppel,
P.T. Birgit Larsen
Contents XVII

Augmentative and Assistive Communication in Patients of Locked-In


Syndrome: A Case Report . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 735
F.A. Purva Sharma, S.B. Yash Jobanputra
Validation and Test of a Closed-Loop Tele-rehabilitation System
Based on Functional Electrical Stimulation and Computer Vision for
Analysing Facial Expressions in Stroke Patients . . . . . . . . . . . . . . . . . . . . . 741
Daniel Simonsen, Ramin Irani, Kamal Nasrollahi, John Hansen,
Erika Geraldina Spaich, Thomas B. Moeslund, Ole Kæseler Andersen
Gait Orthosis Lokomat Combined with Functional Electrical
Stimulation for Foot Drop Correction: A Feasibility Study . . . . . . . . . . . . 751
Erika Geraldina Spaich, Mette F. Bøg, Ema Erkocevic, Anne Smidstrup,
Ole Kæseler Andersen, Jørgen Feldbæk Nielsen
Learning Effect of the Nintendo Wii Agility Test in
Community-Dwelling Older Adults . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 759
Erika Geraldina Spaich, Nicolas B. Hansen, Alberto L.R. Perez,
Martin G. Jørgensen
Functionality of the Contralateral Biceps Femoris Reflex Response
during Human Walking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 765
Andrew J.T. Stevenson, Svend S. Geertsen, Thomas Sinkjær,
Jens B. Nielsen, Natalie Mrachacz-Kersting
Rehabilitation Following Targeted Muscle Reinnervation in
Amputees . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 775
Agnes Sturma, Malvina Herceg, Birgit Bischof, Veronika Fialka-Moser,
Oskar C. Aszmann
Centre of Pressure Assessment in Subjects with Incomplete
Spinal Cord Injury: Preliminary Data of Reliability, Validity and
Effectiveness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 781
Federica Tamburella, Giorgio Scivoletto, Marco Iosa, Marco Molinari
A Functional Muscle Synergy for Forward Reaching . . . . . . . . . . . . . . . . . 789
Denise Taylor, J. Greg Anson
A Brain-Machine Interface Architecture to Control an Upper Limb
Rehabilitation Exoskeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 795
Andrés Úbeda, Daniel Planelles, Enrique Hortal, Francisco Resquín,
Aikaterini D. Koutsou, José María Azorín, José Luis Pons
Transcranial Direct Current Stimulation Enhances Propulsion during
Walking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 805
Edwin H.F. van Asseldonk
XVIII Contents

Design of a Subject-Specific EMG Model for Rehabilitation


Movement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 813
Michele Vivian, Luca Tagliapietra, Monica Reggiani, Dario Farina,
Massimo Sartori
A Pilot Study on Clinical and Neurological Effects of Neurofeedback
Training for Treatment of Central Neuropathic Pain . . . . . . . . . . . . . . . . . 823
Aleksandra Vuckovic, Muhammad A. Hasan, Matthew Fraser,
Bernie Conway, David B. Allan
Parametrization of an Exoskeleton for Robotic Stroke Rehabilitation . . . 833
Patrick Weiss, Georg Männel, Thomas Münte, Achim Schweikard,
Erik Maehle
Pelvic Support Mechanism for Training Dynamic Balancing and
Turning during Treadmill-Based Walking: A Pilot Study . . . . . . . . . . . . . 845
Matjaž Zadravec, Andrej Olenšek, Zlatko Matjačić

Innovation Session Papers


Feature Extraction APP for Pain Profiles . . . . . . . . . . . . . . . . . . . . . . . . . . . 853
Shellie A. Boudreau, Richard Spence, Georgi Vasov, Line L. Egsgaard

Marsi Bionics’ Wearable Exoskeletons for the Daily Rehabilitation of


Children . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 855
Elena Garcia, Nacho Barraque
A Poly-fascicular, In Vitro Nerve Model for Development and
Optimization of Peripheral Nerve Interfaces . . . . . . . . . . . . . . . . . . . . . . . . 859
Kristian Rauhe Harreby
Control of Robotic and Prosthetic Arms Using an Inductive Tongue
Control System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 863
Daniel Johansen, Dejan B. Popovic, Lotte N.S. Andreasen Struijk
A New Device for Measuring Body Part Movements and Stretches . . . . . 867
Michael Skovdal Rathleff, Line Rode, Ole Simonsen
Smattress: A Smart Mattress Providing an Active Unobstructive
Bedding System Based on Musculoskeletal Modeling . . . . . . . . . . . . . . . . . 869
Afshin Samani
Kinect-Based Tele-rehabilitation System for Hand Function . . . . . . . . . . . 871
Daniel Simonsen, John Hansen, Erika Geraldina Spaich,
Ole Kæseler Andersen
A New Method to Diagnose Neuromuscular Disorders in the
Neck-Shoulder Region . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 873
Steffen Vangsgaard, Ernst Albin Hansen, Pascal Madeleine
Contents XIX

Eir Innovation Sessions


How to Turn an Idea into a Commercial Success . . . . . . . . . . . . . . . . . . . . 877
Peter Mørch Eriksen
Industrial Perspectives on Innovation within Neurorehabilitation
between Private and Public Partners . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 879
Bernhard Graimann
Reflex-Based Electrical Therapy: A Novel Method for Gait
Rehabilitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 881
Kristian Hennings
The MedTech Industry at a Glance: Solving Tomorrow’s Healthcare
Challenges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 883
Louise Feilberg
Transferring Rehabilitation Technology to Markets: Lessons Learned
in the Past Ten Years . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 885
Zlatko Matjačić
Translational Research on Tongue Control Interface . . . . . . . . . . . . . . . . . 887
Gert Spender, Lotte N.S. Andreasen Struijk

Author Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 889


Role of Cortical Reorganization in the
Rehabilitation of Chronic Pain

Herta Flor

Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health,


Medical Faculty Mannheim, Heidelberg University,
Mannheim, Germany

The role of cortical plasticity has been in focus for years as the target for
efficient rehabilitation. But how large a role does it play? And how is it most
efficiently targeted to obtain lasting changes. What are the neural mechanisms
and when is the most optimal time window after an injury to the nervous
system. What is the role of sensory feedback to the deafferented brain and is
multisensory input more efficient. These questions will be addressed mainly
from the perspective of chronic pain, but these findings may also be
interesting for other areas of rehabilitation.
Neuroscientific evidence has shown that the adult brain is plastic into high age
even in areas that were formerly thought to be hard-wired after an early
adaptive phase. Injury but also stimulation and learning, including social
factors, thus modify the maps in the sensorimotor areas but also lead to changes
in centers involved in the processing of emotion, motivation and cognition. Two
developments have greatly enhanced the interest in brain-based rehabilitation
methods in the area of chronic pain. First, it was shown that changes in the
representation of body maps in the brain are highly related to both the
intensity and the chronicity of chronic pain, both, injury-related neuropathic
and stimulation-related musculoskeletal pain. Second, there is accumulation
evidence that the representation of the body can modify pain perception. Thus,
that there are great similarities between phantom perceptions and bodily
illusions such as the rabbit or the rubber hand illusions and other body-related
somatosensory phenomena such as supernumerary limbs or out of body feelings.
This research has also shown that the brain does not process the physical but the
perceived reality, which opens the door to manipulations of the perceived reality,
for example via brain computer interfaces or virtual reality applications, in both
research on the basis of these phenomena as well as neurorehabilitation.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 1


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_1, © Springer International Publishing Switzerland 2014
2 H. Flor

Cortical plasticity related to chronic pain can thus be modified by


behavioral interventions that provide feedback to the brain areas that were
altered in a maladaptive manner. Interventions include behavioral extinction,
mirror training, sensory discrimination and prosthesis training. More recent
advances include training in augmented and virtual reality, prostheses with
sensory feedback as well as neurostimulation and neurofeedback applications. In
many instances preventive measures can be taken, e.g. in the pre- and
postoperative phases of a surgical intervention. In addition, pharmacological
interventions designed to alter neuroplasticity can be used alone or in
conjunction with training methods. Detailed studies comparing the efficacy of
these interventions are still lacking but we can provide some initial
evaluations on useful interventions and combinations as well as the optimal
modes of application, much of it derived from extinction learning theory. We
also need better biomarkers and predictors of treatment outcome.
These approaches open new avenues for both the prevention and treatment
of chronicity and physical impairment.

References
Flor, H.: Psychological pain interventions and neurophysiology: Implications for a
mechanism-based approach. American Psychologist 69, 188–196 (2014)
Moseley, G.L., Flor, H.: Targeting cortical representations in the treatment of chronic pain
– rationale and current state of the art. Neurorehabilitation and Neural Repair 26, 646–
652 (2012)
Flor, H., Turk, D.C.: Chronic pain. An integrated biobehavioral approach. IASP Press,
Seattle (2011)
Induction of Cortical Plasticity: Clinical
Applications

Min-Fang Kuo, Walter Paulus, and Michael A. Nitsche

University Medical Center, Dept. Clinical Neurophysiology,


Georg-August-University, Robert-Koch-Str. 40, 37099 Goettingen, Germany
wpaulus@med.uni-goettingen.de

Abstract. Many neurological diseases are associated with adaptations of


cortical plasticity, trying to compensate for functional loss. Transcranial
stimulation techniques allow to up- or downregulate excitability of cortical
areas. Thus the more focal and close to surface cortical deficits are the more
prone they are to transcranially induced induction of cortical excitability. A
summary of possibilities will be given using rehabilitation of stroke induced
dexterity loss and aphasia as examples.

Motor Function

Both repetitive Transcranial Magnetic Stimulation (rTMS) or Transcranial


Direct Current Stimulation (tDCS) can enhance activation of the
dysfunctional or reduce activation of the healthy hemisphere(Nitsche and
Paulus, 2000) and therefore re- establish a closer to normal interhemispheric
balance. In chronic subcortical stroke patients, one session of anodal
excitability-enhancing tDCS over the primary motor cortex of the lesioned
hemisphere can improve fine motor skills of the upper limb, as tested by the
Jebson-Taylor task, during, and also for some time after stimulation
(Hummel et al., 2005), confirmed by applying excitability-diminishing cathodal
tDCS of the contralateral non-lesioned motor cortex (Fregni et al., 2005).
The same procedure, a single session of cathodal tDCS of the unaffected
hemisphere, facilitated motor learning of the paretic hand in chronic stroke
patients (Zimerman et al., 2012). Pinch force, performance of simple
reaction time tasks, and selective muscle contraction can also be improved by
anodal tDCS of the affected or cathodal stimulation of the unaffected motor
cortex (Hummel and Cohen, 2006, Hesse et al., 2007, Bradnam et al., 2012).
A combination of anodal tDCS with peripheral nerve stimulation generates
superior functional effects compared to each stimulation tool applied alone
(Celnik et al., 2009). Moreover, repeated cathodal stimulation for 5
consecutive days resulted in cumulative effects, while stimulation once weekly
over 4 consecutive weeks did not (Boggio et al., 2007). Thus, in line with other

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 3


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_2, © Springer International Publishing Switzerland 2014
4 M.-F. Kuo, W. Paulus, and M.A. Nitsche

data, a once daily session repeated at least over 3-5 days seems to be a
prerequisite for successful motor rehabilitation.
A whole group of studies was dedicated to the integration of tDCS into clinical
routine rehabilitation programs. Bilateral tDCS combining anodal tDCS of the
lesioned hemisphere with cathodal tDCS of the contralateral hemisphere during
physical/occupational therapy resulted in a better outcome of motor functions
than sham tDCS combined with therapy after 5 days of treatment. Interestingly,
only in the combined group functional magnetic resonance tomography
(fMRI) was increased after therapy. Prolongation of this regime to 10 days of
therapy resulted in stronger effects (Lindenberg et al., 2010, Lindenberg et al.,
2012).Later these findings were challenged(O'Shea et al., 2014). Similar effects
are described for bilateral and unilateral cathodal tDCS in combination with
constraint-induced movement therapy (Bolognini et al., 2011, Nair et al.,
2011). All of these studies were conducted in chronic stroke patients. In the
only study, in which the effects of anodal tDCS without combination with any
motor training, on motor functions in acute stroke patients was explored, tDCS
had no effects on motor outcome (Rossi et al., 2013).
With regard to lower limb function, increased force production during anodal
tDCS of the lesioned hemisphere (Tanaka et al., 2011), and improved
ankle control was described by anodal tDCS of the lesioned hemisphere
(Madhavan et al., 2011).
Taken together, these studies show a potential of tDCS to improve fine
motor skills, but also strength and selectivity of motor contraction, in chronic
stroke. This has been explored most extensively for upper limb functional
deficits, but also for lower limb and pharyngeal functions. Repetitive
application of stimulation results in cumulative effects, the effects can outlast
the therapeutic regimen for weeks, as far as explored, and can be associated
with enhanced activity and excitability of the lesioned hemispheres. So far it
is not clear which protocols are optimally suited to improve functions.
Approaches, such as combination of tDCS with peripheral nerve
stimulation, might enhance efficacy of stimulation further. Most of the studies
were conducted in small populations of selected patients, and larger studies are
needed to explore the relevance of the effects in more routine rehabilitation
settings.

Aphasia

Dependent on lesion location, i.e. involving Broca- and Wernicke areas, but also
temporal or parietal association cortices, and white matter, different kinds of aphasic
symptoms are discernible. During recovery rapid neuroplastic alterations of language-
related areas occur, which are associated with functional restitution (for reviews see
(Hamilton et al., 2011, Schlaug et al., 2011)). NIBS is an attractive approach to boost
the conventional rehabilitative approach of speech therapy (Ross et al., 2011, Holland
and Crinion, 2012). Similar to the motor system, an interhemispheric dysbalance
Induction of Cortical Plasticity: Clinical Applications 5

concept has been promoted for aphasia, beyond the rationale for direct plasticity
enhancement of the lesioned hemisphere. Therefore, reduction of excitability of the
healthy contralateral homolog area might indirectly enhance plasticity of the lesioned
one and thus improve regaining speech functions (Mylius et al., 2012).
In most of the studies conducted in aphasic stroke patients, anodal tDCS of
the left lesioned hemisphere was combined with speech therapy for up to 10
sessions. The anode was usually placed over the temporal or frontal cortex, and
the return electrode position was the contralateral supraorbital region (Baker et
al., 2010, Fiori et al., 2011, Fridriksson et al., 2011, Marangolo et al., 2011,
Vines et al., 2011). In general, stimulation improved speech function in these
patients. Moreover, the effects could remain stable for weeks or even
months. In the study of Monti and colleagues (Monti et al., 2008) only
cathodal tDCS of the lesioned hemisphere had a positive effect on picture
naming. The divergent result might be caused by specific stimulation protocol
differences as compared to the other studies, such as stimulation before therapy,
and return electrode position at the shoulder, which might have different
physiological effects due to different current flow direction (Moliadze et al.,
2010). Three studies following a different rationale, namely readjustment of
hemispheric dysbalance by cathodal tDCS of the healthy hemisphere,
demonstrated positive results (Jung et al., 2011, Kang et al., 2011, You et al.,
2011). Interestingly, it was most effective in patients with mild fluent
aphasia when the therapy started within 30 days after stroke (Jung et al.,
2011). In another positive study, anodal tDCS of the right frontal cortex was
combined with melodic intonation therapy, which involves activation of the
right prefrontal cortex (Vines et al., 2011). Taken together, these pilot studies
show that tDCS in combination with speech therapy is suited to enhance
speech function in aphasic patients. The most promising approaches encompass
excitability-enhancing stimulation of left-hemispheric language-related, and
excitability-reducing stimulation of the right hemispheric homolog areas
combined with speech therapy. However, systematic studies exploring
optimal stimulation protocols with regard to stimulation intensity, repetition
rate, electrode positions, which might differ also with regard to lesion location
and size, are needed as well as studies involving larger patient populations to
translate this approach into clinical practice.

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6 M.-F. Kuo, W. Paulus, and M.A. Nitsche

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Celnik, P., Paik, N.-J., Vandermeeren, Y., Dimyan, M., Cohen, L.G.: Effects of combined
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Fiori, V., Coccia, M., Marinelli, C.V., Vecchi, V., Bonifazi, S., Ceravolo, M.G.,
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improves word retrieval in healthy and nonfluent aphasic subjects. Journal of Cognitive
Neuroscience 23, 2309–2323 (2011)
Fregni, F., Boggio, P.S., Mansur, C.G., Wagner, T., Ferreira, M.J., Lima, M.C., Rigonatti,
S.P., Marcolin, M.A., Freedman, S.D., Nitsche, M.A., Pascual-Leone, A.: Transcranial
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Miniaturized Neural Interfaces and Implants
in Neurological Rehabilitation

Thomas Stieglitz

Laboratory of Biomedical Microtechnology,


The Department of Microsystems Engineering-IMTEK,
The Bernstein Center Freiburg and the Cluster of Excellence
BrainLinks-BrainTools (ExC 1086),
Albert-Ludwig–University of Freiburg, Freiburg, Germany
stieglitz@imtek.uni-freiburg.de

Abstract. Restoration of functions after trauma or neurological diseases is the


major goal of rehabilitation. Technical aids complement remaining functions or
even try to replace them completely. Neural prostheses use electrical signals
from the nervous system as control signals or excite nerves by means of
electrical stimulation to elicit perceptions, induce movements or modulate neural
network behavior. Creating novel, neural prostheses applications for the
peripheral or central nervous system require neural interfaces and implants that
are biocompatible, long-term stable and highly robust. However, only few neural
interfaces have been tested or are routinely used in clinical applications today,
most of them made with "old-style" precision mechanics technologies. What are
the biological, tech- nological, electrical and material science challenges that must
be considered when designing an optimal neural interface? Do nano-, micro-
and biohybrid systems have a future in clinical applications of neural
implants? Design aspects and opportunities and challenges of miniaturization
technologies for neural implants will be presented and discussed for peripheral
and central nervous system applications. Devices will be introduced and
compared with respect to selectivity, long-term functionality and their
applicability in funda- mental and translational research as well as for clinical
applications.

Keywords: neural implant, rehabilitation, recording, stimulation, miniaturization.

1 Introduction

Neural prostheses aim to restore or replace lost functions due to trauma or


neurological diseases. Since all neural functions in the human body come along
with electrical activity of the nerve cells, the idea arose decades ago to take
advantage of this property. Technical devices were invented to interface
nervous structures to read out or to inscribe or even overwrite electrical
information. Adequate interfaces are needed for this endeavor. They must

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 9


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_3, © Springer International Publishing Switzerland 2014
10 T. Stieglitz

neither harm the body nor lose their functionality over the course of the
application. The earliest clinical application that replaced lost neural activity
was the cardiac pacemaker. Its rise started in 1958 and it is the most
successful active implant nowadays with more than 350,000 new implantations
per year worldwide [1]. In neural prostheses or implants, only few success
stories have been written so far. Cochlear implants to restore hearing have been
implanted in about 250,000 patients worldwide. Deep brain stimulators to
treat symptoms of Parkinson’s (Lou Gehrig’s) disease symptoms as well as
vagal nerve and spinal cord stimulators modulate network activity by electrical
stimulation very successfully [1]. Implants to activate ankle flexion after brain
stroke, i.e. drop foot stimulators, and retinal vision prostheses have got
medical device approval in the EC and the USA but are still far from market
penetration. Recently, more applications have been developed in the field of
stroke rehabilitation, epilepsy diagnosis and treatment, psychia- tric disease
therapy, control of technical aids after para- lysis and artificial limbs after
amputation to list the main research lines. Some of them are on the way into
clinical practice, others still in different stages of fundamental research [1].
Further scientific findings are still needed to understand physiologic
function and pathophysiological changes in many diseases to develop an
“optimal” neural implant. On the other side, devices still look very “old-
fashioned” or “vintage-style” in most clinical applications. Which target
specifications have to be met to develop a new generation of neural interfaces
and implants with modern miniaturization technologies ? Starting with a
personal view on essential requirements of active implants, peripheral and
central nervous system interfaces will be introduced. Chemical and optical
interaction with the nervous system will be considered as alternative to
established electrical recording and stimulation techniques. System concepts
of implants that connect a kind of control center with its periphery conclude
the overview.

2 Essential Requirements

Implants must not harm the target tissue and need to establish a long-term
stable and functional interface. The technical term “biocompatibility”
summarizes the main requirements that a device shall meet [2]. The used
materials must not be toxic and shall interact with the tissue in a desired manner.
Shape and mechanical material properties determine the structural
biocompatibility that also influences the strength of the foreign body reaction.
Implants will be encapsulated by electrically insulating tissue (either glia or
fibroblasts) that deteriorates the recording and stimulation properties of the
interfaces. Safety of the implant also includes material stability, the absence of
eluates and debris and absence of tissue damage by (leakage) currents and
electrical shock beyond the intended use. All these aspects have to be
considered as fundament of application specific requirements.
Miniaturized Neural Interfaces and Implants in Neurological Rehabilitation 11

3 Interfaces to the Nervous System

The intended use as well as the implantation site determines the design of neural
interfaces. Invasiveness and selectivity in recording and stimulation have to be
well balanced [3]. Miniaturization helps to interface with few nerve cells or
axons but small electrode size results in increased noise and decreased charge
injection. A compromise has to be found for every application. Suitable materials
for implantable nerve interfaces include silicones, precious metals, polymers and
silicon [4-6].

3.1 Peripheral Nerve Interfaces


Electrode arrays have to interface the axons, arranged in fascicles in the
peripheral nervous system. For selective and graded recruitment, an electrode
array is mandatory to be able to address several subgroups of nerve fibers.
Electrodes can be wrapped around the nerve as cuff- electrodes or can be
inserted either between or inside the nerve fascicles [3-5]. Designs differ in
their designs according to electrode arrangement, shape, substrate and electrode
material [3-5]; polyimide, parylene C and silicone rubber have been established
as substrate materials while platinum, platinum iridium alloy, and iridium oxide
are common electrode materials. Precision mechanics, laser structuring and
microsystem technologies have been successfully applied to develop devices for
clinical trials and approved devices. Microsystem based intrafascicular
electrodes have shown highest selectivity in restoring natural sensory feedback
in hand prosthesis control [7]. Long-term stability of the thin-film-based
electrode contacts is of utmost importance [5] to transfer these promising
approaches in clinical practice.

3.2 Central Nervous System Interfaces


Electrode arrays are either placed inside the cortex or deeper structures of the
brain to record single unit activity or local field potentials or on or under the
meninges of the brain. Shaft-like electrode arrays are preferred for intra-
cortical implantations while planar arrays are suitable for epicortical application
[6]. While fundamental researchers prefer stiff silicon-based arrays to record
the activity of single nerve cells, chronic applications suffer from loss of active
channels and signal due to encapsulation of these devices [6]. Reasons of this
foreign body reaction include micromotions between the implant and the brain
tissue. Flexible probes could be a solution. Further investigations are needed to
prove reliability and long-term stability. In epicortical applications, increased
electrode densities and numbers help to better understand mechanisms in the
brain [8]. While polyimide-based microsystems [8] are success- ful in basic
research, silicone rubber is taken for clinical research because of experience
from other applications. Chronic stability and long-term functionality is the
12 T. Stieglitz

limiting factor from the technical side. More complex probes might lead to better
understanding of diseases and neural network activity that eventually leads to
better probes.

3.3 Non-electrical Interfaces


Electrical activity in the nervous system is not only based on distribution of
ions in the intra- and extracellular space but neurotransmitters influence nerve
cell activity and synaptic transmission. Therefore, monitoring of the chemical
environment, sometimes called metabolic monitoring, is of interest as well as
local drug delivery [9]. Integration of microfluidic channels can be done
technically but clogging due to protein and cell adhesion often limits the
usefulness in chronic applications as well as the size of pumps, valves and
reservoirs [9]. Opto- genetics takes advantage of the ability to genetically
modify nerve cells and to obtain light sensitive ion channels. It allows novel
investigation paradigms in basic research and needs adequate tools [10].
Microsystems engineering approaches are manifold to bring light to nerve cells
and record the electrical response. So far, all developments are more or less
in the prototype stage. Miniaturization, wireless communication and long-term
stability are still major tasks on the agenda.

3.4 Tailoring the Material-Tissue Interface


Tailoring the material-tissue interface to either mimic the biological
environment or to hide the technical substrate has a long history in implant
development. Basic research is done on nanostructuring the surface, biochemical
coatings, integration of cells onto or into coatings [11] and genetic engineering
of coatings [12] to influence the tissue reaction after implantation. Most
approaches, however, lack the ability to easily pass legal requirements in the
context of medical device approval, e.g. with respect to sterilization.

4 Implant Concepts

The cardiac pacemaker and the cochlea implant have set standards with respect
to reliability and robustness in (neural) implant concepts. They both protect
implant electronics in a hermetic package against water and ions. Energy
supply is either realized by a battery inside the package or a coil for wireless
electromagnetic energy transmission inside or outside the package [13-14].
Non- hermetic packaging of electronic components can be done for preclinical
studies or clinical studies with limited implantation time but might not be
stable over decades [13]. Hermetic packages include a (limited) number of
electrical feed-throughs that connect the electronic part inside with the electrodes
outside. In approved medical devices this number of feed-throughs is limited to
Miniaturized Neural Interfaces and Implants in Neurological Rehabilitation 13

about 20, so far. Current technology delivers packages at a certain size but has
been able to deliver long-term stable systems that survive about 10 years even in
parts of the body where motions are present [10]. Miniaturized implant
packages have to face the challenge of integrating hundreds of electrical feed-
throughs without deteriorating hermeticity. Ceramic-based packages in
combination with Laser- structuring and micromachining deliver solutions for
highly complex packages with predicted life-time exceed- ing human life
expectancy. In addition, novel measurement and validation techniques have to
be developed to over- come detection limits of established tests, e.g. the helium
leakage test, when certain package volumes are underrun. The major challenge
-according to the author’s personal opinion- lies in the development of high
channel-count connectors that allow reliable connection and detachment of the
different components of an implant. If multiple electrodes with cables and an
implant package with control electronics have to be implanted, detachable
connections might reduce implantation trauma due to smaller incisions and
tunnels. Single parts of an implant system might be replaced in case of failures
and variability of implant components, e.g. lengths of cables, can be better adapted
to the patient’s needs. Commercially available solutions are limited to one,
two, four and recently 8 channels for chronic implants. More sophisticated
solutions are needed to be able to take advantage of microsystems solutions, of
high channel count electrode arrays, and of complex system designs in chronic
applications. Instead of connec- tors, multiple distributed implants with body area
network communication to a central control implant can be envisioned as well as
extracorporal receivers in a distri- buted network integrated in clothes (i.e.
wearable elec- tronics). Intended use, application and patient numbers will
influence the final design while the benefit to the patients’ needs will determine
the success of the implant in neural rehabilitation applications.

5 Conclusions

Miniaturization technologies enable highly complex designs for interfaces and


implants in neural rehabilitation applications. Robustness and reliability of
devices are of utmost importance as well as the benefit for the patient to bring
exciting ideas into clinical applications. Long-term stability and functionality
of neural implants are still major challenges, especially in miniaturized devices,
that have to be solved before further success stories can be written.

Acknowledgment. Many parts of this work have been supported by German and
European grants: Bernstein Center Neuro-technology-The hybrid brain (BMBF-
01GQ0830), Cluster of Excellence BrainLinks-BrainTools (DFG, ExC 1086), Exist Go
Bio (BMBF-01GQ0420), FutureRet (BMBF--16SV3792), BrainCon (BMBF-0316064C),
NEURO- PROBES (FP 6, IST-027017), and TIME (FP 7, CP-FP-INFSO 224012). T.S.
thanks P. Fries for continuous support and discussion on central nervous system implants.
14 T. Stieglitz

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Record Neural Signals from the Cortex. Progr. Brain Res. 175, 297–315 (2009)
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Bidirectional Hand Prostheses. Sci. Transl. Med. 6(22), 222ra19 (2014)
[8] Bosman, C., et al.: Stimulus Selection through Selective Synchronization between
Money Visual Areas. Neuron 75(5), 875–888 (2012)
[9] Stieglitz, T.: Integration of Microfluidic Capabilities into Micromachined Neural
Implants. Int. J.of Micro-Nano Scale Transport 1(2), 139–158 (2010)
[10] Rubehn, B., et al.: A polymer-based microimplant for optogenetic applications:
design and first in vivo study. Lab on a chip 13(4), 579–588 (2013)
[11] Stieglitz, T.: Restoration of Neurological Functions by Neuro- prosthetic
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[12] Kim, Y.J., et al.: Genetically engineered bacteriophage delivers an anti-inflammatory
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[13] Stieglitz, T.: Manufacturing, Assembling and Packaging of Miniaturized Neural
Implants. Microsystem Technol. 16(5), 723–734 (2010)
[14] Guiraud, D., et al.: An Implantable Neuroprostheses for Standing and Walking in
Paraplegia: 5 Year Patient Follow Up. J. Neural Eng. 3(4), 268–275 (2006)
[15] Guiraud, et al.: Implanted functional electrical stimulation: case report of a paraplegic
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Neuroprosthetics: Past, Present and Future

Nitish V. Thakor

Biomedical Engineering Department, Johns Hopkins University


Baltimore, USA
and
Singapore Institute for Neurotechnology (SINAPSE) National University of Singapore,
Singapore
thakorju@gmail.com, sinapseinstitute.org

Abstract. There has been a remarkable convergence in recent years between the
biomedical fields of neuroscience and rehabilitation and engineering fields of
robotics and prosthetics. This “union” of complementary disciplines has
resulted in rapid advances in the robotics and rehabilitation technologies on one
hand, and utilization of brain interfaces and brain signals for targeting suitable
clinical applications on the other hand. This review will address the slow
progress in past, explosive recent developments, and the pending major future
challenges to take the science and technology to the patient. I \ review the
broad field for neuroprosthesis, from sensory (e.g. tactile) to motor (upper and
lower limb) as well as rehabilitation technologies in these fields. I conclude
with recent remarkable developments in the field of brain machine interface,
how these are impacting the development of neutrally controlled prosthesis and
also discuss the challenges of taking the technology to the market and eventually
to the patient.

1 Introduction
The field of prosthesis, orthotics, and rehabilitation has always served great
human need, and has been of steady interest to inventors and scientists for
centuries. Despite the interest, technological progress has only been
incremental. This technology has taken a major leap forward, thanks to major
initiatives such as the “Revolutionizing Prosthesis” program by the Defense
Advanced Research Project Agency (DARPA) in the USA. Emergence of the
field of brain computer interface (BCI) and brain machine interface (BMI) has
further revolutionized the framework, greatly shifting the research focus from the
limbs to the brain and the nervous system. Indeed, the field of neuroengineering
in general, and neuroprosthesis in particular, has captured the interest and
imagination of students and serious researchers. This review presents the current
explosive developments, both in the technology as well as the neural interface
and control, and finally summarizes the challenges still being faced and the
future directions for the field.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 15


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_4, © Springer International Publishing Switzerland 2014
16 N.V. Thakor

2 Robotics, Prosthetics, Orthotics

2.1 Robotics
Robotics is a broad, interdisciplinary field, with applications to industry, as well
as to the medical centers and defense institutions. Overlap and synergy of the
robotics field with the fields of prosthetics and orthotics is quite great,
particularly in the areas of mechatronics, or design of mechanisms for upper
and lower limb prosthetics/orthotics. Both fields also rely on sensing and
actuation to provide that extra perception to the robotic mechanisms and the
rehabilitation devices. While the driver for the robotics field is mostly industry
(and to some extent military and health care), the driver for the field of
rehabilitation and prosthetics/orthotics is the health care services, although
defense establishment has lately taken an interest in providing the extra research
support to spur the technology for the benefit of soldiers and wounded
warriors.

2.2 Prosthetics and Orthotics


The fields of prosthetics and orthotics, and here we refer only to upper and
lower limb systems, have arguably remained stagnant for decades, indeed the
past century; during that period developments mainly comprised the mechanisms
that were predominantly passive or body powered. Constraints of cost, fitting to
the human body, ability to power the devices, and acceptance by the disabled
individuals, have all combined to hold back the field. A combination of recent
technological leaps as well as government investment have made the
prosthetic/orthotic devices significantly more functional, and to help overcome
the adoption issues and make them affordable as well. Among the major
technological developments have been anthropomorphic, or human inspired
prosthetic arms and legs, as well as advanced materials and power sources.
These technologies and synergies between the fields of robotics and
prosthetics/orthotics have now shifted the focus from the mechanisms to their
control. While autonomous or body powered control has been the common
approach for robotics and prosthetics, respectively, more intuitive or natural
would be the approaches of using signals and information from the body, indeed
the brain, to control the mechanisms. Even here, sensing the proprioceptive or
body motions and forces, and muscle activity (electromyogram) are more
common. Only over the past decade or so, the more intuitive and, inevitably,
neural interface and control has been considered and received a great surge in
research interest. This is the emerging field of neuroprosthetics.
Neuroprosthetics: Past, Present and Future 17

3 Neuroprosthetics

The concept of neuroprosthetics comes from the fundamental idea that it is the
brain, or the nervous system, that controls the limbs, and indeed also receives the
sensory input and feedback. Thus, direct interface to the nervous system,
particularly the brain, may eventually afford the best means to communicate to
the prosthetic or orthotic device. As such, considerable research is now underway
to develop technologies for interfacing to the nervous system, whether the brain,
spinal cord or the peripheral nerves. Further elements of this research include
a) microelectrodes and sensors that are implanted in the nervous system, b) high
density low power integrated circuits for amplification, filtering, data and power
harvesting, c) fully packaged hermetically sealed systems that are
biocompatible, d) signal analysis to interpret the information from the neurons,
spinal cord or the nerves, and e) control algorithm to bi-directionally interface to
the prosthetic/orthotic mechanism.
As such, this review will consider different ways to interface to the
nervous system and emerging approaches to interface and control the
prosthetic/orthotic devices by direct signals from the nervous system.

3.1 Neural Interface


The neural interface essentially means microelectrodes and microelectronics that
interfaces to the nervous system.

Microelectrodes – Microelectrode technology makes it possible to record from


individual or population of neurons. The resulting neural spike or local field
potential signals can be used to create a point process model or a population
model of neurons working together to achieve a coordinated control of the
prosthesis. Microelectrodes are made using modern silicon or MEMS technology
and are now commercially available. However, new generations of high density
electrodes, using nanotechnology or unconventional or biocompatible materials
such as polymers or carbon are under development. Spinal cord and nerves,
however, require different approaches, as the electrodes may be both penetrating
or non-penetrating, and may need considerable flexibility along with the ability
to interface to coarse (such as nerve) or fine (such as fascicles) structures.

Sensors – With the recent interest in providing sensory feedback to the nervous
system, the need to develop sensors for prostheses has become all the more
relevant. Human limbs benefit from tactile, proprioception, pressure/force,
temperature, and pain. Modern prostheses are incredibly limited in all these areas,
adopting only some modest research ideas and commercial tactile sensor
technologies. Even greater problem and concern is how to interface these
sensors, or sensory signals to the nervous system. Indeed, the most common
18 N.V. Thakor

and highly limited approach is to sensory feedback is through electrical


stimulation to the nerves or the sensory cortex.

VLSI circuits – Very large scale integrated (VLSI) are highly integrated circuits
that incorporate a large number of amplifier and interface electronics on single or
few chips. These chips interface to microelectrode arrays to transduce the
electrical signals. Critical circuit components include amplifiers interfacing to
electrodes to capture neural spike activity or to brain tissue to capture the local
field potentials. To provide feedback, electrical stimulation is given to
peripheral nerves or directly to the sensory cortex, resulting in a sensory percept.
This requires multi-channel stimulator with biphasic pulse output and high
voltage compliance if interfaced to muscles.
Power and data transfer – Implanted systems need their own power for
considerable lengths of time that the implant might last (indeed, prostheses may
last decades). Traditional option for powering is to use implanted Lithium-
based batteries which can last several years. But for even more extended
periods lasting decades, or when size is of serious concern, wireless power
transfer or continuous power harvesting may be needed. Various radio-
frequency and inductive powering approaches are therefore used. When the
neural interface is implanted chronically, it also captures a great deal of data
continuously. These data (from neuronal spike activity to nerve signals) must be
processed continuously and in real- time, a capability that stretches the current
implantable signal processing technology. Therefore, another option is to
wirelessly transfer data from within the cortex to outside, or bidirectionally, that is
if stimulation is also provided by the signal processor.

System integration – Last but not the least, this hardware must be fully integrated
into an implantable package. Key features of the implanted system are to
provide hermetically sealed package (providing protection to the sensors and
electronics) and biocompatibility (to make the implant acceptable to the body).
Very few materials, such as Platinum metal for electrodes, silicones and
ceramics, and Titanium can for hermetically sealing, have proven track record
and regulatory approval. Therefore, full system integration and packaging
remains a major barrier to taking various research products to commercial and
clinical practice.

3.2 Neural Signal Analysis and Control


Signals from brain – Neural signals, as eluded to earlier, include neuronal spike
activity (single or multiunit) recorded by an array of microelectrodes. Thus,
the signal processing involves detection and sorting of neural spikes as well as
building a model of the inter-spike interval distributions. From this
distribution, or a point-process model of the spiking activity, a generalized
model is created to determine what the neural activities code for, e.g. movement,
Neuroprosthetics: Past, Present and Future 19

direction, velocity or force of the intended limb movement. It is also possible to


work with local field potentials to achieve the same goal, although not as
effectively (these potentials, though, may be more robust over long term).

Signals from nerves and spinal cord – While cortical prostheses have
garnered a great deal of attention, prostheses controlled by signals from nerves or
the spinal cord also serve special needs. Nerve interfaces are arguably less
traumatic or invasive, e.g. nerve prostheses would not require brain surgery, and
may be used to decode the target signals carried to the muscles. Nerves also
carry sensory signals back and thus decoding signals from the nerve or its
fascicles can provide an indicator of tactile or other sensory information. Spinal
signals are arguably much more difficult to tap into, not only because they are
difficult to access through the vertebra but also due to the very complex
organization of the spinal cord. Tapping into ganglia out of the spinal cord may
be an option.

3.3 Applications
Cortical control: motor prosthesis and sensory feedback – Building motor
prostheses is the most popular, vibrant area of research. Application of neural
interface and signals to control prosthetic limbs has now been demonstrated
in animal models and human subjects. Microelectrodes are implanted (most
commonly this research is done on non- human primates) in the motor and the
premotor cortex and neural spikes or local field potential signals are decoded to
predict the end point or the trajectory of the movement. Neural decoding and
algorithms are trained or adapted, but it has also been shown that neurons
adapt their output under reinforced learning to achieve the desired end point or
trajectory. In nonhuman primates as well as human subjects, different
decoding results such as reach and grasp of objects has been demonstrated.
Researchers continue to enhance the degrees of freedom, i.e. complexity of
movements (such as different grasps) and increasing the speed and precision.
Research on sensory prosthesis, i.e. getting the sensory information back to
brain is less well advanced but preliminary work indicates that
microstimulation of the cortex may provide some sensory percepts and may be
used to provide feedback for object reach and grasp. Much additional work is
needed to provide high-resolution sensory feedback of object shape or texture,
or other senses such as proprioception (instantaneous positional feedback).

Spinal interface for prosthetic or assistive locomotion – Spinal cord injury


results in devastating consequences potentially resulting in paralysis and life
long impairment of limb function - most vivid is the paralysis that impairs
locomotion. To restore locomotion, it would be necessary to provide some motor
command pertaining to the intended movement from the brain to the limb
muscles. These signals may be tapped directly from the cortex (motor
20 N.V. Thakor

command signals encoded by neurons) or from the spinal cord (such as the
central pattern generator oscillator signals pertaining to locomotion). Using
microstimulation, it has been shown in rodent and cat models that such
locomotion signals can also be activated. Very early, preliminary evidence of
the beneficial effects microstiulation on restoring some degree of locomotion
has also been demonstrated.

Peripheral nerve interface: motor and sensory– Peripheral never injury commonly
results from accidents and once the nerve is severed, corresponding muscle
atrophies and despite the limb being intact loss of limb function occurs.
Interfacing to the intact end of the peripheral nerve may allow us to tap into
the neural signals coding for the intended movement. Microelectrodes may be
inserted longitudinally or transversely into the nerve to capture the signals from
the nerve fascicles. A less invasive, although less specific, approach is to put
an electrode cuff around the nerve to be monitored. Although the nerve interface
is may appear to be less invasive than the cortex, that connection is also
harder to maintain and decode due to small nerve fiber size, its movement
along with the limb, and the complex nature of nerve fascicles and axons.
Nevertheless, some degree of decoding may be possible to elicit a command
signals to use for functional electrical stimulation of the limb and achieve
some level of functional response. Sensory feedback requires a reversal of the
process; seeking input from sensors on the limb (such as tactile sensors
mounted on the hand) and stimulating the nerve to provide some degree of
sensory perception. This type of sensory feedback, as of now, is quite
experimental and only some crude mapping of perception of touch on the hand
has been demonstrated.
Nerve signals are quite small and are difficult to get capture and decode.
However, when nerves innervate muscles, that interface results in an
amplification of the nerve signals when the muscle contracts producing the
electromyogram. Thus, artificial peripheral nerve innervation may provide an
indirect means of tapping into the nerve signals, i.e. by interpreting the innervated
muscle an estimate of the motor command carried by the nerve can be obtained
from the muscle contracture. Put it other way, when there is a loss of limb, the
reinnervated muscle provides the signature of the intended motor function,
which can then be relayed to the prosthetic limb. This approach, called
targeted muscle reinnervation, has been a very successful, rapidly gaining
clinical acceptance due to its effectiveness, despite the rather invasive and
complex nature of the interface and the overall technology.

4 Discussion and Conclusion

Prosthetics and orthotics technologies substitute for or augment the natural


human limb function. To function as a natural extension of the human body,
these devices need an intuitive and naturalistic human-like – meaning cortical or
Neuroprosthetics: Past, Present and Future 21

cognitive - interface. This need has spawned the field of neuroprosthesis and
neuroorthosis. Current research is at the demonstrative phase, suggesting
through work in rodent or nonhuman primate models that neural control of an
arm or a leg is possible by tapping into the cortical neurons, spinal cord, or
peripheral nerve. Pioneering studies in humans have also been carried out,
demonstrating the feasibility of this approach.
The technology of neural interface, from microelectrode arrays to VLSI
circuits is advancing rapidly. Higher density recording, coupled with better
decoding algorithms may provide better signature of the brain’s intent and
correspondingly control of the prosthesis. These technologies need further
refinement and integration in chronically implanted systems so that long
term performance, both recording and stimulation can be demonstrated. For
long term implantation, the electrode- brain tissue interface needs to be
improved. Major barriers that remain, including demonstrating chronic
reliability and biocompatibility, demonstrating safety and efficacy, and
obtaining regulatory approvals, ethical considerations of carrying out clinical
trials and balancing the risk and reward, and formulating a suitable business
model including scale up, cost effectiveness and reimbursement.
Future research should focus on greatly enhancing the functionality and
bidirectional intuitive interface that restores limb function over the life-time
of the subject. Motor prostheses need to be more continuous and show higher
level of functionality, such as for dexterous manipulation. Sensory prostheses
need to carry information other than tactile to include other sensory percepts.
Fully integrated bidirectional prosthesis is close to demonstrability but far from
ubiquitous use by amputees and disabled. Some of the challenges are
technical, however greater challenge is to carry out quality experimental studies
and clinical trials to demonstrate the feasibility and performance pertaining to
the use of neuroprosthesis by the disable in their daily living.
Continuing research, technological refinement, and extended experimental
and clinical validation, including patient safety and effectiveness will be
needed to brain neural prosthesis to wide spread clinical realization. High level
of interest and creativity shown by researchers, and considerable progress over
the past decade, however, bodes well for the field.

Acknowledgment. My research over the past decade has been funded by the
U.S. Defense Advanced Research Project Agency, the National Institutes of
Health, the National Science Foundation, and presently the Singapore Institute
for Neurotechnology and the National Research Foundation of Singapore.
Neuroplasticity in Constraint-Induced
Movement Therapy

Jakob Udby Blicher1,2, Jamie Near3, Erhard Næss-Schmidt2, Leif Østergaard1,


Heidi Johansen-Berg4, Charlotte J. Stagg4, Jørgen Feldbæk Nielsen2,
and Yi-Ching Lynn Ho1
1
Center for Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmark
2
Hammel Neurorehabilitation & Research Centre, Aarhus University Hospital,
Hammel, Denmark
3
Dept. of Psychiatry, McGill University, Montreal, QC, Canada
4
Oxford Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of
Clinical Neurosciences, University of Oxford, UK

Background: In healthy subjects, decreasing GABA facilitates motor learning[1].


Recent studies, using PET[2], TMS[3-5], and pharmacological challenges[6], have
pointed indirectly to a decrease in neuronal inhibitory activity after stroke.
Therefore, we hypothesize that a suppression of GABA levels post stroke might
be beneficial to motor recovery during Constraint-Induced Movement Therapy
(CIMT).

Objective: To relate GABA changes to motor relearning after stroke through the
use of j-difference edited Magnetic Resonance Spectroscopy (MRS).

Methods: 21 patients (3-12 months post stroke) and 21 healthy, age-matched


subjects were recruited. Patients had mild to moderate hand impairment, with at
least 10° of active wrist extension, at least 10° of thumb abduction/extension, and
at least 10° of extension in at least two additional digits. Patients were examined
by a medical doctor and a physiotherapist prior to enrollment in the study. Patients
completed two weeks of CIMT, and were scanned before and after training.
For MRS a 2x2x2 cm voxel was placed on the “hand knob” (hand area located in
the primary motor cortex[7]) in the affected hemisphere of the patients and in the
dominant hemisphere of the healthy subjects. GABA was expressed as a ratio to
Creatine (Cr). Motor function was measured using the Wolf Motor Function Test
(WMFT)[8].

Results: GABA/Cr was significantly lower (p< 0.001) in patients (0.33) at


baseline compared to healthy subjects (0.42). After therapy, patients showed a
significant improvement in hand function (p< 0.001), which was negatively
correlated with GABA/Cr changes (R=-0.57 , p=0.015) – larger improvements in
patients were associated with greater reductions in GABA/Cr. Results were also
significant after correcting for changes in intracortical grey matter volume.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 23


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_5, © Springer International Publishing Switzerland 2014
24 J.U. Blicher et al.

Conclusion: A decrease in GABA levels appears to facilitate motor recovery after


stroke. GABA, as measured non-invasively with MRS, could be a biomarker for
neuronal plasticity during post stroke recovery and guide rehabilitation
interventions as transcranial direct current stimulation[9].

References
1. Stagg, C.J., Bachtiar, V., Johansen-Berg, H.: The role of GABA in human motor
learning. Curr. Biol. 21, 480–484 (2011)
2. Heiss, W.D., Grond, M., Thiel, A., et al.: Permanent cortical damage detected by
flumazenil positron emission tomography in acute stroke. Stroke 29, 454–461 (1998)
3. Liepert, J., Storch, P., Fritsch, A., Weiller, C.: Motor cortex disinhibition in acute
stroke. Clin. Neurophysiol. 111, 671–676 (2000)
4. Swayne, O.B., Rothwell, J.C., Ward, N.S., Greenwood, R.J.: Stages of motor output
reorganization after hemispheric stroke suggested by longitudinal studies of cortical
physiology. Cereb Cortex 18, 1909–1922 (2008)
5. Blicher, J.U., Jakobsen, J., Andersen, G., Nielsen, J.F.: Cortical Excitability in Chronic
Stroke and Modulation by Training: A TMS Study. Neurorehabil. Neural Repair 23,
486–493 (2009)
6. Lazar, R.M., Berman, M.F., Festa, J.R., Geller, A.E., Matejovsky, T.G., Marshall, R.S.:
GABAergic but not anti-cholinergic agents re-induce clinical deficits after stroke. J.
Neurol. Sci. 292, 72–76 (2010)
7. Yousry, T.A., Schmid, U.D., Alkadhi, H., et al.: Localization of the motor hand area to
a knob on the precentral gyrus. A new landmark. Brain 120(Pt. 1), 141–157 (1997)
8. Wolf, S.L., Lecraw, D.E., Barton, L.A., Jann, B.B.: Forced use of hemiplegic upper
extremities to reverse the effect of learned nonuse among chronic stroke and head-
injured patients. Exp. Neurol. 104, 125–132 (1989)
9. O’Shea, J., Boudrias, M.H., Stagg, C.J., et al.: Predicting behavioural response to TDCS
in chronic motor stroke. Neuroimage (2013)
Advanced Prosthetic Control in Transhumeral
Amputees Using Osseointegration and
Bidirectional Neuromuscular Interfaces

Rickard Brånemark

Integrum Company,
Gothenburg, Sweden

Abstract. Bidirectional neuromuscular interfaces have been permanently


implemented in a patient using an osseointegrated percutaneous implant system.
Preliminary results from the first year of use will be presented.

1 Introduction

Although myoelectric prostheses have been clinically implemented since the


1960’s, they are still far from the functionality of their biological counterpart. It is
a widely known fact that the lack and instability of physiologically appropriate
control signals are the bottleneck of the field. Implantable neuromuscular
interfaces could provide enough and long-term stable signals [1], however, the
permanent communication with implanted devices is a major constraint that has
hindered this solution for decades. In order to overcome this problem, we have
developed a permanent bidirectional interface into the human body, the
Osseointegrated Human-Machine Gateway (OHMG).

2 Method

The OHMG is an enhancement of the OPRA Implant System [2], which is a


percutaneous osseointegrated implant for treatment of amputees. It has a modular
design that allows customization of the neuromuscular interfaces according to the
patient’s anatomy and prosthetic needs (Figure 1). It initially comprises epimysial
and cuff electrodes combinations, which account for up to 12 contacts. The
recording features of the cuff electrodes have been optimized in a frog sciatic
nerve model [3]. Furthermore, analog electronics and advanced control strategies
based in pattern recognition have been developed (BioPatRec) [4].

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 25


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_6, © Springer International Publishing Switzerland 2014
26 R. Brånemark

Fig. 1 The Osseointegrated Human-Machine Gateway (OHMG), an enhancement of the


OPRA Implant system [2]. Animation to illustrate the concept at:
http://youtu.be/w8hlziytLkM.

3 Results

Preliminary clinical results show that the OHMG has the potential to allow
permanent access to implanted electrodes, and once validated, it will open new
possibilities for more advanced and natural prosthetic control. Long-term clinical
studies are required to prove the benefits of implantable interfaces in prosthetic
control. The early clinical results from the OHMG study will be reported.

4 Conclusion

For the first time bidirectional neuromuscular interfaces have been implemented in
a patient for the daily control of the arm prosthesis in activities of the daily living;
that is without being confined inside a research laboratory. The patient has been
using the system for over one year without complications, thus demonstrating the
potential of this novel technology to improve rehabilitation of individuals with arm
amputations.

Acknowledgment. This project was funded by ALF, Vinnova, Västra Gotalandsregionen,


Connacyt, Integrum, and Promobilia.
Advanced Prosthetic Control in Transhumeral Amputees 27

References
[1] Ortiz-Catalan, M., Brånemark, R., Håkansson, B., Delbeke, J.: On the viability of
implantable electrodes for the natural control of artificial limbs: Review and
discussion. Biomed. Eng. Online 11, 33 (2012)
[2] Brånemark, R., Berlin, Ö., Hagberg, K., Bergh, P., Gunterberg, B., Rydevik, B.: A
novel osseointegrated, percutaneous prosthetic system for treatment of patients with
transfemoral amputation: A prospective study of 51 patients. Bone Jt. J. 96-B(1), 106–
113 (2014)
[3] Ortiz-Catalan, M., Marin-Millan, J., Delbeke, J., Håkansson, B., Brånemark, R.: Effect
on signal-to-noise ratio of splitting the continuous contacts of cuff electrodes into
smaller recording areas. J. Neuroengineering Rehabil. 10, 22 (2013)
[4] Ortiz-Catalan, M., Brånemark, R., Håkansson, B.: BioPatRec: A modular research
platform for the control of artificial limbs based on pattern recognition algorithms.
Source Code Biol. Med. 8, 11 (2013)
The Control of Interlimb Coordination during
Left-Right and Transverse Split-Belt
Locomotion in Intact and Spinal
Cord-Injured Cats

Alain Frigon, Yann Thibaudier, Marie-France Hurteau, Alessandro Telonio,


Charline Dambreville, and Victoria Kuczynski

Université de Sherbrooke, Sherbrooke, Qc J1H 5N4 Canada


{alain.frigon,marie-france.hurteau,alessandro.telonio,
charline.dambreville}@usherbrooke.ca,
thibaudiery@hotmail.com, vkuczynski10@ubishops.ca

Abstract. Proper coordination of the four limbs, or interlimb coordination, is a


fundamental requirement for locomotion in terrestrial mammals. The control of
interlimb coordination during quadrupedal locomotion was studied in adult cats by
independently controlling the speed of the left and right sides, or of the fore- and
hindlimbs, using a treadmill with four independent running surfaces. Here, we
briefly present some of our recent findings pertaining to the control of interlimb
coordination during quadrupedal locomotion in intact and spinal cord-injured
adult cats.

1 Introduction
Precise and flexible coordination of the four limbs (i.e. interlimb coordination) is a
fundamental requirement for quadrupedal or bipedal locomotion. Maintaining
dynamic stability in a changing environment requires constant adjustments in
interlimb coordination. Despite its importance, the neural control of interlimb
coordination in mammalian systems is largely unknown, although genetic
manipulations in mice have begun to identify some of the neuronal populations
involved [1,2]. It has been well documented that humans have conserved a
quadrupedal-like control of interlimb coordination during bipedal walking [3,4].
As such, studies in quadrupedal terrestrial mammals that walk on all four limbs,
such as the cat, are appropriate and useful translational models to uncover
neurophysiological and biomechanical mechanisms involved in the control of
interlimb coordination during human locomotion. To study interlimb coordination
during locomotion, we recently devised a series of experimental paradigms
whereby the speeds of the left and right sides [5] or of the fore- and hindlimbs [6]
were independently controlled, respectively. Here, we briefly review recent
findings during left-right (i.e. unequal speeds for the left and right sides) and
transverse (i.e. unequal speeds for the fore- and hindlimbs) split-belt locomotion
paradigms in intact and spinal cord-injured cats.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 29


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_7, © Springer International Publishing Switzerland 2014
30 A. Frigon et al.

2 Methods

2.1 Animals and Surgical Procedures


All procedures were approved by the Animal Care Committee of the Université de
Sherbrooke and were in accordance with policies and directives of the Canadian
Council on Animal Care. Before and after experiments, animals were housed and
fed within designated areas. Five adult cats (1 male, 4 females) weighing between
3.5 and 7.7 kg were used. Cats were trained to walk on an animal treadmill with
four independently controlled running surfaces 120 cm long and 30 cm wide
(Bertec Corporation, Columbus, Ohio). A Plexiglas separator (120 cm long, 3 cm
high, 0.5 cm wide) was placed between the left and right belts for left-right split-
belt locomotion. Two Plexiglas separators (120 cm long, 50 cm high) were also
placed 30 cm apart to constrain the animal to walk with the left and right sides
separately on the two belts during left-right split-belt locomotion or at the midline
between the front and rear belts on the left side of the treadmill for transverse split-
belt locomotion. Cats were given food and affection as reward.
Implantation and spinal transection surgeries were performed under aseptic
conditions in an operating room with sterilized equipment. Prior to surgery, the cat
was sedated with an intramuscular (i.m) injection of Butorphanol (0.4 mg/kg),
Acepromazine (0.1 mg/kg), and Glycopyrrolate (0.01 mg/kg). Induction was done
with Ketamine/Diazepam (0.11 ml/kg in a 1:1 ratio, i.m.). Once anesthetized, the
cat was quickly intubated with a flexible endotracheal tube and anesthesia was
maintained by adjusting isoflurane concentration as needed (1.5 - 3%). The fur
overlying the back, stomach, and hindlimbs was shaved with electric clippers and
loose hair was vacuumed. The level of anesthesia was confirmed and adjusted
throughout the surgery by monitoring cardiac and respiratory rates, by applying
pressure to the paw to detect limb withdrawal, and by assessing jaw tone. Body
temperature was monitored using a rectal thermometer. In two cats (2 females), the
spinal cord was completely transected (i.e. spinalized) at low thoracic levels. A
small laminectomy was performed between the junction of the 12th and 13th
vertebrae, the dura was removed, and after local lidocaine application (Xylocaine,
2%), the spinal cord was transected with surgical scissors. Hemostatic material
(Surgicel) was inserted within the gap, and muscles and skin were sewn back to
close the opening in anatomic layers.
For electromyography (EMG), pairs of Teflon insulated multistrain fine wires
(AS633; Cooner wire, Chatsworth, CA, USA) were directed subcutaneously from a
head-mounted 24 pin connector (Hirose Electric Co Ltd) and sewn into the belly of
selected hindlimb and forelimb muscles for bipolar recordings. During surgery an
antibiotic (Convenia, 0.1 ml/kg) was injected subcutaneously and a transdermal
fentanyl patch (25 mcg/hr) was taped to the back of the animal 2-3 cm from the
base of the tail. During surgery and approximately seven hours later, another
analgesic (Buprenorphine 0.01 mg/kg) was administered subcutaneously. After
surgery, cats were placed in an incubator and closely monitored until they regained
consciousness.
The Control of Interlimb Coordination during Left-Right and Transverse Split-Belt 31

For the spinalized cats, the bladder was manually emptied 1–2 times each day.
The hindlimbs were frequently cleaned by placing the lower half of the body in a
warm soapy bath. After a few days, cats were trained 5 times a week to walk on the
treadmill. Early after spinalization, training consisted of two experimenters moving
the hindlimbs over the moving treadmill belt to simulate locomotion with similar
joint kinematics and paw contacts while the forelimbs were positioned on a fixed
platform located ∼1 cm above the belt. After a few days, the skin of the perineal
region was stimulated to evoke stepping movements. A Plexiglas separator was
placed between the hindlimbs to prevent them from impeding each other because of
increased adductor activity. Initially, the experimenter supported the hindquarters
by lifting the tail. Recording sessions started once the animals attained a stable
locomotor pattern with full weight bearing and consistent plantar foot placement.
The experimenter provided equilibrium by holding the tail.

2.2 Experimental Paradigms


Left-right split-belt locomotion: Each cat performed two sessions that consisted of
several episodes of tied-belt (i.e. equal speeds for the left and right sides) and left-
right split-belt locomotion. In spinalized cats only the hindlimbs moved, with the
forelimbs on a fixed platform. During tied-belt locomotion, speeds ranged from 0.3
to 1.0 m/s in 0.1-m/s increments. During left-right split-belt locomotion, one side
walked at a constant speed of 0.4 m/s, 0.5 m/s or 0.6 m/s while the other side varied
its speed from 0.3 to 1.0 m/s in 0.1-m/s increments. Episodes of tied-belt or left-
right split-belt locomotion at the different speeds were presented randomly from
one session to another and approximately 30 seconds of rest were given between
episodes. Each episode lasted approximately 20 s to obtain 10-15 cycles. Left and
right treadmill speeds were increased with an acceleration of 0.1 m/s and data
collection started when the desired speeds were attained.

Transverse split-belt locomotion: Each cat performed five sessions of several


locomotor episodes in five conditions: (1) fore- and hindlimbs walking at equal
speeds (i.e. tied-belt locomotion) from 0.4 m/s to 0.8 m/s in 0.1-m/s increments; (2,
3) forelimbs walking at a constant speed of 0.4 m/s or 0.8 m/s with the speed of the
hindlimbs increasing from 0.4 to 0.8 m/s in 0.1-m/s increments; (4, 5) hindlimbs
walking at a constant speed of 0.4 m/s or 0.8 m/s with the speed of the forelimbs
increasing from 0.4 to 0.8 m/s in 0.1-m/s increments. In a few sessions, faster
speeds (up to 1.4 m/s) were used to evaluate the effects of increasing the speed
difference between the front and rear belts. Only episodes where the animal had its
forelimbs and hindlimbs on their respective belts were retained for analysis. Each
episode lasted approximately 20 s to obtain 10-15 cycles. Front and rear treadmill
speeds were increased with an acceleration of 0.1 m/s and data collection started
when the desired speeds were attained.
32 A. Frigon et al.

2.3 Data Acquisition and Analysis


Videos of the left and right sides were captured with two cameras (Basler AG) at
60 frames per second. A custom-made Labview program acquired the images and
synchronized the cameras. Videos were analyzed off-line. Cycle duration was
measured from successive paw contacts. Paw contact was defined as the first frame
where the paw made visible contact with the treadmill surface. Stance duration
corresponded to the interval of time from paw contact to the most caudal
displacement of the paw relative to the hip or the shoulder, while swing duration
was measured as cycle duration minus stance duration.

3 Results

3.1 Left-Right Split-Belt Locomotion


One form of adjustment in interlimb coordination occurs when walking along a
circular path, where the outer leg must walk faster than the inner leg [7]. One way
to simulate some features of circular path walking is by independently controlling
the speed of the left and right sides (i.e. left-right split-belt locomotion). During
left-right split-belt locomotion, the stance and swing phases on the slow side are
increased and decreased, respectively, while the stance and swing phases on the
fast side are decreased and increased, respectively [5,8,9]. We recently studied
bilateral changes in hindlimb stance and swing phases by measuring the slopes of
the linear regressions between stance duration and cycle duration (rSTA) and
between swing duration and cycle duration (rSW) during left-right split-belt and
tied-belt (i.e. equal speeds on left and right sides) locomotion in intact and chronic
spinalized adult cats [5]. The slopes of the regressions between the phases and
cycle duration quantify how the stance and swing phases vary as a function of cycle
duration. During tied-belt locomotion, rSTA was significantly greater than rSW
bilaterally, as shown previously [10,11]. During left-right split-belt locomotion,
rSTA and rSW were respectively decreased and increased on the constant side,
compared to values obtained during tied-belt locomotion, whereas on the varying
side, rSTA and rSW were respectively increased and decreased. Thus, phase variations
were differentially modulated in both hindlimbs concurrently. Results were similar
in intact and chronic spinalized cats, indicating that the bilateral control of phase
variations is mediated at the level of the spinal cord, most likely by a sensory
mechanism.

3.2 Transverse Split-Belt Locomotion


While left-right split-belt locomotion alters some features of interlimb coordination,
independently controlling the speed of the fore- and hindlimbs primarily alters
inter-girdle coordination. The adaptation to transverse split-belt locomotion is
The Control of Interlimb Coordination during Left-Right and Transverse Split-Belt 33

strikingly different if it is the forelimbs or the hindlimbs that are walking faster [6].
If the forelimbs walk faster than the hindlimbs, there is often an uncoupling of the
forelimb and hindlimb rhythms (i.e. unequal cycle durations) with the forelimbs
taking two or more steps for every hindlimb cycle. As a result, the sequence of limb
contacts (i.e. footfall patterns) that normally proceeds with a hindlimb contact
followed by contact of the homolateral forelimb, termed a lateral sequence [12], is
altered. When the forelimbs walk faster than the hindlimbs, a diagonal sequence
can emerge whereby contact of the hindlimb is followed by contact of the
contralateral forelimb. In contrast, if the hindlimbs walk faster than the forelimbs,
cycle duration is equal at both girdles, even with hindlimb speeds up to 1.4 m/s.
The footfall pattern also maintains a normal lateral sequence. From these results, it
is clear that inter-girdle coordination is organized asymmetrically in quadrupeds.

4 Conclusion

Left-right and transverse split-belt locomotion are useful tools to study interlimb
coordination during quadrupedal locomotion. We recently showed that phase
variations are bilaterally altered during left-right split-belt locomotion and that a
spinal mechanism is involved [5]. We have also shown that inter-girdle
coordination is organized asymmetrically and that an uncoupling of the forelimb
and hindlimb rhythms occurs when the forelimbs are made to walk at a faster
speed than the hindlimbs [6]. An uncoupling of the forelimb and hindlimb
rhythms also occurs following incomplete thoracic [13] or cervical [14] spinal
cord injuries and it is always the forelimbs that take extra steps, similar to what
occurs with transverse split-belt locomotion with the forelimbs walking faster.
Transverse split-belt locomotion could help elucidate the mechanisms involved in
this uncoupling and its potential role in adapting interlimb coordination to certain
environmental demands. In coming years, we will determine how the control
systems regulating interlimb coordination are modified and adapt following
incomplete spinal cord injuries and other types of injuries or diseases that disrupt
the control of locomotion.

Acknowledgment. The present research was funded by a Discovery Grant and by a


Research Tools and Infrastructure Grant from the Natural Sciences and Engineering
Research Council of Canada to Alain Frigon.

References
[1] Talpalar, A.E., Bouvier, J., Borgius, L., Fortin, G., Pierani, A., Kiehn, O.: Dual-mode
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[2] Kiehn, O.: Development and functional organization of spinal locomotor circuits.
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34 A. Frigon et al.

[3] Dietz, V., Michel, J.: Human bipeds use quadrupedal coordination during locomotion.
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[4] Zehr, E.P., Hundza, S.R., Vasudevan, E.V.: The quadrupedal nature of human bipedal
locomotion. Exerc. Sport Sci. Rev. 37(2), 102–108 (2009)
[5] Frigon, A., Hurteau, M.F., Thibaudier, Y., Leblond, H., Telonio, A., D’Angelo, G.:
Split-belt walking alters the relationship between locomotor phases and cycle
duration across speeds in intact and chronic spinalized adult cats. J. Neurosci. 33(19),
8559–8566 (2013)
[6] Thibaudier, Y., Hurteau, M.F., Telonio, A., Frigon, A.: Coordination between the
fore- and hindlimbs is bidirectional, asymmetrically organized, and flexible during
quadrupedal locomotion in the intact adult cat. Neuroscience 240, 13–26 (2013)
[7] Courtine, G., Schieppati, M.: Human walking along a curved path. II. Gait features
and EMG patterns. Eur. J. Neurosci. 18(1), 191–205 (2003)
[8] Dietz, V., Zijlstra, W., Duysens, J.: Human neuronal interlimb coordination during
split-belt locomotion. Exp. Brain Res. 101(3), 513–520 (1994)
[9] Forssberg, H., Grillner, S., Halbertsma, J., Rossignol, S.: The locomotion of the low
spinal cat. II. Interlimb coordination. Acta Physiol. Scand. 108(3), 283–295 (1980)
[10] Gossard, J.P., Sirois, J., Noue, P., Cote, M.P., Menard, A., Leblond, H., Frigon, A.:
Chapter 2–the spinal generation of phases and cycle duration. Prog. Brain Res. 188,
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[11] Frigon, A.: Central pattern generators of the mammalian spinal cord.
Neuroscientist 18(1), 56–69 (2012)
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sequence pattern in primates. J. Exp. Zool. A Comp Exp. Biol. 305(11), 953–963
(2006)
[13] Barriere, G., Frigon, A., Leblond, H., Provencher, J., Rossignol, S.: Dual spinal lesion
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Neurophysiol. 104(2), 1119–1133 (2010)
[14] Cote, M.P., Detloff, M.R., Wade Jr., R.E., Lemay, M.A., Houle, J.D.: Plasticity in
ascending long propriospinal and descending supraspinal pathways in chronic
cervical spinal cord injured rats. Front. Physiol. 3, 330 (2012)
Chiropractic Alters TMS Induced Motor
Neuronal Excitability: Preliminary Findings

Heidi Haavik1, Imran Khan Niazi1,2, Jens Duehr1, Mat Kinget1,


Paulius Ugincius3, Oğuz Sebik4, Gizem Yılmaz4, and Kemal S. Türker4,*
1
Centre for Chiropractic Research, New Zealand College of Chiropractic,
Auckland, New Zealand P.O. Box 113-044 Newmarket
2
Department of Health Science and Technology, Aalborg University, Denmark
3
Institute of Physiology and Pharmacology, Medical Academy,
Lithuanian University of Health Sciences, Kaunas, Lithuania
4
School of Medicine, Koç University, Rumelifeneri Yolu, 34450,
Sariyer, Istanbul, Turkey

Abstract. The objective of this study was to use the electromyography (EMG) via
surface and intramuscular single motor unit recordings to further characterize the
immediate sensorimotor effects of spinal manipulation and a control intervention
using TMS. The results provide evidence that spinal manipulation of dysfunctional
spinal segments increases low threshold motoneurone excitability.

1 Introduction

Spinal manipulation has been reported to help individuals suffering from neck
pain [1,2], back pain [1,3], and headaches [4]. However, the mechanisms for this
improvement in function and reduction in pain are not well understood and remain
largely theoretical [5,6,7].
The changes brought about by spinal manipulation may involve central and / or
peripheral nervous systems. Although some studies examined the effects of it on
peripheral reflex pathways [8,9], only a few papers exist on the central effects of
the spinal manipulation. These studies have shown no changes in motor evoke
potential (MEP) amplitude [10,11] with spinal manipulation.
However, recently a new method has been used to study central and peripheral
effects of a stimulus using peristimulus frequencygram [PSF; 12] and claimed that
the classical methods of determining neuronal pathways contain significant errors
and needs to be re-studied [13]. This novel method has recently been used to re-
characterize the excitatory muscular responses evoked by the transcranial
magnetic brain stimulation (TMS) [14]. Their study highlighted the importance of
using both classical probability-based and novel frequency-based analysis to
accurately determine the muscular activity in response to TMS. Due to this

*
Corresponding author.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 35


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_8, © Springer International Publishing Switzerland 2014
36 H. Haavik et al.

evidence, the aim of the current study was to re-investigate the TMS induced
muscle responses following spinal manipulation using single motor unit data and a
combination of surface electromyography (EMG), peristimulus time histogram
(PSTH) and peristimulus frequencygram (PSF) analyses on tibialis anterior (TA).
We also aimed to utilize both the classical and novel methods of analyses of the
data.

2 Methods

Nine male subclinical spinal pain subjects received single pulse TMS via a double
cone coil over the TA motor area during weak isometric dorsiflexion of the foot.
On two separate days several hundred stimuli were delivered at a frequency of
about 0.3Hz and the intensity set at active motor threshold before and immediately
after either a spinal manipulation (high-velocity, low-amplitude spinal
manipulation of dysfunctional spinal segments) or a control intervention. The order
of the interventions was randomized. The control intervention consisted of passive
and active movements of the subject’s head, spine and body that was carried out by
the same chiropractor who pre-checked the subjects for spinal dysfunction and who
performed the spinal manipulations in the experimental intervention session. This
control intervention involved the subjects being moved into the manipulation setup
positions where the chiropractor would normally apply a thrust to the spine to
achieve the manipulations. This control intervention was not intended to act as a
sham manipulation but to act as a physiological control for possible changes
occurring due to the cutaneous, muscular or vestibular input that occur with the
type of passive and active movements involved in preparing a subject/patient for a
manipulation. It also acted as a control for the effects of the stimulation necessary
to collect the dependent measures of the study, and acted as a control for the time
required to carry out the manipulation intervention. Koç University Human Ethical
Committee approved the study in accordance with the Declaration of Helsinki.
Written informed consent was obtained prior to participation.
TA EMG was recorded with surface and intramuscular fine wire electrodes.
Three subjects also received sham double cone coil TMS pre and post a spinal
manipulation intervention. The single motor unit data were analyzed from the
constructed PSF and PSTH.
From the averaged surface EMG data MEPs were constructed and analyzed.
Seven single motor units were identified for the spinal manipulation intervention
and five single motor units were identified for the control intervention.

3 Results and Discussion

Following spinal manipulations there was an increase in the single unit MEP
amplitude. The individual single motor unit MEP amplitudes were clearly
observed in all identical single units tested pre and post spinal manipulation.
Chiropractic Alters TMS Induced Motor Neuronal Excitability 37

The PSF results confirmed that these MEPs were genuine excitatory events as the
discharge rates underlying these PSTH peaks increased. No overall MEP
amplitude changes were observed from surface EMG. No changes were observed
following the control intervention. The results provide evidence that spinal
manipulation of dysfunctional spinal segments increases low threshold
motoneurone excitability.
A significant increase in the level of excitation may indicate subject’s
confidence to move his leg after the manipulation. Therefore, spinal manipulation
can be used on to strengthen weakened muscles in human subjects.

References
[1] Bronfort, G., Haas, M., Evans, R.L., Bouter, L.M.: Efficacy of spinal manipulation
and mobilization for low back pain and neck pain: a systematic review and best
evidence synthesis. Spine J. 4, 335–356 (2004)
[2] Bronfort, G., Evans, R., Anderson, A.V., Svendsen, K.H., Bracha, Y., Grimm, R.H.:
Spinal manipulation, medication, or home exercise with advice for acute and subacute
neck pain: a randomized trial. Ann. Intern. Med. 156, 1–10 (2012)
[3] Kuczynski, J.J., Schwieterman, B., Columber, K., Knupp, D., Shaub, L., Cook, C.E.:
Effectiveness of physical therapist administered spinal manipulation for the treatment
of low back pain: a systematic review of the literature. Int. J. Sports Phys. Ther. 7,
647–662 (2012)
[4] Gross, A., Miller, J., D’Sylva, J., Burnie, S.J., Goldsmith, C.H., Graham, N., Haines,
T., Bronfort, G., Hoving, J.L.: Manipulation or mobilisation for neck pain. Cochrane
Database Syst. Rev. 15, 315–333 (2010)
[5] Pickar, J.G.: Neurophysiological effects of spinal manipulation. Spine J. 2, 357–371
(2002)
[6] Haavik, H., Murphy, B.: The role of spinal manipulation in addressing disordered
sensorimotor integration and altered motor control. J Electromyogr. Kinesiol. 22,
768–776 (2012)
[7] Henderson, C.N.: The basis for spinal manipulation: Chiropractic perspective of
indications and theory. J. Electromyogr. Kinesiol. 22(5), 632–642 (2012)
[8] Suter, E., McMorland, G., Herzog, W.: short term effects of spinal manipulation on
H-reflex amplitude in healthy and symptomatic subjects. Journal of Manipulative &
Physiological Therapeutics 28, 667–672 (2005)
[9] Herzog, W., Conway, P.J., Zhang, Y.T., Gail, J., Guimaraes, A.C.S.: Reflex responses
associated with manipulative treatments on the thoracic spine: a pilot study. Jouranl
of Manipulative and Physiological Therapeutics 18, 233–234 (1995)
[10] Haavik Taylor, H., Murphy, B.: Transient modulation of intracortical inhibition
following spinal manipulation. Chiropractic J. Australia 37, 106–116 (2007)
[11] Haavik Taylor, H., Murphy, B.: Altered sensorimotor integration with cervical spine
manipulation. J. Manipulative Physiol. Ther. 31, 115–126 (2008)
[12] Türker, K.S., Cheng, H.B.: Motor-unit firing frequency can be used for the estimation
of synaptic potentials in human motoneurones. J. Neurosci. Meth. 53, 225–234 (1994)
[13] Türker, K.S., Powers, R.K.: Black box revisited: a technique for estimating
postsynaptic potentials inneurons. Trends Neurosci. 28, 379–386 (2005)
[14] Todd, G., Rogasch, N.C., Türker, K.S.: Transcranial magnetic stimulation and
peristimulus frequencygram. Clin. Neurophysiol. 123, 1002–1009 (2012)
Strength and Motor Function after Arm
Training with an Exoskeleton Robot

Verena Klamroth-Marganska, Georg Rauter, and Robert Riener

The Sensory-Motor Systems Lab, Department of Health Science and Technologies,


Swiss Federal Institute of Technology in Zurich, 8092 Zurich, Switzerland
and
The Spinal Cord Injury Center, University Hospital Balgrist, 8008 Zurich, Switzerland
verena.klamroth@hest.ethz.ch

Abstract. Strength training of the arm after stroke can have a beneficial effect not
only on strength but also on activity. We aimed to explore whether arm motor
function, achieved with robot-assisted training with the arm therapy robot ARMin,
correlated to strength. We measured isometric strength in arm movements
involving six joints with the therapy robot ARMin. In addition, we assessed grip
strength with a hand held dynamometer. Furthermore, we compared the strength
gains under therapy between robot-assisted training and conventional,
occupational or physical therapy. We could show that patients with ARMin
therapy gain less strength than patients in the control group although they improve
in motor function. Furthermore, conventional therapy shows higher association
between motor function and strength.

1 Introduction

Stroke is a leading cause of long-term disability and weakness is a major


contributor to the reduced arm function following stroke [1,2]. Although disability
from stroke results generally from upper-motor neuron lesion and recovery
appears to happen mainly through central nervous system plasticity, strengthening
exercises may improve the functional outcomes after stroke and strengthening
programs should be part of rehabilitation after stroke [2]. We aimed to explore to
what extent motor function of the arm, achieved with robot-assisted or
conventional training, was correlated to strength. Furthermore, we investigated
whether robot-assisted training differed from conventional, occupational or
physical therapy with regard to its ability to enhance strength.
We obtained data from a clinical study where we had compared conventional
therapy of the upper limb to robot-assisted therapy with ARMin in patients after
stroke [3]. The ARMin system consists of an exoskeleton robot applied in three-
dimensional, task-specific training in a virtual environment that allows to integrate
important key factors for successful motor recovery into therapy (e.g. high number
of movement repetitions) [4]. Training was applied over a period of eight weeks

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 39


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_9, © Springer International Publishing Switzerland 2014
40 V. Klamroth-Marganska, G. Rauter, and R. Riener

(three times weekly) for one hour to patients with moderate to severe arm
hemiparesis (8 to 38 points out of maximum 66 points in the upper extremity
section of the Fugl-Meyer assessment, FMA) in the chronic phase after stroke. We
found that in comparison to the patient group receiving conventional therapy, the
patient group that underwent ARMin therapy revealed significantly larger -
although clinically modest - improvements in motor function over the whole
course of the study as measured by the (FMA: mean difference 0.78 points, 95%
CI 0.03–1.53, p=0.041). However, ARMin therapy was less effective than
conventional therapy at rebuilding arm strength (i.e. mean strength torque of six
joint measurements; mean difference -1.29 Nm, 95% CI -2.34 to - 0.23, p =
0.017). We had taken the average of six joint measurements to derive the
composite mean strength score in Nm. The six torque measures were summed for
a composite isometric torque score that was used for analysis. Furthermore, hand
grip strength was measured.
In this article, we report the extent to which motor function (as measured by the
FMA) would compare to the single isometric joint measurements and the hand
grip strength. We compared the strength changes between the ARMin therapy and
conventional therapy groups.

2 Methods

Methods are described in more detail elsewhere [3].

2.1 Study Population


Four clinical centers participated in the trial (Zürcher Höhenklinik Wald ZHW,
Uniklinik Balgrist UKB, Reha Rheinfelden RRh, and Zentrum für Ambulante
Rehabilitation Zürich ZAR). Participants were recruited if they had sustained a
single cerebrovascular accident confirmed by brain imaging (magnet resonance
imaging, MRI, or computer tomography, CT) more than five months prior to
recruitment, satisfied all eligibility criteria, and had a moderate to severe arm
paresis, as indicated by a score of 8 to 38 out of maximally 66 points in the FMA.
Seventythree individuals were eligible and completed follow-up. 35 individuals
were assigned to conventional therapy and 38 individuals to robotic therapy with
ARMin.
Following were the other eligibility criteria: minimum age 18 years; stable
recovery stage (outpatients, change of FMA within four weeks ≤3 points); able to
sit in a chair without any additional support and without leaning on the back rest;
passive range of motion (pROM, as assessed with the neutral zero method[5]) in
the shoulder: anteversion/retroversion 80˚/0˚/20˚, abduction/adduction 60˚/0˚/10˚,
inner and outer rotation 20˚/0˚/20˚; in the elbow: flexion/extension 100˚/40˚/40˚;
no excessive spasticity of the affected arm (modified Ashworth Scale mAS ≤ 3 out
of 0-5); no serious medical or psychiatric illness; no participation in any clinical
investigation within four weeks prior to the start of this study; no participation in
Strength and Motor Function after Arm Training with an Exoskeleton Robot 41

any therapeutic treatment (outside therapy) performed with the paretic arm during
the therapy phase of the study; no anticipated need for any major surgery during
the study; no pregnancy or breast feeding in women; no orthopedic, rheumatologic
or other disease restricting movements of the paretic upper extremity; no shoulder
subluxation (palpatory < 2 fingers); no skin ulcerations at the paralyzed arm;
ability to communicate effectively with the examiner such that the validity of the
patient’s data could not be compromised; no cybersickness; no pace-maker or
other implanted electric devices; body weight lower than 120 kg; no serious
cognitive deficits and aphasia preventing the performance of the ARMin
treatment.

2.2 Therapy
Patients of both groups received the same amount of therapy (three times weekly
for one hour, over a period of eight weeks, resulting in 24 sessions). Therapy with
ARMin was conducted by physical and occupational therapists. Each of the three
therapy modes of the device -mobilization, games, and ADL training- had to be
performed for a minimum of ten minutes each. No further restrictions were
imposed on therapy. The control group received conventional physical or
occupational therapy. Individual treatment was delivered in the therapy facilities of
the corresponding clinic by a therapist. No guidelines for the form of therapy or
methods used were given in order to achieve an active control group that represents
the common clinical rehabilitation practice for chronic stroke patients. The only
restriction was not to use technical devices that were designed for promoting
rehabilitation process. Minimal time for therapy in both groups (not including
preparations, diagnostic procedures, and documentation etc.) was 45 minutes.

2.3 Outcome Measures


Clinical evaluations were performed by certified physical and occupational
therapists. Individuals were assessed with a battery of instruments on the following
test days: before therapy (test 0), after 4 weeks of therapy (test 1), at the end of
therapy after 8 weeks (test 2), at the 16 weeks follow-up (test 3) and at the 34
weeks follow-up (test 4). We present here results of the FMA and strength
measurements, i.e. joint torques of the arm (in Newtonmeter) and grip strength (in
newton).
The FMA is a well-standardized assessment tool intended to quantify sensory-
motor function of the arm after stroke with established validity, reliability, and
responsiveness [6-8]. The clinical test is composed of 33 items with a cumulative
numerical score of a maximum of 66 points. Three FMA items concern reflexes (0
= no reflex activity, or 2 = reflex activity). The remaining FMA items relate to
movements of shoulder, arm, elbow, wrist and hand, and assess isolated
movements both within and outside of the pathological synergy patterns as well as
coordinated movements. They are scored on a 3-point ordinal scale (0 = cannot
42 V. Klamroth-Marganska, G. Rauter, and R. Riener

perform, 1 = performs partially, 2 = performs fully). The score can be divided into
a proximal (FMAprox for shoulder, arm and elbow, total of 36 points) and a distal
part (FMAdist for wrist and hand, total of 30 points).
The isometric strength of the arm was measured (in Newtonmeters, Nm). The
maximally detectable joint torques of the motors were 59 Nm (elbow, shoulder
rotation and horizontal movement) to 82Nm (arm elevation). ARMin moved the
patient`s arm in fixed predefined positions (Table 1), held the position, and the
patient was asked to apply maximal torque in the joint being measured (arm
elevation/retroversion, arm abduction/adduction in the horizontal plane, elbow
flexion/extension). The measured joint torques were derived from the motor current
needed to hold the patient’s arm in the defined position.
Grip strength was attained with a handheld dynamometer (Jamar, Sammons
Preston Rolyan, Bolingbrook, IL, USA). Values of three consecutive measurements
in newton (N) were averaged.

Table 1 Fixed arm positions in ARMin during joint measurements

ARM POSITION JOINT MEASUREMENT


Arm elevation/ Horizontal arm abduction Elbow flexion
retroversion and adduction and extension
Arm elevation 70 70 70
Horizontal arm abduction 70 70 70
Inner/outer arm rotation 0 25 0
Elbow flexion 20 20 60
Pro-/supination 0 90 0
Wrist flexion 0 0 0

Spearman’s correlation coefficients (rho) describing the bivariate relationship


between the single joint measurements and FMA (proximal, distal, and total) were
generated. We elected to use the nonparametric test of association in view of the
ordinal nature of the FMA and the non-normal distribution of the data. To test
Spearman’s correlation coefficients between groups we applied the Fisher z-
transformation. We used a repeated measures linear mixed model to assess the
effect of treatment over the entire course of the study. All calculations were done
with SPSS (version 20.0).

3 Results

There were no baseline differences in the single strength measurements between


the ARMin and the control groups (data not shown). Looking at all patients, the
correlation between FMAtotal and the joint measurements was medium to high
with a significant and fairly strong positive correlation for horizontal arm abduction
(rho 0.58) and elbow extension (rho 0.62) (Table 2).
Strength and Motor Function after Arm Training with an Exoskeleton Robot 43

Table 2 Spearman's correlations coefficients between FMA (FMA total, FMA proximal
and FMA distal) and single strength measurements in all patients, ARMin group and
control group, and Fisher z-transformation (z) for ARMin and control group

FMA total FMA proximal FMA distal

all ARMin Control z all ARMin control z all ARMin Control z


patients group group patients group group patients group group

grip strength 0.38 0.30 0.47 1.9* 0.34 0.26 0.45 2.07* 0.35 0.24 0.45 2.27*

arm elevation 0.40 0.51 0.30 -2.4* 0.43 0.51 0.34 -1.97* 0.26 0.30 0.23 -0.71

arm 0.39 0.30 0.47 1.9* 0.41 0.34 0.47 1.48 0.28 0.12 0.39 2.76*
retroversion
horizontal arm 0.58 0.58 0.60 0.29 0.60 0.59 0.62 0.45 0.43 0.34 0.50 1.85*
abduction
horizontal arm 0.37 0.32 0.42 1.10 0.40 0.38 0.44 0.68 0.24 0.10 0.35 2.51*
adduction
elbow flexion 0.48 0.45 0.52 0.87 0.48 0.48 0.49 0.12 0.38 0.25 0.50 2.78*

elbow extension 0.62 0.62 0.62 0.00 0.64 0.66 0.63 -0.49 0.46 0.35 0.54 2.26*

*: significant at p < 0.05.

In the ARMin group, the correlation to FMAtotal was significantly smaller than
in the control group concerning grip strength and arm retroversion, but stronger
concerning arm elevation (z = 1.9, 1.9, and – 2.4, respectively). These results were
more pronounced looking at FMAprox. In FMAdist, ARMin and control group
differed significantly concerning the strength of association in all joint
measurements but arm elevation, with the control group showing significantly
higher correlations between FMAdist and joint measurements (and grip) than the
ARMin group.

Fig. 1 Changes in arm retroversion strength (left ordinate) and FMA total (right ordinate)
over the course of the study (abszisse). Solid lines: ARMin group, dashed lines: control
group, rhombus: changes in arm retroversion strength, bullets: change in FMA total. Error
bars are ± 1 SE.
44 V. Klamroth-Marganska, G. Rauter, and R. Riener

Looking at strength changes in the groups, the control group gained


significantly more strengths than the ARMin group, namely in arm retroversion,
horizontal arm abduction, and horizontal arm adduction (Table 3, example of arm
retroversion in Figure 1).

Table 3 Change in strength in different joint measurements for ARMin and control groups

Control ARMin mean Confidence


group group difference Interval
Δ grip strength
1.21 0.75 0.46 -0.20 - 1.12
(newton)
Δ arm elevation
1.69 1.56 0.13 -1.33 – 1.59
(Nm)
Δ arm
retroversion 4.10 2.59 1.51* 0.02 – 3.01
(Nm)
Δ horizontal
arm abduction 1.99 -0.38 2.36* 1.20 – 3.52
(Nm)
Δ horizontal
arm adduction 3.31 0.21 3.10* 0.97 – 5.24
(Nm)
Δ elbow flexion
2.24 1.72 0.52 -1.96 – 3.00
(Nm)
Δ elbow
2.39 1.97 0.42 -0.93 – 1.77
extension (Nm)
*: significant at p < 0.05.

4 Discussion

Overall, the ARMin group gained less strength than the control group, particularly
in joint measurements that require the shoulder girdle. Surprisingly, the ARMin
group did not even demonstrate strength gains on horizontal arm movements. The
ARMin therapy includes a simple ball game that requires the patient to move the
arm in the horizontal plane in a highly repetitive manner. We would have expected
that this movement would not only train dexterity but also strength in the respective
muscles. Probably the support function of the robot was chosen too supportive by
the therapist and impeded training of strength. Another reason might be that
strength is a function of joint positions and our isometric strength measurement
might have assessed in a joint position that does not require the same pattern of
muscle activity trained during the ball game.
When comparing strength to motor function, the robot-assisted group showed a
lower association between the two than the control group in all joints but arm
retroversion. Muscle strength is potentially important for joint alignment, range of
Strength and Motor Function after Arm Training with an Exoskeleton Robot 45

motion and performance of activities. But other factors than strength building seem
to underlie the enhanced effects of ARMin training on motor function. Beside of
high repetition of functional and meaningful tasks, these factors might encompass
coordination and dexterity gains by “close to physiological” movements, variable
assistance (“patient cooperative path controller”), enhanced feedback (i.e. visual,
auditory and haptic) and also motivation [9].
ARMin strength measures were confined to proximal muscles of the upper
extremity and only grip strength assessed distal functions. The control group
showed a significantly higher association between proximal muscle strength and
the distal part of the FMA (which assesses wrist and hand function). We cannot
exclude that all the assessed, proximal muscular strength gains in the control group
came along with distal muscle gains which we did not capture with our system but
which might promote gains in distal motor function. Although training in ARMin
also involves the whole arm from the shoulder to the hand, it does not promote
strength gains, and changes in FAMdist might be attributable to skills rather than
strength in this group.
A drawback of our study is that we only analyzed isometric peak strength and no
dynamic force generations which might shed more light on the mechanisms of arm
hemiparesis after stroke, such as force magnitude, force production, fatigability or
excessive effort [10].
Our result are in accordance to the general observation that robot-assisted arm
training enhances motor function an activities of daily living, but not strength [11].
Whether strength gains have been the basis for the control group’s improvements
during the follow-up should be investigated in future analyses. Strength training
could be a significant key factor to boost robot-assisted arm training with ARMin
and should be integrated into functional robot-assisted training.

References
1. World Health Organization International Classification of Functioning, Disability and
Health. World Health Organization, Geneva,
http://www.who.int/classifications/icf/en
2. Ada, L., Dorsch, S., Canning, C.G.: Strengthening interventions increase strength and
improve activity after stroke: a systematic review. Aust. J. Physiother. 52, 241–248
(2006)
3. Klamroth-Marganska, V., Blanco, J., Campen, K., Curt, A., Dietz, V., Ettlin, T.,
Felder, M., Fellinghauer, B., Guidali, M., Kollmar, A., et al.: Three-dimensional, task-
specific robot therapy of the arm after stroke: a multicentre, parallel-group randomised
trial. The Lancet Neurology (2013)
4. Nef, T., Guidali, M., Riener, R.: ARMin III - arm therapy exoskeleton with an
ergonomic shoulder actuation. Applied Bionics and Biomechanics 6, 127–142 (2009)
5. Gerhardt, J.J.: Clinical measurements of joint motion and position in the neutral-zero
method and SFTR recording: Basic principles. Disability and Rehabilitation 5, 161–
164 (1983)
46 V. Klamroth-Marganska, G. Rauter, and R. Riener

6. Fugl-Meyer, A.R., Jääskö, L., Leyman, I., Olsson, S., Steglind, S.: The post-stroke
hemiplegic patient. 1. a method for evaluation of physical performance. Scand. J.
Rehabil. Med. 7, 13–31 (1975)
7. Gladstone, D.J., Danells, C.J., Black, S.E.: The fugl-meyer assessment of motor
recovery after stroke: a critical review of its measurement properties. Neurorehabil.
Neural Repair 16, 232–240 (2002)
8. Sanford, J., Moreland, J., Swanson, L.R., Stratford, P.W., Gowland, C.: Reliability of
the Fugl-Meyer assessment for testing motor performance in patients following stroke.
Phys. Ther. 73, 447–454 (1993)
9. Guidali, M., Duschau-Wicke, A., Broggi, S., Klamroth-Marganska, V., Nef, T.,
Riener, R.: A robotic system to train activities of daily living in a virtual environment.
Med. Biol. Eng. Comput. 49, 1213–1223 (2011)
10. Patten, C., Lexell, J., Brown, H.E.: Weakness and strength training in persons with
poststroke hemiplegia: rationale, method, and efficacy. J. Rehabil. Res. Dev. 41, 293–
312 (2004)
11. Mehrholz, J., Hädrich, A., Platz, T., Kugler, J., Pohl, M.: Electromechanical and robot-
assisted arm training for improving generic activities of daily living, arm function, and
arm muscle strength after stroke. Cochrane Database Syst. Rev. 6, CD006876 (2012)
Tongue Motor Training – Behavioral
and Neurophysiological Aspects

M. Kothari1,2, P. Svensson1,3, J. Jensen2, A. Kjaersgaard2,


L. Baad-Hansen1, and Jørgen Feldbæk Nielsen2
1
Section of Clinical Oral Physiology, Department of Dentistry,
Aarhus University, Aarhus, Denmark
2
Hammel Neurocenter and Rehabilitation Center, Hammel, Denmark
3
MIND Lab, Center for Functionally Integrative Neuroscience,
Aarhus University Hospital, Aarhus, Denmark

The purpose of this overall project was to elucidate the influence of different
tongue training paradigms on behavioral motor learning and cortical plasticity.

Study I

In this study, the improvement of training success during 2 training paradigms –


Tongue Protrusion Task (TPT; 1N and 3N force levels) and the Tongue Drive
System (TDS) were investigated in 16 healthy participants. Subject-based reports
of motivation, fun, pain and fatigue between the 2 paradigms were also compared.
Performance improved during training in all sessions. The mean relative increase
in success was highest in TDS. Training with the TDS was rated as more fun, less
painful, less fatiguing, and more motivating compared with TPT. In conclusion,
force level and complexity of tongue training influences behavioral aspects of
tongue motor learning.

Study II

The primary aim of this study was to investigate the effect of different training
types and secondary to test gender differences on the training-related cortical
plasticity induced by three different tongue training paradigms: 1. Therapeutic
tongue exercises (TTE), 2. Playing computer games with the tongue using TDS
and 3. TPT. 48 participants were randomized into 3 groups with 1 h of TTE, TDS,
or TPT. Stimulus–response curves of motor evoked potentials (MEPs) and motor
cortex mapping for tongue muscles and first dorsal interosseous (FDI; control)
were established using transcranial magnetic stimulation (TMS) at three time-
points: (1) before tongue training, (2) immediately after training, (3) 1 h after
training. Subject-based reports of motivation, fun, pain and fatigue were

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 47


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_10, © Springer International Publishing Switzerland 2014
48 M. Kothari et al.

evaluated. The resting motor thresholds of tongue MEPs were lowered by training
with TDS and TPT but not by TTE. Tongue MEP amplitudes increased after
training with TDS and TPT but not with TTE. Men had higher MEPs than women
in the TDS group. No significant effect of tongue training on FDI MEPs was
observed. The tongue cortical motor map areas were not significantly increased by
training. Training with TDS was most motivating and fun and TTE was rated most
painful. These findings suggest a differential effect of tongue training paradigms
on training-induced cortical plasticity and subject-based scores of fun, motivation
and pain in healthy subjects.

Study III

This study aimed to investigate the influence of tongue-disability, age and gender
on motor performance using the TDS. In study IIIa, eleven tongue-disabled
patients and 11 age and sex-matched controls participated and in study IIIb, 16
healthy elderly and 16 healthy young participants volunteered for 30 min and 40
min tongue training with TDS respectively. In study IIIa, tongue-disabled patients
performed poorer than healthy controls and men performed better than women. In
study IIIb, healthy young participants performed better than healthy elderly but
there was no effect of gender. In both studies, performance improved over time.
Tongue disability, gender and age had an effect on the outcome of motor
performance and learning.

References
1. Kothari, M., Svensson, P., Huo, X., Ghovanloo, M., Baad-Hansen, L.: Force and
complexity of tongue task training influences behavioral measures of motor learning.
Eur. J. Oral Sci. 120, 46–53 (2012)
2. Kothari, M., Svensson, P., Jensen, J., Kjærsgaard, A., Jeonghee, K., Nielsen, J.F.,
Ghovanloo, M., Baad-Hansen, L.: Training induced cortical plasticity compared
between three tongue training paradigms. Neuroscience 246, 1–12 (2013)
3. Kothari, M., Svensson, P., Jensen, J., Holm, T.D., Nielsen, S.F., Mosegaard, T.,
Nielsen, J.F., Ghovanloo, M., Baad-Hansen, L.: Tongue controlled computer game: A
new approach for rehabilitation of tongue motor function. Arch. Phys. Med. Rehab. 95,
524–530 (2014)
Functional Electrical Stimulation, Clinical
Perspective and Implications
for Future Neurorehabilitation

P.T. Birgit Larsen

Health Education UCN - Physiotherapy


Aalborg, Denmark
BGL@ucn.dk

Functional electrical stimulation devices have been available for the purpose of
orthotic aids as well as therapeutic tools since many years; however, except for
some selected countries the use of functional electrical stimulation (FES) has
previously not been extensively used in clinical practice. The reason for this is
probably manifold. The development of new technologies improving usability,
more reports on user satisfaction and confidence during use [1][2] will probably
lead to a renewed interest of FES also outside the more addicted supporters. More
so the growing evidence on the therapeutic effects of using electrical stimulation
as a supplement to other training modalities supports the acknowledgement of the
benefits of using electrical stimulation in the clinic. Altogether this is reflected in
more national clinical guidelines including FES in neurorehabilitation [3][4].
During the presentation some of the obstacles to the implementation of FES in
clinical practise that have led to further development of FES devices will be
addressed [5], and some of the recent evidence on training effects during the use
of FES alone or in combination with other training modalities [6] will be
presented.

References
[1] Bulley, C., Shiels, J., Wilkie, K., Salisbury, L.: User experiences, preferences and
choices relating to functional electrical stimulation and ankle foot orthoses for foot-
drop after stroke. Physiotherapy 97(3), 226–233 (2011)
[2] Kottink, A.L., Ijzerman, M.J., Groothuis-Oudshoorn, C.G., Hermens, H.J.: Measuring
quality of life in stroke subjects receiving an implanted neural prosthesis for drop foot.
Artif. Organs. 34(5) (May 2010)
[3] NICE Clinical Guidelines. Stroke Rehabilitation CG162 (June 2013)
[4] Danish Health and Medicines Authority. Hjerneskaderehabilitering – en medicinsk
teknologivurdering: Hovedrapport (December 2010)

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 49


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_11, © Springer International Publishing Switzerland 2014
50 P.T.B. Larsen

[5] Larsen, B., Patriciu, A.: ActiGait®: a partly implantable drop-foot Stimulator system.
In: Farina, D., Jensen, W., Akay, M. (eds.) Introduction to Neural Engineering for
Motor Rehabilitation, pp. 421–432. John Wiley & Sons, New Jersey (2013)
[6] Lee, H.-J., Cho, K.-H., Lee, W.-H.: The effects of body weight support treadmill
training with power-assisted functional electrical stimulation on functional movement
and gait in stroke patients. Am. J. Phys. Med. Rehabil. 92(12) (December 2013)
Fully Implantable Multichannel EMG
Measurement System: First Results

Sören Lewis1, Michael Russold1, Marie Hahn2, and Oskar C. Aszmann2


1
Otto Bock Healthcare Products GmbH, Vienna, Austria
{soeren.lewis,michael.russold}@ottobock.com
2
CD Labor für Wiederherstellung von Extremitätenfunktionen,
Medical University of Vienna, Austria

Abstract. Recently developed state of the art upper extremity prostheses feature
an ever-increasing number of degrees of freedom (DoF). This added functionality
and dexterity is of limited use unless new ways of prostheses control will be
developed. Currently control with two surface electrodes, allowing sequential
control of each DoF separately, is still most often found. Efficient use of dexterous
hand-prostheses though requires an intuitive and simultaneous control scheme.
This generally will also require an increasing number of control signals. These can
be acquired by application of advanced signal processing techniques on the
electromyogram (EMG) measured at the skin surface, or by means of implantable
EMG measurement systems. The latter aim at providing more independent and
intuitively generated control signals by acquisition of the EMG directly on single
muscles. The following article will first give a short overview of some of these
systems and will then present one such system – the MyoPlant system – in more
detail. In this part, we will present a system overview as well as first EMG data
collected in sheep.

Keywords: implantable EMG measurement system, intramuscular EMG, prosthesis


control.

1 Introduction
Use of the electromyogram (EMG) for control of powered upper limb prostheses
was first demonstrated by Reiter as early as 1948 [1]. Since then, state of the art
prostheses use the surface electromyogram (sEMG) measured at the skin surface
as control signal. Modern prostheses and their higher number of degrees of
freedom achieve higher dexterity but also require more control signals and make
provision of an intuitive control scheme more important and challenging.
There are several limiting factors for application of sEMG for prosthesis
control. Summation of muscle activity originating from muscles below the
electrode introduces a considerable amount of crosstalk and restricts acquiring
signals from small muscles, which generate EMG of lower amplitude, or deep
muscles, whose signals are filtered by tissue between muscle and electrode.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 51


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_12, © Springer International Publishing Switzerland 2014
52 S. Lewis et al.

Surface electrodes pick up external noise and their measurements are affected by
changes in skin impedance (e.g. due to sweating). For positioning on the stump,
electrodes are integrated into the socket, which is also transferring mechanical
loads between prosthesis and stump. Despite careful positioning, this leads
to movement and lift-off of electrodes introducing artefacts to the measured
sEMG [2].
In general, two approaches to overcome these limitations are often found. The
first approach tries to compensate for limitations related to sEMG by application of
advanced signal processing, while the second approach targets the signal
acquisition itself, by implanting electrodes directly onto muscles of interest, thus
measuring intramuscular EMG (imEMG).

1.1 Advanced Processing of sEMG Signals


In an attempt to control modern hand prostheses with sEMG signals, pattern
recognition techniques have been applied. They divide EMG data into segments,
calculate signal features on these segments and finally use these features for
classification of a limited number of movements [3]. These approaches provide a
means for simultaneous control of multiple degrees of freedom but several
challenges remain to be solved until they become relevant for clinical application
[4,5]:
• Variation in limb position lead to changes in blood perfusion and load transfer
between socket and stump, which influence sEMG signals [6]
• Many approaches focus on classification of different movements but
classification performance is reduced as soon as different contraction levels are
considered [5]
• Shift in electrode position in relation to the muscles in the stump [7]
• In addition, these signal processing approaches are still susceptible to external
noise and transient changes between signal source and electrode, like changes
in the skin impedance (e.g. due to sweating) as well as electrode movement or
lift-off.

1.2 Improved Signal Acquisition by Measuring imEMG


Implanted electrodes to measure imEMG could solve many challenges related to
prosthesis control by sEMG. The activity of smaller and deeper muscles could be
measured directly avoiding issues such as tissue filtering, crosstalk, external noise
and electrode artifacts. Careful selection of target muscles should provide more
and highly independent control signals that may result in an intuitive control
scheme for the user [8,9]. Percutaneous cables are applied in many short-term
studies but are not suitable for chronic use, since they are subject to breakage,
introduce a serious risk of infection and occurrence of granuloma [10]. Therefore,
fully implantable systems which use different solutions for energy supply, data
Fully Implantable Multichannel EMG Measurement System: First Results 53

transmission, electrode configuration and implantation surgery have been


developed in the last years (Tab. 1). A number of these have already demonstrated
that they are a viable alternative and can be considered a safe alternative for chronic
applications.

2 Implantable Systems

2.1 Telemetry Electrodes


The first implantable EMG measurement system applied for control of myoelectric
prostheses was developed as early as 1966 [11]. This system used an amplifier that
was powered by an inductive link and EMG data was transferred to the external
prosthesis via a radio frequency (RF) link. Measurement electrode and electronics
were integrated into one unit that was encapsulated in two layers of epoxy. This
resulted in a distributed system with one independent implant for each muscle
measured. In a clinical trial, it was subcutaneously implanted in one amputee for
10 days. After this period, failure of the epoxy capsule led to damage of implant
electronics. Two years later this system was revised with a focus on a more
durable housing [12]. Using a hermetic metal housing and an improved epoxy
encapsulation extended the implantation period to up to fifteen months.
Challenges encountered with these early systems comprised mechanical failures of
the epoxy housing, breakage of gold contacts where they pass through the housing
and malfunction of implant electronics. In addition, the inductive energy
transmission was critical, regarding the relative positioning of primary and
secondary coil, while data transmission was working over a distance of several
meters [12].
Nevertheless, the concept of Hirsch and Herberts was revived in the
development of Implantable Myo-Electric Sensors (IMES) [13]. Advances in
ceramic housing and electronics design allowed the integration of a first signal
processing stage on the implant [14]. In contrast to the previous system, which
was placed epimysially on superficial muscles close to the skin surface, IMES
electrodes were designed for intramuscular placement also in deeper muscles.
While this secures good EMG signal quality it can impede optimal power transfer
between primary and secondary coil. This can be further aggravated by
independent movement of single sensors due to muscle contractions [15].

2.2 Central Implant


In contrast to the distributed systems shown so far, an alternative concept is to
integrate all electronic components in a central implant and connect numerous
electrodes to it. By this, the central implant can be placed shallow underneath the
skin where an external coil can easily be placed directly above. This results in a
small distance between and a more reliable coaxial alignment of primary and
54 S. Lewis et al.

secondary coils. In addition, the secondary coil can be larger to enclose a larger
area of the electromagnetic field. Electrodes can be placed on muscles most
relevant to generate suitable control signals even if they are deep within the arm or
lying far apart.
Technical challenges in this design are the cables between electrodes and
central implant, possible connectors within these cables and passing the
connections through a hermetical housing. Additionally, implantation and possible
revision surgeries are more extensive, especially if no connectors were employed.
Implantable EMG measurement systems based on a central implant include a
system developed by Ripple [16,17] and the MyoPlant system described in more
detail below.

2.3 Distributed Systems


Distributed systems are built up from several active components that are
connected via cables for data and energy transmission. They are based on a central
implant that is providing a telemetry link for communication with external
components and energy supply either by a battery [18] or inductive coupling [19].
For each muscle that should be measured, one sensing module, which is
containing measurement and signal processing electronics, can be added over the
data bus. These sensing modules are capable of processing several features from
the measured EMG and send them towards the central unit which is forwarding
them to an external prosthesis control. This approach allows for adaptation of the
system to each patient individually and revision of single components.

Table 1 Comparison of different implantable EMG measurement systems for prosthesis


control

System IMES Ripple MyoPlant NNS


Publications [13,14,15,25] [16,17] [21,22,23,24] [18]
Topology telemetry electrode central implant central implant distributed system
(concept)
Packaging ceramic tube epoxy and silicone silicone metal
power supply inductive inductive inductive battery
data modulated on
RF transceiver RF transceiver RF transceiver
inductive link
transmission
implantation in a
implantation in sheep and primates awaiting FDA
Status primate for two
dogs for one week for up to 5 months approval
years
two RF bands with research prototype initially intended
additional ground
Comments low and high for EMG
electrode proof of concept
bandwidth controlled FES
Fully Implantable Multichannel EMG Measurement System: First Results 55

3 MyoPlant System

As one example, we will now elaborate the implantable EMG measurement


system, that was developed in the MyoPlant project [20]. It is based on a central
implant, which contains all electric components and is responsible for energy
supply, EMG measurement and data transmission. Four silicone electrodes are
connected to this central implant and allow measurement of small and deep
muscles, depending on their placement.

3.1 System Components

1) Electrodes
The developed implantable (Fig. 1) silicone electrode [21] is based on a silicone
carrier built from two layers of PTFE reinforced silicone sheet (NA 501-1, Nagor)
stuck together with silicone (MED 4011, NuSil). It carries two platinum-iridium
(Pt/Ir 90/10) contact disks with a surface area of 3.1 mm² that were laser welded to
single stranded, PTFE isolated cables (MP35N, Heraeus). The cables were coiled
and placed in a silicone tube (Silastic Rx 50, Dow Corning). Two electrode cables
ended in one of two multipolar connectors (NCP-06, Omnetics Connector
Corporation). These connectors were intra-operatively plugged in the central
implant and subsequently sealed with silicone (MED2000, Nusil).

2) Central Implant
The central implant (Fig. 2) is built around a custom designed microchip, a
microcontroller (Texas Instruments MSP430) and a RF transceiver (Zarlink
ZL70101) [22]. Input signals from the electrodes are bandpass filtered (6–1500 Hz)
and subsequently amplified in a two stage differential amplifier with adjustable
gain. The resulting signal is then digitized with 10 bit resolution. Energy was
inductively coupled into the implant at a frequency of 125 kHz and wireless data
transmission from implant to a base station used the MICS band between 402 and
405 MHz [23]. For the early experimental phase, packaging was realized by
preparation of the surface by a silicone primer (MED160, Nusil) and subsequent
injection molding the implant electronics into silicone (MED4244, Nusil).

3.2 In Vivo Evaluation


In a first step, silicone electrodes were implanted in rats. During these experiments
the low invasive surgical procedure for implantation achieved reliable positioning
of electrodes on target muscles and all electrodes stayed mechanically intact for up
to twelve weeks [21]. Subsequently, the whole system was implanted in rhesus
macaques [24] and in sheep.
During sheep trials, the system was implanted at the forelimb of two sheep. The
central implant was positioned caudal to the scapula and electrodes were implanted
56 S. Lewis et al.

at musculus brachialis, musculus triceps brachii and musculus latissimus dorsi.


First EMG measurements, carried out during three subsequent steps backward, are
presented in Fig. 3. Red bars highlight times when the limb is lifted off the ground.
Clear agonist and antagonist activity is present between musculus triceps brachii,
which extends the forelimb during stance, and musculus brachialis, which flexes
the knee and becomes active as soon as the leg is lifted off the ground. Musculus
latissimus dorsi is moving the whole forelimb backwards when it is lifted and
stabilizes the limb during stance.

Fig. 1 Schematic of the epimysial silicone electrode

Fig. 2 Central implant consisting of all electronics for energy suppl, measurement and data
transmission capsuled in silicone

4 Discussion
The systems introduced above follow different approaches, which have different
advantages and disadvantages. Telemetry electrodes are generally easier to implant
and can be placed independently, but if implanted into deep muscles revision of
broken electrodes may become traumatic. On the other hand, inductive energy
supply might be challenging due to small diameters of secondary coils and lack of
alignment between coils of different electrodes. Systems based on a central implant
provide a basis for easier energy supply and data transmission by positioning a
comparable large secondary coil close below the skin. This raises the need to
connect electrodes placed on the muscles via cables. These cables have to be routed
during implantation surgery and therefore result in a more traumatic implantation.
Fully Implantable Multichannel EMG Measurement System: First Results 57

Fig. 3 EMG signals measured during level walking of a sheep. Red areas denote times
when the leg is lifted for a step backward.

For these systems, an integration of connectors into these cables is essential for
modular replacement and lower traumatic revision surgeries. Finally, distributed
systems provide high modularity and allow individual adaptation for each patient.
While centralizing energy and data transfer they also introduce multiple points of
failure due to the bus system. It should be mentioned though that it should be
possible to place components in a manner that greatly reduces this risk.
Currently most of the systems presented above have shown proof of concept in
animal trials of varying duration. Nine IMES telemetry electrodes were implanted
in the forearm of one rhesus macaque allowing EMG measurement for two years
[25]. The MyoPlant system was implanted in a rhesus macaque [24] and two sheep,
where it allowed measurement of EMG. Ripple implanted eleven systems in dogs
and reported measurement approximately one week after implantation [16].

5 Conclusion

Proof of concept has been achieved with a number of different concepts. Ongoing
work by a number of groups is happening in order to prove the chronic stability
and applicability of these systems in human subjects. Moreover, further work in
the areas of signal processing, number of channels, pattern recognition and
surgery will have to be completed. It is most important to develop these systems
together with surgeons since it has to be expected that amputation surgery will
have to be adapted to accommodate implanted EMG acquisition. While the
projects have proven successful already, there still is no commercial version of
58 S. Lewis et al.

any of these available. Further development into a device, fulfilling all regulatory
requirements and subsequent successful commercialization are necessary steps,
which most likely will take a number of years to complete. Of high importance in
this is the aspect of seamless integration into existing prosthesis systems to
provide amputees with an intuitive control of dexterous, multi-degree-of-freedom
prosthetic hands.

Acknowledgment. This work was conducted in the MyoPlant project, which was supported
by the German Federal Ministry of Education and Research under Grant 16SV3695. The
implantable EMG measurement system was conjointly developed by the project partners
Fraunhofer Institute for Biomedical Engineering, Institute of Nanoelectronics at Hamburg
University of Technology and Otto Bock Healthcare Products GmbH in cooperation with
the subcontractor Center for Medical Physics and Biomedical Engineering at Medical
University of Vienna. Pre-clinical evaluation was carried out in cooperation with Cognitive
Neurosciences at German Primate Center, Center for Spinal Cord Injuries at Werner-
Wicker-Hospital Bad Wildungen, Institute of Biomedical Research at Medical University
of Vienna and Lehr- und Forschungsgut, University of Veterinary Medicine, Vienna.

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[18] Kirsch, R.F.: Department of Orthopaedics, Case Western Reserve University School
of Medicine, Cleveland, OH. Private Communication (January 2014)
[19] Coppey, G., Andreu, D., Guiraud, D.: Distributed Measurement Unit for Closed-Loop
Functional Electrical Stimulation: Prototype for Muscular Activity Detection. In:
IFESS Conf. (2012)
[20] Hoffmann, H.-P., Dietl, H.: Handprothesen – Nach dem Vorbild der Natur. Deutsches
Ärzteblatt 107(45), 11–14 (2010)
[21] Lewis, S., et al.: Implantable Silicone Electrode for Measurement of Muscle Activity:
Results of First in Vivo Evaluation. In: Proc. BMT, Graz (2013)
[22] Abu-Saleh, L., et al.: Ein implantierbares System zur Aufnahme von EMG-Signalen
zur Ansteuerung einer Prothese. In: Proc. BMT, Rostock, Germany, October 6-8
(2010)
[23] Cardona, A.J., et al.: Inductive energy transmission system and real-time data link for
intelligent implants. In: Proc. BMT, Freiburg, Germany (September 2011)
[24] Lewis, S., et al.: Fully Implantable Multi-Channel Measurement System for
Acquisition of Muscle Activity. IEEE Trans. Instrum. Meas. 62(7), 1972–1981 (2013)
[25] Baker, J.J., et al.: Continuous detection and decoding of dexterous finger flexions with
implantable myoelectric sensors. IEEE Trans. Neural Syst. Rehabil. Eng. 18(4), 424–
432 (2010)
Does Computerized Cognitive Rehabilitation
Generalize?

Jonas Lindeløv

Department of Communication and Psychology,


Aalborg University, Aalborg, Denmark

Computerized cognitive training is a very flexible intervention. Patients can do the


exercise anytime they want and any place they want. The training software can
adapt to the patient's current ability in a statistically optimal way, even if that
ability fluctuates. Being automated means that it can be deployed on a very large
scale at low cost.
This talk will get you up to date in the field of computerized cognitive training
and rehabilitation with practical advices on how to separate the wheat from the
chaff.
Interventions that improve Working Memory (the ability to sustain and process
information simultaneously) are particularly important, and sadly also lacking, in
brain injury rehabilitation. Working memory is one of the most prevalent
cognitive impairment following acquired brain injury across etiologies (Serino et
al., 2006; Roca et al., 2010). Furthermore, Working Memory functioning has
several times been identified as the strongest predictor of the patient's social life as
well as quality of life (Engberg & Teasdale, 2004; Teasdale et al., 1997; Ip,
Dornan & Schentag, 1995; Ruff et al., 1993).
The feasibility of computerized cognitive rehabilitation depends on cognitive
transfer: to what extent does computerized cognitive training and rehabilitation
improve general cognitive functions, such as attention, working memory and
decision making? The training should transfer to the patient's ability to process
information in everyday life.
Current research on healthy subjects is ambiguous with respect to whether this
goal is attainable. For example, Jaeggi et al., (2008, 2010) showed large effects
but they did not replicate (Jaeggi et al., 2011, Redick et al., 2012, Chooi &
Thomson, 2012). Trials on brain injured patients are sparse with some evidence of
positive effects (e.g. Westerberg et al., 2007).
In my research I've created an online adaptive training task which aims at
transfer to working memory. In a controlled randomized trial, 39 patients started
the training and 19 completed. The effect of training was evaluated on everyday
activity as well as cognition. Prospects and perils for computerized cognitive
training in a rehabilitation setting will be evaluated in light of these data.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 61


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_13, © Springer International Publishing Switzerland 2014
62 J. Lindeløv

References
Engberg, A.W., Teasdale, T.W.: Psychosocial outcome following traumatic brain injury in
adults: a long-term population-based follow-up. Brain Injury 18(6), 533–545 (2004),
doi:10.1080/02699050310001645829
Ip, R.Y., Dornan, J., Schentag, C.: Traumatic brain injury: factors predicting return to work
or school. Brain Injury 9(5), 517–532 (1995)
Jaeggi, S.M., Buschkuehl, M., Jonides, J., Perrig, W.J.: Improving fluid intelligence with
training on working memory. Proceedings of the National Academy of
Sciences 105(19), 6829–6833 (2008)
Jaeggi, S.M., Buschkuehl, M., Jonides, J., Shah, P.: Short- and long-term benefits of
cognitive training. Proceedings of the National Academy of Sciences 108(25), 10081–
10086 (2011), doi:10.1073/pnas.1103228108
Jaeggi, S.M., Studer-Luethi, B., Buschkuehl, M., Su, Y.F., Jonides, J., Perrig, W.J.: The
relationship between n-back performance and matrix reasoning–implications for training
and transfer. Intelligence 38, 625–635 (2010)
Redick, T.S., Shipstead, Z., Harrison, T.L., Hicks, K.L., Fried, D.E., Hambrick, D.Z.,
Engle, R.W.: No Evidence of Intelligence Improvement After Working Memory
Training: A Randomized, Placebo-Controlled Study. Journal of Experimental
Psychology: General (2012), doi:10.1037/a0029082
Ruff, R.M., Marshall, L.F., Crouch, J., Klauber, M.R., Levin, H.S., Barth, J., et al.:
Predictors of outcome following severe head trauma: follow-up data from the Traumatic
Coma Data Bank. Brain Injury 7(2), 101–111 (1993)
Teasdale, T.W., Christensen, A.L., Willmes, K., Deloche, G., Braga, L., Stachowiak, F.,
Leclercq, M.: Subjective experience in brain injured patients and their close relatives: A
European Brain Injury Questionnaire study. Brain Injury 11(8), 543–564 (1997)
Westerberg, H., Jacobaeus, H., Hirvikoski, T., Clevberger, P., Östensson, M.-L., Bartfai,
A., Klingberg, T.: Computerized working memory training after stroke–A pilot study.
Brain Injury 21(1), 21–29 (2007), doi:10.1080/02699050601148726
Clinical Rationale and Guidelines
for Rehabilitation at Home

Andreas Luft

Division of Vascular Neurology and Neurorehabilitation,


Department of Neurology, University Hospital of Zurich, Switzerland

1 Introduction

Rehabilitation after stroke or central nervous system injury requires personalized


and intensive training to regain functions and abilities that were impaired by the
injury. Early after the stroke training is often performed in an inpatient setting
because patients are unable to live at home for reasons of dependence on nursing
aid. Inpatient rehabilitation also allows for greater training intensity (duration)
because patients do not have to take the logistical or financial burden that transport
from home to a rehabilitation center poses. But, inpatient rehabilitation is often time
limited and training therapy has therefore to continue in the home environment.
Home-based therapy can be performed as domiciliary therapy by physical or
occupational therapist coming to the house of the patient. However, this approach is
often restricted to a few hours of training per week. Developing methods for
effective and intense, i.e., more frequent home training are therefore required.

2 Objectives
In its simplest form, home-based training consists of “home-work” given to the
patient. However, compliance with home-work is poor and training schemes
cannot be adjusted to the progress that the patient makes during recovery. Such
adjustments would require frequent visits with the therapist. Therefore,
computer/sensor based training can provide a novel avenue for successful home-
based training, often referred to as “telerehabilitation”.
The objectives for home-based telerehabilitation are as follows:
- maximize compliance so that the patient retains his/her motivation to train.
- adjust therapies in a progressive way so that the training always poses a similar
learning challenge to the patient as he/she progresses through training.
- maximize safety, so that despite continuous challenge the training remains
safe, e.g., the patient does not fall during balance training or tear the shoulder
during upper extremity training.
- retain an information link between the patient and the therapist/clinician to
monitor training success.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 63


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_14, © Springer International Publishing Switzerland 2014
64 Does Computerized Cognitive Rehabilitation Generalize?

- maintain a technically sound and error-proof system that is simple to use even
for patients with cognitive disabilities.

When the patient leaves the hospital and goes home, they have to apply what
they learned as inpatients to their live at home. Application means that they train
themselves further and may continue to improve or at least retain their abilities. If
the patient cannot implement what he/she learned at home, they are likely to loose
the ability. Especially for those patients, it is necessary to continue rehabilitative
training. Home-based training solution may provide a solution to this requirement.

3 Summary

Rehabilitative training at home based on interactive IT solutions and sensors may


provide a unique opportunity to implement effective training schemes in the
patients home thereby increased training intensity (duration) even after the
inpatient phase. Home-based rehabilitation may also assist in translating functions
recovered during inpatient rehabilitation to the daily life at home.
The Learning Benefits of Haptic Guidance
Are Age-Dependent

Laura Marchal-Crespo*, Mark van Raai, Georg Rauter,


Peter Wolf, and Robert Riener

Sensory-Motor Systems Lab, Department of Health Sciences and Technology,


ETH Zurich, Switzerland
and
Medical Faculty, Balgrist University Hospital,
University of Zurich, Switzerland
laura.marchal@hest.ethz.ch

Abstract. In a previous study with young healthy subjects, we found that the
training condition –haptic guidance, visual feedback, and no guidance- that
enhanced learning of a discrete time-dependent task the most depended on the
subjects’ initial skill level. Haptic guidance seemed to be especially suitable for
initially less skilled subjects, while skilled subjects benefited more from visual
feedback. The aim of the present study was to evaluate which feedback condition
enhanced learning in a smaller group of elderly subjects. The experiment consisted
in performing a fast tennis forehand stroke in a virtual environment. A tendon-
based parallel robot was used to apply haptic guidance during training. Results
showed that elderly subjects performed worse than young subjects during
baseline, and that they reduced the errors by a similar amount. However, in
contrast to the results obtained with young subjects, training without guidance
resulted in better learning compared to training with visual and haptic guidance.
Training with haptic and visual guidance was especially detrimental in subjects
older than 75 years. Thereby, the training strategy that enhanced learning the most
seemed to be age-dependent. The sensory and motor limitations associated with
age may have limited the effectiveness of visual and haptic guidance.

1 Introduction
Recent work has emphasized the relevance of motor learning in neuro-
rehabilitation [1][2]. The proliferation of robotic devices to provide rehabilitation
therapy following neurologic injuries has increased the interest in understanding
the underlying mechanisms of motor learning. The most widely used training
strategy in rehabilitation robotics is haptic guidance. This strategy is commonly
used to reduce performance errors for tasks that are dangerous to practice, such as
learning to walk after a neurologic injury. However, there is little evidence that

*
Laura Marchal-Crespo holds a Marie Curie International income fellowship PIIF-GA-
2010-272289.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 65


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_15, © Springer International Publishing Switzerland 2014
66 L. Marchal-Crespo et al.

haptic guidance improves human motor learning when compared to unassisted


practice [3][4], auditory or visual feedback [3][5].
Haptic guidance has been recently found to be especially beneficial for less-
skilled participants [3][4][6]. Previous studies have suggested that haptic guidance
can make the task difficulty more appropriate for the individual participant’s level
of expertise, thereby optimizing learning, as stated by the challenge point theory
[7]. Recent studies have found that haptic guidance seems to be especially suitable
for learning the timing components of motor tasks [5] [8]. We recently conducted
an experiment with young healthy subjects, and found that the training condition –
visual feedback, haptic guidance, and no guidance– that maximized learning of a
discrete time-dependent motor task depended on the subjects’ initial skill level.
Haptic guidance was especially suitable for initially less-skilled subjects while
visual feedback seemed especially suitable for initially more skilled subjects [3].
Most of the previous motor learning studies have been performed with young
healthy subjects, while little has been shown on the effect of robotic training in an
older population. Neurologic injuries, such as stroke, are more preeminent at older
ages. Thereby, studying the training strategy that optimizes motor learning with
healthy elderly subjects might help to get a better inside in robotic rehabilitation. It
is an open question if the findings reported with young participants can be
extrapolated to elderly subjects.
In this study, we aimed to extend our previous results on the effect of haptic
guidance, visual feedback, and unguided training on learning a discrete timing
task [3]—a tennis stroke— with a smaller group of elderly subjects. Motor
performance and motor learning have been documented to be impaired with age
[9]. In particular, specific skill-learning deficits in visuomotor performance have
been reported in older adults [10]. Thereby, based on our previous findings with
young subjects [3], haptic guidance might provide a means to improve motor
learning in older subjects, since their initial performance is expected to be
degraded [9]. On the other hand, the proprioceptive feedback mechanisms have
been shown to deteriorate with age, impelling elderly subjects to rely intensely on
visual control [11][12]. Thereby, a positive effect of concurrent visual feedback is
nevertheless hypothesized.

2 Material and Methods

2.1 Assistive Robotic Tennis Trainer


The assistive robotic tennis trainer consists in a tendon-based robotic system
integrated in a large CAVE with three high-resolution screens that surround the
viewer. The subjects were physically restrained to a safe area with a harness and
quickdraws, and the robot ropes were connected to a 0.5-m-long stick that figured
the racket (Fig.1).
The motor learning task consisted in a tennis forehand stroke performed with
the right arm fully stretched. The desired stroke trajectory of the racket tip was
previously measured with an optical tracking system and can be approximated by
a circular arc of radius 1.1 m that subtends an angle of 110°. The desired velocity
The Learning Benefits of Haptic Guidance Are Age-Dependent 67

at each time step was modeled following an asymmetric bell-shaped velocity


profile derived from the minimum jerk equation [13].

Fig. 1 The tennis trainer [14]

Different control modes were developed that (i) allowed the robot to enforce
the position and timing of the end-effector (fixed haptic guidance), that (ii)
allowed subjects to intend the task by themselves while limiting position errors
(flux guidance), and that (iii) allowed the robot to modulate the amount of
guidance that enforced the position and timing of the racket as training progressed
(fading haptic guidance). The design and evaluation of the training conditions
were described in detail in [14]. Here, only a brief summary is given for
completeness.
Fixed haptic guidance: position controller
A stiff PD controller was developed to enforce the desired racket trajectory and
velocity at each sampling instant. The PD controller is a practical solution to
prevent errors during a tracking task, without taking into consideration the
subjects’ intentions. The system friction was compensated with a feed-forward
term.
Flux guidance: path controller with assisting flux
An artificial potential field based on the obstacle-avoidance approach [15] was
designed to allow subjects to start the stroke when desired, while limiting position
errors. A repulsive potential field restricted the movement to a tunnel surrounding
the desired trajectory. The region of influence of the repulsive potential field was
delimited by a stiff tunnel and a soft tunnel that limited the area where the field
had no influence. Subjects could move freely the end effector inside the no
influence area without feeling the robot (No guidance mode), thanks to a closed-
loop force controller.
68 L. Marchal-Crespo et al.

Alternatively, the artificial potential field could also enforce a desired position-
dependent velocity profile by means of an attractive potential field. The assisting
flux was tangent to the desired trajectory and dependent on the position of the end
effector, not their time, and thus the subject was allowed to start the movement
when desired. However, once the movement was initiated, the robot guided the
subject to perform the stroke at the enforced speed.
Fading haptic guidance
The fading haptic guidance controller was developed as a transition between a PD
controller that enforced the time to start a stroke and the velocity, toward a path
controller with assisting flux that enforced only the velocity [8]. The smooth
transition was accomplished performing a weighted sum of the control signals
from the PD controller and path with assisting flux outputs. The weights
associated with the PD controller (wPD) and path controller with flux (wflux) were
updated after each trial using a forgetting factor as in [10]. The training session
started with the PD controller only (wPD = 1, wflux = 0).

2.2 Study Protocol


The experimental protocol was the same as the one described in our previous
study with young subjects (aged 28.2 ±3.1) [3]. In the current study, five elderly
subjects participated (aged 63, 67, 75, 80, 84 years old). The task consisted in
rebounding a virtual ball moving toward them performing a forehand stroke, so
that the rebounding ball hit a highlighted court area (Fig. 2). Three targets located
on the left (T1), middle (T2), and right (T3) side of the court were randomly
presented. Targets T1 and T2 were more challenging (range of correct racket
angles at ball impact was 6.9°), while the range of correct racket’s angles to hit T3
was 15.5°.

Fig. 2 The virtual game projected on the front screen [3]. Three different targets were
randomly presented (here, the three targets are pictured for explanation purposes).
The Learning Benefits of Haptic Guidance Are Age-Dependent 69

All subjects trained with three different conditions:


Flux guidance: the controller enforced the stroke trajectory and the velocity
profile, but allowed the subjects to start the movement whenever they considered
adequate (i.e. no guidance on timing).
Fading haptic guidance: the robot started the training enforcing the correct timing
to start the stroke, but faded the guidance on timing as training progressed. The
last five trials were performed without guidance
Concurrent visual feedback: same as flux guidance, but the correct time to start
the stroke was indicated by a change in the color of the ball (from yellow to red).
The ball changed the color 300 ms before the optimal time to start the movement
to account for the subjects’ reaction time.
A within-subject cross-over design was used to test the effects of training with
the three different training modes. During baseline, the robot was controlled in no
guidance mode (path controller without assisting flux) and all three targets were
randomly presented a total of 9 times (3 strokes × 3 targets). Subjects were
randomly assigned into one of the 6 possible training configurations (depending
on the training order). Subjects only played with the left (T1) and right (T3)
targets during training, presented 40 times (20 hits × 2 target). The untrained
target T2 was employed to test for generalization. The short-time retentions after
training were identical to baseline (thus, 3 strokes × 3 targets).

2.3 Data Processing and Statistical Analysis


For each trial, the absolute error between the position of the racket at ball impact
and the optimal position that rebounds the ball to the center of the target was
calculated. To determine whether the elderly subjects’ performance was different
from the performance measured in our previous experiment with young subjects
[3], we ran an independent samples t-test to compare the error created during
baseline and retention tests between age groups. To determine whether the
learning rate was different in elderly subjects, we ran an independent samples t-
test to compare the error reduction after training between age groups.
To determine whether elderly subjects learned, Wilcoxon signed-rank tests
between baseline and retentions were performed. To determine if error reduction
was different between training strategies, we performed a Friedman test. To
determine differences in learning to hit different targets, we performed Wilcoxon
signed-rank tests between targets. The significance value was set to p = 0.05.
Statistical analyses were performed using the IBM SPSS Statistics software
(Version 21).

3 Results
Elderly subjects performed systematically worse than young subjects from our
previous experiment during baseline and retention. Elderly subjects created
70 L. Marchal-Crespo et al.

significantly larger errors during baseline than young subjects (p=0.027) [3] (Fig.
3). Similarly, elderly subjects performed worse than young subjects during
retention tests (p=0.003). However, we did not find significant differences
between age groups in the error reduction from baseline to retentions (Fig. 3).
Elderly subjects reduced their errors to a similar extent as did young subjects.
Elderly subjects only reduced significantly the errors created during baseline
after training with flux guidance (Fig. 4 up, p=0.043). Although the error
reduction after flux guidance seemed to be greater compared to the other
strategies, the differences did not reach significance.
We found that the amount of error reduction was different between targets
(p=0.032). In particular, we found that subjects reduced the errors significantly
more after training the easy target (T3), compared to the difficult target (T1)
(p=0.043). In fact, subjects significantly reduced the errors in the easy target
(p=0.043), while they showed a tendency towards an increase of error in the
difficult target (p=0.080).
Elderly subjects did not generalize learning, i.e. they did not reduce errors when
hitting the untrained target (T2).

Fig. 3 Effect of initial skill level (i.e., mean baseline error) on the error reduction after
training with the different training conditions for young subjects from our previous study
(small markers), and elderly subjects (large filled markers). The lines fit the data from
young subjects [3]. The elderly subject age is indicated with arrows.

We did not observe an interaction between training conditions and initial skill
level. However, we observed that flux guidance seemed to be more beneficial for
subjects older than 75 years, while haptic and visual guidance seemed to be more
beneficial for younger elderly subjects (Fig. 4, down).
The Learning Benefits of Haptic Guidance Are Age-Dependent 71

Fig. 4 Up: Mean absolute error during baseline and retention tests. Error bars show ± 1 SE.
Significant differences are identified with an asterisk (p < 0.05). Down: Effect of age on the
error reduction after training.

4 Discussion
A decline of motor performance with age has been observed in previous studies
[9][10]. It has been also suggested that aging slows the rate of motor learning
72 L. Marchal-Crespo et al.

[12][16]. In the present study, elderly subjects performed systematically worse


than younger participants during baseline and retention tests. However, we did not
find significant differences between age groups in the amount of error reduction
gained following training. This is in line with a previous experiment that showed
no differences in the amount of error reduction after training with haptic guidance
between young and elderly subjects [14].
In our previous experiment with young subjects, we found that training with
haptic guidance resulted in better learning of the discrete motor task, especially in
initially less-skilled subjects [3]. Thereby, we hypothesized that older subjects
may benefit specially from haptic guidance, since a poorer performance during
baseline was expected. On the other hand, we hypothesized a positive effect of
concurrent visual feedback, since previous studies showed that elderly subjects
tend to rely intensely on visual control [11][12]. However, although elderly
subjects performed systematically worse than young subjects during baseline,
training with haptic and visual feedback did not improve learning, while training
with flux guidance (i.e. without guidance on timing) resulted in a significant error
reduction after training. Thereby, although the acquisition of new skills seemed
relatively unaffected by age, the training strategy that optimized learning seemed
to be age-dependent.
We found that training without guidance was especially suitable for subjects
older than 75 years. Cognitive changes in the very old population, the so-called
fourth age, have been extensively reported [9]. Sensory limitations, slower speed
of processing and motor limitations are some characteristics of older ages that may
have limited the effectiveness of the designed concurrent visual and haptic
feedbacks. However, further studies with a larger group of old and/or disabled
subjects are needed to drive stronger conclusions.

5 Conclusion

There has been an increasing interest from the rehabilitation community to


understand the underlying mechanisms of motor learning [1][2]. There is an
increasing body of motor learning studies performed with healthy young subjects.
However, since neurologic injuries are more preeminent at older ages, studying
the training strategy that optimizes motor learning with elderly subjects might help
to get a better understanding of robotic rehabilitation.
In this study we found that the acquisition of new skills seems unaffected by
age. However, the learning benefits of haptic guidance seemed to be age-
dependent. Training with haptic and visual guidance was especially detrimental
for very elderly subjects. This finding suggests that care should be taken when
designing motor learning experiments to better understand rehabilitation
processes.
The Learning Benefits of Haptic Guidance Are Age-Dependent 73

References
[1] Huang, V., Krakauer, J.W.: Robotic neurorehabilitation: a computational motor
learning perspective. J. Neuroeng. Rehabil. 6, 5 (2009)
[2] Krakauer, J.W.: Motor learning: its relevance to stroke recovery and
neurorehabilitation. Curr. Opin. Neurol. 19(1), 84–90 (2006)
[3] Marchal-Crespo, L., van Raai, M., Rauter, G., Wolf, P., Riener, R.: The effect of
haptic guidance and visual feedback on learning a complex tennis task. Exp. Brain
Res. 231(3), 277–291 (2013)
[4] Marchal-Crespo, L., McHughen, S., Cramer, S., Reinkensmeyer, D.: The effect of
haptic guidance, aging, and initial skill level on motor learning of a steering task.
Exp. Brain Res. 201(2), 209–220 (2010)
[5] Sigrist, R., Rauter, G., Riener, R., Wolf, P.: Augmented visual, auditory, haptic, and
multimodal feedback in motor learning: A review. Psychonomic Bulletin &
Review 20(1), 21–53 (2013)
[6] Milot, M.-H., Marchal-Crespo, L., Green, C., Cramer, S., Reinkensmeyer, D.:
Comparison of error-amplification and haptic-guidance training techniques for
learning of a timing-based motor task by healthy individuals. Exp. Brain Res. 201(2),
119–131 (2010)
[7] Guadagnoli, M.A., Lee, T.D.: Challenge point: a framework for conceptualizing the
effects of various practice conditions in motor learning. J. Mot. Behav. 36(2), 212–
224 (2004)
[8] Bluteau, J., Coquillart, S., Payan, Y., Gentaz, E.: Haptic guidance improves the visuo-
manual tracking of trajectories. PLoS ONE 3(3), e1775 (2008)
[9] Voelcker-Rehage, C.: Motor-skill learning in older adults: a review of studies on age-
related differences. Eur. Rev. Aging Phys. Activity 5, 5–16 (2008)
[10] Seidler, R.D.: Differential effects of age on sequence learning and sensorimotor
adaptation. Brain Res. Bull. 70, 337–346 (2006)
[11] Hedel, H.J.A., Dietz, V.: The influence of age on learning a locomotor task. Clin.
Neurophysiol. 115, 2134–2143 (2004)
[12] Wishart, L., Lee, T., Cunningham, S., Murdoch, J.: Age-related differences and the
role of augmented visual feedback in learning a bimanual coordination pattern. Acta
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[13] Flash, T., Hogan, N.: The coordination of arm movements: an experimentally
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[14] Marchal-Crespo, L., Rauter, G., Wyss, D., von Zitzewitz, J., Riener, R.: Synthesis and
Control of an Assistive Robotic Tennis Trainer. In: IEEE Int. Conf. on Biomedical
Robotics and Biomechatronics (2012)
[15] Khatib, O.: Real-time obstacle avoidance for manipulators and mobile robots. In:
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[16] Swinnen, S.P.: Age-related deficits in motor learning and differences in feedback
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Robot Supported Gait Rehabilitation: Clinical
Needs, Current State of the Art and Future

Zlatko Matjačić, Andrej Olenšek, and Matjaž Zadravec

University Rehabilitation Institute, Ljubljana, Slovenia


{zlatko.matjacic,andrej.olensek}@ir-rs.si

Abstract. Rehabilitation robots have made their way into clinical practice and are
being readily used in the routine rehabilitation treatment of people with disabilities
following neurological insult/disease. Currently, rehabilitation robots for training
walking have limited number of mechanical degrees of freedom thus enabling also
limited scope of gait training, limited to training of cyclical leg movement in the
plane of progression. Efficient training of proper weight shifting, overall dynamic
balance as well as turning capabilities is currently poorly incorporated in
contemporary rehabilitation robots. In this paper we propose two conceptual
approaches of mechanical devices that may overcome limited factors listed above.
We further discuss possible control approaches for the presented concepts that will
inevitably have to include some degree of cognitive abilities in future
rehabilitation robotic devices.

1 Introduction

In the last decade rehabilitation robots have made their way into clinical practice
where they are becoming an indispensable tool in neurological rehabilitation of
the upper and lower extremities [1, 2]. Rehabilitation of walking is readily aided
through the use of commercial devices in the form of robotic exoskeletons or foot-
plate based robotic platforms. These devices however currently enable gait
training only of straight-line walking due to a lack of appropriate mechanical
degrees-of-freedom (DOF). Selection of appropriate leg kinematics and relevant
training parameters such as speed of walking and a level of robotic assistance are
under the discretion of a therapist while patients are statically stable due to an
appropriate level of body-weight-support (BWS) and use of their arms holding
onto firm support. Therefore, there is clear challenge to extend the number of
DOFs to enable appropriately robot supported movement also in frontal and
transverse planes; consequently i) this will enable practicing of a more challenging
maneuvers during walking such as turning thus significantly extending the scope
of cognitive involvement of a patient, which will require also adequate cognitive-
based control of a robot and ii) it will present an additional challenge to both
patient and robot to jointly take care of adequate dynamic balance control during
walking.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 75


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_16, © Springer International Publishing Switzerland 2014
76 Z. Matjačić, A. Olenšek, and M. Zadravec

The aim of this contribution is 1.) To review clinical needs associated with
therapist and/or robot supported gait training in neurological population, 2.) To
review current state of the art in the field of rehabilitation robotics currently
incorporated into clinical practice and 3.) To propose possible further
development addressing the needs for training of turning and dynamic balancing
capabilities during walking.

2 Clinical Needs and Current State of the Art

From the biomechanical and functional point of view there are several aspects of
walking that need to be practiced following neurological insult/disease in order to
make the most from neural plasticity of the damaged brain and consequently to re-
learn functional abilities. These are:
- Cyclical leg movement (mostly in the line of progression)
- Weight-shifting capabilities (mostly in the frontal plane)
- Dynamic balancing abilities (in all three planes of motion)
- Turning skills (mostly in the transverse plane around the vertical body axis)
Physiotherapists during their clinical work readily focus first on restoring the
cyclical leg movement, which can be done in the beginning also while patient
assumes lying position. In parallel weight bearing abilities are practiced during
standing and stepping in place. Further step involves training of weight shifting
between both lower limbs, frequently while making use of partial body weight
support (BWS). This is done while standing and also while walking on a treadmill.
After certain walking speed is achieved on a treadmill progression to over ground
training of walking is possible while patient can be supported by one or two
therapists and/or using moveable parallel bars or a suitable walking aid such as
rolator. Like in any sensory-motor task a substantial number of repetitions of all
the above listed tasks are needed to take advantage of neural plasticity of the brain
to acquire necessary skills. This is why rehabilitation robotic devices have made
way into clinical practice since they can offer large number of repetitions on one
hand while on the other hand the degree of variability of the executed movement
may be under control and within the limits that facilitate successful learning.
Table 1 illustrates skills to be practiced and the current state of the art in
rehabilitation robots (only commercially available devices are listed) together with
its limitations.
Limited number of DOFs that are currently used in the contemporary
rehabilitation robots limits the completeness of walking training. The clinical
practice have shown that the listed devices are excellent tools for various phases
of rehabilitation where isolated motor skills can be reliably practiced in a safe and
repeatable manner while at the same time relieving the therapists from physical
effort as well as substantially increasing the number of repetitions of the practiced
Robot Supported Gait Rehabilitation 77

Table 1 Overview of clinical needs and state of the art rehabilitation robots in walking
training

Skill to be practiced Robotic system Brief description Limitation

Cyclical leg LOKOMAT (Hocoma AG) BWS supported treadmill walking Movement limited to sagittal plane;

movement G-EO (Reha Technologies) with robotic guidance (either not all joints of the leg are supported

AutoAmbulator (Motorika Ltd) exoskeleton or foot-plate based

LokoHelp (LokoHelp Group) mechanisms)

Gait Trainer (RehaStim GmbH)

Weight shifting Balance Trainer (medica Adjustable mechanical impedance Practicing is limited to standing.

between both legs Medizintechnik GmbH) support at the level of pelvis Axial rotation in the transverse plane

enables weight shifting in left/right is not possible.

and forward/backward directions

Dynamic balancing E-go (medica Medizintechnik Motorized platform and adjustable Natural rotation of pelvis during

during walking and GmbH) mechanical impedance support at turning is not supported in a

turning – without the level of pelvis enable practicing repeatable manner. Turning can be

using arms for of dynamic balance and turning initiated only by machine/therapists.

support skills during over ground walking Leg movement is not supported.

motor skill. However, the most evident deficits of the contemporary rehabilitation
robots for walking are related to a lack of safe, adequately supported/controlled
and stimulating training environment for 1.) Practicing proactive and reactive
dynamic balance skills and 2.) Practicing abilities to initiate and execute turning
during walking, which are both vital for safe and independent bipedal walking. It
seems that in order to achieve the above two critical aspects of robot assisted
rehabilitation of walking the future systems need to increase the number of DOFs
to match those present in a human lower body such that movement of the lower
limbs and the pelvis will be adequately supported /controlled in all three planes of
motion.

3 Ongoing and Future Development

One possible design of an exoskeleton, which would enable movement in all three
movement planes, is conceptually shown in Fig. 1a. The mechanism has in total
10 DOFs. In the hip of each leg there are three rotational joints that intersect in a
single point that ideally should coincide with the biomechanical hip joint of a
human, and then there is one rotational joint coinciding with the biomechanical
knee joint and another translational joint performing ankle plantarflexion.
In the remaining of the Figure 1 possible DOFs of movement of a subject
wearing the proposed exoskeleton are illustrated: Figure 1b shows hips
abduction/adduction; Figure 1c shows hip flexion/extension; Figure 1d shows hip
78 Z. Matjačić, A. Olenšek, and M. Zadravec

Fig. 1 Conceptual design of an exoskeleton enabling motion in all three planes

internal/external rotation; Figure 1e shows knee flexion/extension; Figure 1f


shows ankle plantarflexion/dorsiflexion. These DOFs may be actuated or can be
passive and gravity compensated by suitable spring arrangements. The conceptual
mechanical linkage shown in Figure 1 has been used as a starting point in the
development of an over ground walking rehabilitation robot within the EU 7FP
project CORBYS. The exoskeleton is attached to a robotic mobile platform via a 4
DOF pelvis interface mechanism, which enables pelvic rotation in the frontal and
transverse planes as well as pelvis vertical and side to side movement. All listed
DOFs enable more physiological movement including turning, which is
considerable step forward compared to the existing rehabilitation robots presented
in Table 1. The CORBYS system has been constructed and assembled while
the control modules including the “low-level” impedance-based control of the
mechanism as well as “high-level” cognitive control modules are under the
development.
The presented conceptual exoskeleton from Figure 1 enables/supports
movement of the lower extremity in the frontal and transversal plane, thus enabling
practicing of turning motion. Training of dynamic balance during walking may be
also possible within presented concept, however clinical practice shows that
powered exoskeletons may be suitable in the early stage of rehabilitation when
physical support in the joint of lower extremity are necessary, while later when
practicing of dynamic balancing and turning during walking becomes primary goal
of rehabilitation, active support of an exoskeleton might no longer be a necessity.
Robot Supported Gait Rehabilitation 79

Fig. 2 Conceptual design of a rehabilitation robot for training dynamic balancing and
turning while walking on a regular treadmill

Figure 2 shows a conceptual design of another rehabilitation robotic device,


which is designed to target specifically dynamic balancing and turning training
issues during walking. The key element of the system shown in Figure 2 is a
pelvic support mechanism which is based on two parallel bars that are at the
bottom connected to helical springs while at the top two hole-through spherical
joint arrangements are used to connect with a pelvis support link. This passive
mechanism has all six DOFs needed for physiological movement of the pelvis in
space. Pelvis forward/backward, left/right and up/down translations are possible as
well as pelvis tilt, list and rotation are enabled. The three DOFs are supported via
visco-elastic forces provided by the helical springs: forward/backward translation,
left/right translation and rotation of pelvis around the vertical axis. The remaining
three DOFs are passive and enable unhindered motion of the pelvis. The helical
springs are at the bottom tightened to a platform that has one DOF and enables
rotation around the vertical axis. A regular treadmill is placed on the platform and
a human subject is walking on the treadmill while being supported at the level of
80 Z. Matjačić, A. Olenšek, and M. Zadravec

pelvis by the described mechanism. A virtual reality scheme that moves in


accordance with the selected speed of treadmill provides a visual feedback to a
walking subject, indicating also the curvature of the path. When a curved motion
is indicated, also the rotation platform rotates for a given angle with selected
angular velocity. In this way the presented stationary device to considerable extent
emulates situation that occurs also during turning while walking over ground.
With the presented concepts shown in Figure 1 and 2 the possibilities for
movement training may be considerably increased and are closely related to the
way the rehabilitation robots are controlled. Control approaches may be traditional
in a sense that robots based on various sensory inputs execute pre-determined
actions. However, it seems that much more versatile training environment could
be achieved if the control of rehabilitation robots would also poses a certain
degree of “cognitive” capabilities. By this term we mean a capability of a device
“to reason” and make appropriate decisions based on the behavior of a training
subject assessed by various sensory systems, which can be distributed between the
man (various physiological parameters) and machine (kinematic and kinetic
parameters). Also, incorporation of a control scheme that can efficiently take into
account dynamic balance maintenance of the man-machine system is one of the
key challenges that need to be solved before a successful implementation of the
proposed concepts can be expected. Research addressing specifically balancing
aspects is currently underway in the EU 7 FP project BALANCE.

Acknowledgment. This work has been supported by EU 7 FP grants (project CORBYS,


contract no. 270219 and project BALANCE, contract no. 601003) and grants of the
Slovenian Research Agency (grants P2-0228 and L2-5471).

References
[1] Viteckova, S., Kutilek, P., Jirina, M.: Wearable lower limb robotics: A review.
Biocybernetics and Biomedical Engineering 33, 96–105 (2013)
[2] Diaz, I., Gil, J.J., Sanchez, E.: Lower-limb robotics rehabilitation: Literature review
and challenges. Journal of Robotics, 11 pages (2011)
Spinal Cord Stimulation:
Background and Clinical Application

Kaare Meier

Department of Neurosurgery and Department of Anesthesiology,


Aarhus University Hospital, Denmark

1 Introduction
Spinal cord stimulation (SCS) is a surgical treatment for chronic neuropathic
pain that is refractory to other treatment. Originally described by Shealy et al.
in 1967(1), it is used to treat a range of conditions such as complex regional
pain syndrome (CRPS I)(2), angina pectoris(3), radicular pain after failed back
surgery syndrome (FBSS)(4), pain due to peripheral nerve injury, stump pain(5),
peripheral vascular disease(6) and diabetic neuropathy(7,8); whereas phantom
pain(9), postherpetic neuralgia(10), chronic visceral pain(11), and pain after
partial spinal cord injury(12) remain more controversial. SCS is not effective in
relieving central neuropathic pain states.
The treatment consists of an electrode implanted in the epidural space of the
spinal cord, either via a percutaneous approach or via a surgical (hemi-)
laminectomy. When the lead is estimated to be in the optimal position and
have clinically significant effect, it is directly connected to a subcutaneously
implanted pulse generator (IPG). Depending on the indication, around 2/3 of
patients treated with SCS experience a significant pain relief.
The theoretical foundation behind the therapy was originally based on
Melzack & Wall’s Gate Control Theory,(13) but the mechanism of action is
likely to be a complex interplay of many factors, including changes in the
spinal neurotransmitter GABA/glutamate balance(14), an antidromically
mediated reduction of spinal neuronal hyperexcitability(15), recruitment of a
spinal-brainstem- spinal loop,(16) and cerebral modulating mechanisms(17).

2 The Presentation
The talk will give a basic introduction to the therapy, including its practical
use, its clinical applications, and possible complications. The clinical effects of
the treatment will be described, along with the limited experience using
quantitative sensory testing (QST) to investigate possible neurological changes.
Finally, a new initiative will be presented: An international, generic, clinical
and scientific database covering neuromodulation(18).

Acknowledgment. The author acknowledges the support from St. Jude Medical.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 81


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_17, © Springer International Publishing Switzerland 2014
82 K. Meier

References
1. Shealy, C.N., Mortimer, J.T., Reswick, J.B.: Electrical inhibition of pain by stimulation of
the dorsal columns: preliminary clinical report. Anesth Analg 46, 489–491 (1967)
2. Kemler, M.A., de Vet, H.C., Barendse, G.A., van den Wildenberg, F.A., van, K.M.:
Effect of spinal cord stimulation for chronic complex regional pain syndrome Type I:
five-year final follow-up of patients in a randomized controlled trial. J. Neurosurg.
108, 292–298 (2008)
3. Mannheimer, C., Eliasson, T., Augustinsson, L.E., Blomstrand, C., Emanuelsson, H.,
Larsson, S., Norrsell, H., Hjalmarsson, A.: Electrical stimulation versus coronary
artery bypass surgery in severe angina pectoris: the ESBY study. Circulation 97, 1157–
1163 (1998)
4. North, R.B., Kidd, D.H., Farrokhi, F., Piantadosi, S.A.: Spinal cord stimulation versus
repeated lumbosacral spine surgery for chronic pain: a randomized, controlled trial.
Neurosurgery 56, 98–106 (2005)
5. Simpson, B.A., Meyerson, B.A., Linderoth, B.: Spinal cord and brain stimulation. In:
McMahon, S., Koltzenburg, M. (eds.) Wall and Melzack’s Textbook of Pain, 5th edn.,
pp. 563–582. Elsevier (2006)
6. Klomp, H.M., Spincemaille, G.H., Steyerberg, E.W., Habbema, J.D., van Urk, H.:
Spinal-cord stimulation in critical limb ischaemia: a randomised trial. ESES Study
Group. Lancet 353, 1040–1044 (1999)
7. Tesfaye, S., Watt, J., Benbow, S.J., Pang, K.A., Miles, J., MacFarlane, I.A.: Electrical
spinal-cord stimulation for painful diabetic peripheral neuropathy. Lancet 348, 1698–
1701 (1996)
8. de Vos, C.C., Rajan, V., Steenbergen, W., van der Aa, H.E., Buschman, H.P.: Effect
and safety of spinal cord stimulation for treatment of chronic pain caused by diabetic
neuropathy. J. Diabetes Complications 23, 40–45 (2009)
9. Viswanathan, A., Phan, P.C., Burton, A.W.: Use of spinal cord stimulation in the
treatment of phantom limb pain: case series and review of the literature. Pain Pract. 10,
479–484 (2010)
10. Meglio, M., Cioni, B., Rossi, G.F.: Spinal cord stimulation in management of chronic
pain. A 9-year experience. J. Neurosurg. 70, 519–524 (1989)
11. Kapural, L., Nagem, H., Tlucek, H., Sessler, D.I.: Spinal cord stimulation for chronic
visceral abdominal pain. Pain Med. 11, 347–355 (2010)
12. Lagauche, D., Facione, J., Albert, T., Fattal, C.: The chronic neuropathic pain of spinal
cord injury: which efficiency of neuropathic stimulation? Ann. Phys. Rehabil.
Med. 52, 180–187 (2009)
13. Melzack, R., Wall, P.D.: Pain mechanisms: a new theory. Science 150, 971–979 (1965)
14. Stiller, C.O., Cui, J.G., O’Connor, W.T., Brodin, E., Meyerson, B.A., Linderoth, B.: Release
of gamma-aminobutyric acid in the dorsal horn and suppression of tactile allodynia by
spinal cord stimulation in mononeuropathic rats. Neurosurgery 39, 367–374 (1996)
15. Guan, Y., Wacnik, P.W., Yang, F., Carteret, A.F., Chung, C.Y., Meyer, R.A., Raja,
S.N.: Spinal cord stimulation-induced analgesia: electrical stimulation of dorsal
column and dorsal roots attenuates dorsal horn neuronal excitability in neuropathic
rats. Anesthesiology 113, 1392–1405 (2010)
16. El-Khoury, C., Hawwa, N., Baliki, M., Atweh, S.F., Jabbur, S.J., Saade, N.E.:
Attenuation of neuropathic pain by segmental and supraspinal activation of the dorsal
column system in awake rats. Neuroscience 112, 541–553 (2002)
17. Stancak, A., Kozak, J., Vrba, I., Tintera, J., Vrana, J., Polacek, H., Stancak, M.:
Functional magnetic resonance imaging of cerebral activation during spinal cord
stimulation in failed back surgery syndrome patients. Eur. J. Pain 12, 137–148 (2008)
18. Meier, K., Nikolajsen, L., Flink, M., Simonsen, R., Milidou, I., Jensen, T.S., Sorensen,
J.C.: The Aarhus Neuromodulation Database. Neuromodulation 16, 506–513 (2012)
Clinical Evaluation of Training System
for Recovery of Motor Function after Stroke
in Patients with Hemiplegia

Yoshifumi Morita1, Noritaka Sato1, Hiroyuki Ukai1, Hirofumi Tanabe2,


Toru Nagao3, Rumi Tanemura3, Yoshiaki Takagi4, and Yoshitaka Aoki4
1
Nagoya Institute of Technology, Gokiso-cho, Showa-ku,
Nagoya, Aichi 466-8555, Japan
morita@nitech.ac.jp
2
Self-Defence Force Central Hospital, Tokyo, Japan
3
Kobe University, Kobe, Japan
4
Sanyo Machine Works, Ltd., Aichi, Japan

Abstract. We developed a training system (URSystem: Useful and Ultimate


Rehabilitation System) for recovery of motor function of the upper limb after stroke
in patients with hemiplegia. Clinical evaluation of the therapeutic effect of the
URSystem was performed in eight patients. Active ranges of motion (A-ROMs) of
elbow extension and supination of the forearm were improved after training with
the URSystem within two weeks. Moreover, the modified Ashworth scale scores for
elbow extension and supination of the forearm were increased. This means that
spastic paralysis was reduced. These effects persisted for one month after the
training. These results show the effectiveness of training with the URSystem for
recovery of motor function of the upper limb.

1 Introduction

With Japan's gradual advancement toward a so-called superannuated society, the


number of people handicapped by disease and aging is increasing. Moreover, in
Japan, the number of stroke patients is increasing; there were 1.235 million stroke
patients in 2012 [1]. The corresponding increase in the workload of therapists has
become a social issue. Moreover, according to proposals for health care reform, in
the rehabilitation field a change from a system of empiric treatment to
evidence-based medicine is required. These challenges will be addressed by
introducing technology such as robotics, mechatronics, information processing,
and motion control into the rehabilitation exercises carried out by human
therapists in order to reduce their workload and to improve therapeutic effects.
Recently, many rehabilitation support systems have been developed. Some are
used for motor function exercises of the lower limbs so that the patient is able to
walk independently [2]. Others are used for motor function exercises of the upper
limbs so that the patient is able to function independently in daily life [3–8].

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 83


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_18, © Springer International Publishing Switzerland 2014
84 Y. Morita et al.

In this context, we previously developed a three-dimensional force display


robot (3D robot) for use in rehabilitation [5]. We exchanged opinions with
therapists about the practical uses of our 3D robot, and based on their responses,
developed testing systems [5,6,7] and a training system [8] using our 3D robot.
Recently, it has been shown that the motor function of stroke patients may be
restored even six months or more after the onset of a stroke. CI
(Constraint-Induced movement) therapy [9], which is a form of rehabilitation
therapy that improves upper limb function in stroke patients, has been developed.
One of the authors (H.T.), who is a therapist, has developed Severe CI therapy for
severe hemiplegic stroke patients [10–12]. In this therapy, he performs repeated
resistance training, using his hands, on patients to help them recover their motor
function and achieved a good treatment outcome. Fig. 1 shows repeated resistance
training being performed by using the therapist's hands. In this type of training,
however, the burden on the therapist is too heavy. Therefore, we analyzed the
therapist's movement during resistance training and, based on the results,
developed a rehabilitation support system designed to reduce the therapist's burden
in repeated resistance training [13]. To introduce a system that is easy for
therapists to operate, even for on-site rehabilitation, we have developed a
simplified resistance training system (simplified training system), shown in Fig. 2
[14]. This system provides unidirectional resistance training. We have also
developed a brace for securing the upper limb to the simplified training system, as
shown in Fig. 3.
In previous work [15], we have evaluated the effectiveness of the simplified
training system and brace based on interviews with a patient and a therapist. We
also have evaluated the therapeutic effects of repeated resistance training with the
simplified training system and brace for patients with hemiplegia after a stroke. In
training with the system, it was possible to reduce compensatory (trick) motion
and synergic movement by constraining the forearm movement along the training
trajectory, which facilitated isolated movement.
In the work described in this paper, we proposed a new training system
(URSystem: Useful and Ultimate Rehabilitation System) for more effective
recovery of upper limb motor function in patients with hemiplegia after a stroke.
We also evaluated the therapeutic effects of training with the URSystem in a
clinical setting. In this paper, “hemiplegic patient” refers to a patient with
hemiplegia after a stroke.

Fig. 1 Repeated resistance training using the therapist's hands


Clinical Evaluation of Training System for Recovery of Motor Function 85

2 Training System for Recovery of Motor Function

We modified the existing training system to facilitate elbow extension of a


hemiplegic patient.

2.1 Existing Training System


The existing training system [14,15] is a force display system with one degree of
freedom. The system consists of a mechanical system and a controller. The
mechanical system consists of a training grip, training arm, and powder brake
(Mitsubishi, ZKG-50YN). The training grip is attached to the tip of the training
arm. The patient moves the training arm independently while grasping the training
grip. However, it was difficult for a hemiplegic patient to grasp the training grip.
For this reason, instead of using the training grip, a brace was used to secure the
patient's forearm to the training system. The brace has two degrees of freedom,
allowing yawing and pitching motions of the fixing plate as shown in Fig. 3. The
powder brake generates a brake force that serves as the resistance force during
training. The system is equipped with an encoder and a strain gauge as a force
sensor. The encoder and the strain gauge measure the angle of the training arm and
the resistance force, respectively. Because this system is not equipped with motors,
it is extremely safe and economical. It should be noted that the system is used only
for active exercise training.

2.2 Functions of the Existing Training System


In the previous study [13], it was found from an interview that the therapist
selectively used four different resistance patterns during resistance training. These
patterns were also seen from the movement analysis performed during manual
training by the therapist using his hands. The four different resistance patterns,
namely, step, slope, wall, and constant modes, were installed in the controller.
The training system is equipped with six functions. The arm length adjustment
function allows therapists to easily adjust the length of the training arm. The length
of the training arm can be changed within the range of 0.15–0.75 m. The resistance
display function allows therapists to perform various types of resistance training by
changing the arm length and the resistance level. The maximum resistance is 43.1
N when the length of the training arm is 0.75 m, and 127.9 N when the length is
0.25 m.
The touch panel parameter setting function allows therapists to easily set the
parameters of the resistance patterns by pushing the buttons on the touch panel
display. The parameters consist of the magnitudes and the positions of the
resistance patterns. The magnitudes are selected from among nine levels. The
positions are determined by moving the training arm and stopping it at the desired
position. This function provides good visibility and easy operation for therapists.
86 Y. Morita et al.

2.3 Modification of the Existing Training System for Facilitating


Elbow Extension
To improve motor function of the hemiplegic upper limb, especially to facilitate
elbow extension, a new function is installed in the existing training system. The
new training system with the additional function is the URSystem (Useful and
Ultimate Rehabilitation System). The new apparatus to realize the additional
function consists of a T-shaped frame and a rubber belt for facilitating the elbow
extension. The T-shaped frame is fixed to the training arm as shown in Fig. 4. The
T-shaped frame and the upper arm are connected with the rubber belt. The
magnitude and the direction of the tension of the rubber belt acting on the upper
arm can be changed by adjusting the connecting point of the rubber belt on the
T-shaped frame and the length of the rubber belt. The therapist adjusts these
parameters on the basis of a patient's condition. When the patient extends his/her
elbow, the rubber belt is extended, the tension of the rubber belt pulls the forearm,
and the pulling force compresses the elbow joint. The resistance to the movement
of the forearm and the compression of the elbow are expected to facilitate elbow
extension. These ideas are devised on the basis of the facilitation elements of
proprioceptive neuromuscular facilitation (PNF) techniques. Therefore, the patient
is expected to extend the elbow joint fully. Moreover, pronation and supination of
the forearm, wrist flexion, and finger flexion are not allowed during elbow
extension and flexion because the forearm is fixed on the fixing plate of the brace,
preventing a synergy pattern from occurring. Therefore, isolated movement is
expected to be facilitated by using the URSystem.

Training grip
Training arm

Stoppers
Mechanical system Controller

Fig. 2 Resistance training system

Yawing motion

(a) Top view


Pitching motion

(b) Side view


Fig. 3 Brace for securing the upper limb to the training system
Clinical Evaluation of Training System for Recovery of Motor Function 87

URSystem Rubber belt for facilitating


elbow extension
T-shaped frame

Fig. 4 URSystem and repeated resistance training for a hemiplegic patient

3 Clinical Evaluation of Therapeutic Effect

We conducted clinical evaluations with hemiplegic patients to confirm the


therapeutic effect of training with the URSystem.

3.1 Assessment
The therapeutic effects of training with the URSystem were assessed using the
modified Ashworth scale (MAS) and the active range of motion (A-ROM) test.
The directions of movement of the elbow and the forearm are shown in Fig. 5. The
MAS is a quantitative evaluation method for spastic paralysis, which is graded in
six levels. Level 6 means no increase in muscle tone. Level 0 means affected parts
are rigid in flexion or extension. The A-ROM test is performed to evaluate
voluntary motor performance and has been widely used in clinical settings. The
A-ROM is measured when a patient moves a joint without any assistance of the
muscles surrounding the joint.
The statistical analysis system EXSAS, version 7.5, and STATCEL (add-in
software for Microsoft Excel), version 2, were used for statistical analysis. The
Tukey–Kramer method was used for a multiple comparison test to find the
significant differences among the MAS scores or the A-ROMs in pretraining,
posttraining, and one-month follow-up.

3.2 Training Protocol


The training protocol was as follows. The training period was two weeks (10 days).
Repeated training was performed 50 times per set for three sets. A photograph of
the training scene is shown in Fig. 4. The training time was less than 20 min per
day. Movement speed and the movement timing instructions were not given to the
patients. The resistance pattern, and the magnitude and direction of the tension
acting on the upper arm were designed by the therapist to be suitable for the
patient’s condition. The length of the rubber belt was adjusted so that the tension of
88 Y. Morita et al.

the rubber belt was maximized when the elbow was fully extended. In this test, the
length of the training arm was set to 750 mm. The patient performed the repeated
training for paralyzed elbow flexion and extension in the supination position of the
paralyzed forearm.

3.3 Patients
We prepared eight subjects to satisfy the following conditions:
1) The subject has an upper limb with hemiplegia after a stroke.
2) More than one year has passed since the stroke onset.
3) The subject did not feel pain in training with the URSystem.
4) The subject did not receive other therapy during training with the URSystem or
for one month after completing the training with the URSystem.
5) The MAS scores for elbow flexion and pronation of the forearm are three or less.
6) The A-ROMs of elbow extension and supination of the forearm are limited.
The patients' characteristics are listed in Table I.

3.4 Results and Discussion


All subjects completed training with the URSystem according to the training
protocol. It was seen in clinical evaluation that the restriction of forearm movement
along the training trajectory can reduce compensatory (trick) motion and synergic
movement in the URSystem. This facilitated isolated movement such as elbow
extension and supination of the forearm. Moreover, the resistance and the
compression applied to muscle contraction facilitated a smooth motor response.
Table 2 presents the summary of scores for outcome measures. It can be seen
from Table 2 that the MAS scores for elbow extension and supination of the
forearm were increased significantly after training, and that the effect persisted for
one month after completion of the training. The spasticity of the elbow flexor
muscle and the pronator muscle of the forearm were reduced by the active elbow
flexion and extension. Moreover, it can also be seen from Table 2 that the A-ROMs
of elbow extension and supination of the forearm were improved significantly after
training and that the effect also persisted for one month after completion the
training. The A-ROMs of elbow extension and supination of the forearm in a
healthy person are 0° and 90°, respectively. When measuring the A-ROM, the
angle of the elbow when fully extended is defined as 0°. The improvement of the
A-ROMs of one patient is shown in Fig. 6. Thus, isolated movement was facilitated
by repeated training with the URSystem.
The motor function of all the patients was restored after repetition of elbow
extension and flexion because the brain learned the movement patterns after
Clinical Evaluation of Training System for Recovery of Motor Function 89

repeated training. Moreover, it is noteworthy that motor function was restored even
in patient No. 3 and No. 4, whose poststroke times were ten years (No. 3) and three
years (No. 4) respectively.
Consequently, it is shown that training with the URSystem can improve motor
function of the upper limb after stroke in patients with hemiplegia. The results
show the effectiveness of the URSystem. The following was found from the
therapist's interview: It was easy for therapists to operate the system and to set
parameters suitable for the patients' conditions. The workload of therapists will
decrease because the system can be used for independent training for recovery of
motor function.

Fig. 5 Directions of movement of the elbow and forearm

Table 1 Patient characteristics

A-ROM [°] MAS score


No. Age TP PS
EE SF EE SF
1 51 26 R -25 20 2 2
2 62 14 L -30 15 3 3
3 63 118 L -20 5 2 2
4 31 42 L -35 30 3 3
5 32 23 R -25 45 2 2
6 54 12 L -20 30 2 2
7 51 24 R -25 50 3 2
8 52 16 L -25 25 2 2
Mean 49.5 34.4 - -25.6 27.5 2.4 2.3
SD 12.1 35.1 - 5.0 14.9 0.5 0.5
Age: Age (years), TP: Time poststroke (months), PS: Paralyzed side (right/left), EE: Elbow extension,
SF: Supination of the forearm, SD: Standard deviation
90 Y. Morita et al.

Table 2 Summary of scores for outcome measures

Measures Pretreatment Posttreatment 1-mo. follow-up

MAS score
Elbow 2.4 (0.5) 3.8 (0.5)** 3.3 (0.5)**
extension
Supination 2.3 (0.5) 3.4 (0.5)** 3.1 (0.4)**
of forearm

A-ROM [°]
Elbow
extension -25.6(5.0) -2.5(3.8)** -4.4(6.8)**

Supination 27.5(14.9) 48.8(16.0)** 44.4(12.9)**


of forearm

Values are shown as the mean±SD; *P < 0.05, **P < 0.01.

(a) (b) (c)

(d) (e)
Fig. 6 Therapeutic effects in hemiplegic patients showing the A-ROM of supination (a)
before training, (b) after 1 week of training and (c) after two weeks of training, and the
A-ROM of elbow extension (d) before training and (e) after 1 week of training
Clinical Evaluation of Training System for Recovery of Motor Function 91

4 Conclusion

The therapeutic effect of training with the URSystem was shown from the results of
the clinical evaluation. It was found that training with the system can improve
motor function of the hemiplegic upper limb.
In future work, we aim to confirm the therapeutic effect for a larger number of
subjects and to develop the training method for recovery of motor function of the
shoulder and lower extremities of hemiplegic patients by modifying the URSystem.

References
[1] Ministry of Health, Labour and Welfare, Japan. Overview of the 2011 patient survey
(2012)
[2] Sakaki, T.: TEM: therapeutic exercise machine for recovering walking functions of
stroke patients. Industrial Robot: Int. J. 26(6), 446–450 (1999)
[3] Krebs, H.I., Hogan, N., Aisen, M.L., Volpe, B.T.: Robot-Aided Neurorehabilitation.
IEEE Trans. Rehabil. Eng. 6(1), 75–87 (1998)
[4] Kikuchi, T., Xinghao, H., Fukushima, K., Oda, K., Furusho, J., Inoue, A.:
Quasi-3-DOF rehabilitation system for upper limbs: Its force-feedback mechanism and
software for rehabilitation. In: Proc. 2007 IEEE 10th Int. Conf. Rehabilitation
Robotics, pp. 24–27 (2007)
[5] Morita, Y., Furuhashi, Y., Nagasaki, M., Aoki, T., Ukai, H., Matsui, N.: Development
of muscle test system for upper limbs using 3D force display robot. Preprints of the 9th
Int, Federation of Automatic Control Symp. Robot Control, pp. 817–822 (2009)
[6] Hiramatsu, Y., Iida, Y., Yamazaki, K., Morita, M., Ukai, H., Komori, K., Taguchi, S.:
Fundamental study on evaluation of rotator cuff function using three-dimensional force
display robot. In: Proc. 4th Int. Conf. Biomedical Engineering and Informatics 2011,
pp. 1325–1329 (2011)
[7] Sato, N., Kamada, K., Hiramatsu, Y., Yamazaki, K., Morita, Y., Ukai, H., Komori, K.,
Taguchi, S.: Quantitative evaluation of shoulder joint function to reproduce results of
clinical tests by therapist. J. Robotics Mechatron. 25(6), 983–991 (2013)
[8] Furuhashi, Y., Nagasaki, M., Aoki, T., Morita, Y., Ukai, H., Matsui, N.: Development
of rehabilitation support robot for personalized rehabilitation of upper limbs. In: Proc.
Int. Conf. Rehabilitation Robotics, pp. 787–792 (2009)
[9] Ostendorf, C.G., Wolf, S.L.: Effect of forced use of the upper extremity of a hemiplegic
patient on changes in function. A single-case design. Phys. Ther. 61(7), 1022–1028
(1981)
[10] Tanabe, H.: CI therapy effects a habit of daily actions and the improvement of sensory
impairment for hemiplegic stroke patient. Japanese Soc. Brain Funct. Rehabil. 6,
16–23 (2006) (in Japanese)
[11] Tanabe, H.: CI therapy laboratory to rehabilitation, http://citherapy.com/ (in
Japanese)
[12] Tanabe, H., Nagao, T., Tanemura, R.: Application of constraint-induced movement
therapy for people with severe chronic plegic hand. Asian J. Occup. Therapy 9(4),
7–14 (2012)
92 Y. Morita et al.

[13] Iida, Y., Hiramatsu, Y., Yamazaki, K., Morita, Y., Ukai, H., Tanabe, H., Tanemura, R.,
Yokoyama, K.: Development of resistance training and evaluation support system for
upper limbs - Study on resistance training using robot in CI therapy. In: Proc. 11th
SICE System Integration Division Annu. Conf., pp. 1808–1811 (2010) (in Japanese)
[14] Morita, Y., Iida, Y., Hiramatsu, Y., Yasukita, M., Yamazaki, K., Sato, N., Ukai, H.,
Takagi, Y., Aoki, Y., Tanabe, H., Tanemura, R.: Development of simplified repeated
resistance training system for severe hemiparetic stroke patient. In: 61th Well-being
Information Technology of The Institute of Electronics, Information and
Communication Engineers, pp. 67–72 (2012) (in Japanese)
[15] Yasukita, M., Iida, Y., Yamazaki, K., Sato, N., Morita, Y., Ukai, H., Takagi, Y., Aoki,
Y., Tanabe, H., Tanemura, R.: Evaluation of simplified repeated resistance training
system for severe hemiplegic stroke patient. In: Proc. Int. Conf. Control, Automation
and Systems 2012, pp. 1566–1569 (2012)
Exotendon Glove System for Finger
Rehabilitation after Stroke

Shunji Moromugi1, Toshio Higashi2, Ryo Ishikawa3, Seiya Kudo3, Naoki Iso4,
Shirou Ooso4, Takeaki Shirotani5, Murray J. Lawn2, and Takakazu Ishimatsu3
1
Faculty of Science and Engineering, Chuo University, Japan
moromugi@elect.chuo-u.ac.jp
2
Graduate School of Biomedical Science, Nagasaki University, Japan
higashi-t@nagasaki-u.ac.jp
3
Graduate School of Engineering, Nagasaki University, Japan
4
Miharadai Hospital, Nagasaki, Japan
5
Geriatric Health Service Facility Miharanosono, Nagasaki, Japan

Abstract. An innovative electric-powered glove system has been prototyped to


support finger rehabilitation for people with motor impairment on their fingers
after a stroke. This glove system is composed of a leather glove which has a
unique actuation mechanism called an exotendon system, a muscle activity sensor
is fixed on the upper forearm to detect user’s efforts during finger exercises and a
controller including a microcomputer and a drive unit. An evaluation has been
conducted based on A-B design of a single subject study and it has been observed
that finger exercises carried out using the prototyped glove system has effectively
improved the finger functionality of a stroke patient.

1 Introduction

Recovery of hand functionality is very important for people with motor


impairments such as post stroke patients, not only to improve their quality of life
but also to accelerate rehabilitation of the entire upper-limb. Upper-limb training
is currently very limited for patients with severe finger motor impairment. One
promising approach to this problem is to provide repetitive body rehabilitation
with robotic assistance.
Recently many studies on neurorehabilitation based around robotic assistance
have been documented [1][2][3]. Also regarding hand rehabilitation, several
interesting studies using robotic devices have been done. Mouri et al. developed a
robot for hand rehabilitation for post stroke patients [4]. Connelly et al. used a
pneumatic glove system for finger rehabilitation [5].
However, most of these robotic devices are large and heavy and not practical
for patient’s everyday use. Furthermore these robots provide finger exercises with
only one degree of freedom, simply an open/close action of one or more fingers.
Exercises with multiple degrees of freedom are needed for finger rehabilitation in
order to improve the dexterity of the fingers. Therefore further developments are

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 93


and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_19, © Springer International Publishing Switzerland 2014
94 S. Moromugi et al.

needed to develop a practical rehabilitation robot which is slim, light, and


comfortable for daily use and also can allow users complex finger exercises under
a therapist’s instruction for upper-limb rehabilitation.

2 Description of System

Considering the above problems regarding robotic devices for hand rehabilitation
the authors propose an innovative electric-powered glove system called an
“exotendon glove system”. A detailed description of the proposed system follows.

2.1 Overview of the System


The exotendon glove system consists of three major parts, a leather glove with
tendon systems for finger flexion and extension, a muscle activity sensor to detect
user’s efforts during finger exercises and a controller composed of a
microcomputer and a drive unit. A prototype has been developed and tested in this
study. Fig. 1 and Fig.2 show an overview of the system and a photo of a
prototyped system, respectively. The glove is worn by the user, a muscle activity
sensor is fixed on the user’s forearm using a band. The controller is located near
the user, placed on such as a nearby table. The intensity of user’s efforts in flexion
or extension of the finger is extracted from the data obtained by the muscle
activity sensor. The controller actuates the glove based on user’s efforts in such as
to assist the user’s efforts toward completing the required exercises.

2.2 Glove
The glove is mainly made of leather sheets thus making it slim, light and soft
compared to other robotic hand orthotic devices which typically consist of rigid
structures.
The prototype used in this study focused on recovery of forefinger dexterity,
which is frequently used for daily activities. Four tendons are configured in the
glove for the exercise of the forefinger. The first for flexion of all three joints, the
MP (Metacarpophalangeal), PIP(Proximal interphalangeal) and DIP (Distal
interphalangeal) joints, the second for flexion of the MP joint and extension at the
PIP and DIP joints, the third for the extension at all three joints, the fourth for
extension at the MP joint only. Various finger positions can be provided by
combining actuation of these four tendons. Fig.3 shows photos of finger exercise
achieved by the actuation of the glove.

2.3 Muscle Activity Sensor


User’s efforts during finger exercises needs to be detected as part of this glove
system. A sensor that has been developed by one of the authors detects the level of
muscle activity [6] is used in this system. This sensor has several advantages
Exotendon Glove System for Finger Rehabilitation after Stroke 95

Fig. 1 Overview of the system

Fig. 2 Exotenson glove system developed

Fig. 3 Forefinger exercise under glove actuation


96 S. Moromugi et al.

compared to conventional EMG sensory systems as it measures more selectively


and is easy to install. Fig.4 shows photos of the sensor. This sensor mechanically
detects the hardness (stiffness) of human tissue through gentle contact with the
skin. The sensed data reflects the activity level of the muscle right over which it is
placed, higher levels of muscular actuation increasing the muscle’s stiffness. The
effects of the skin and fat tissue is typically negligible. Therefore the activity level
of the target muscle located under the sensor can be estimated. This sensor can be
easily installed and removed. It uses an elastic band and can be conveniently
placed directly over most clothes. Therefore the glove and sensor system are user-
friendly. In this glove system one or two muscle activity sensors are placed on the
user’s forearm. The number of sensors and the locations are selected based on the
user’s condition and training requirements.

Fig. 4 Muscle activity sensor

2.4 Controller
The controller and the glove are connected to each other by using four bowden
cables. Each electric motor pulls one glove tendon via a bowden cable. The
controller is composed of a microcomputer and a drive unit which includes four
electric motors and an interaction panel. The microcomputer estimates the user’s
finger exercise intention based on the muscle activity sensor data and drives the
four electric motors so that appropriate finger exercise assistance can be provided
in real time.
There is an interaction panel as a part of the controller. This glove system
provides a function to repetitively perform given finger exercises predefined by
the trainer. The interaction panel also allows the trainer to manually operate the
glove system by operating controls on the interaction panel. Status of the glove
system such as the level of muscle activity, rotation angle of the electric motors,
the control and setting mode are displayed on the interaction panel’s LCD display
so that the trainer and user can see the system status at a glance. The position of
each control corresponds to the rotation angle of each electric motor. After
Exotendon Glove System for Finger Rehabilitation after Stroke 97

installing the glove on the user’s hand the trainer operates the glove system
through the controls and checks several finger positions. The rotation angles of the
motors corresponding to each finger position is stored in the controller’s memory.
The glove system can then repeat the memorized finger positions in series and
thus provide repetitive finger exercise with a specific path specified by trainer.

2.5 Two Exercise Modes of the System


There are two exercise modes in this system. One is a passive training mode and
the other is an active training mode. In the passive training mode the glove system
simply repeats predefined exercises. In the active training mode the glove system
stops the exercise at each phase and goes on to the next exercise phase when the
user’s effort during the exercise is detected through the muscle activity sensor
system. Therefore the finger exercise is always in synchronization with the user’s
effort in the active training mode.

3 Experiment
An experiment has been conducted to evaluate the efficiency of the proposed
glove system on upper-limb motor function training on a stroke patient.

3.1 Protocol
One patient suffering from hemiparesis after a stroke participated in the
experiment as a subject. This single-subject study is conducted based on A-B
design [7]. In the first three weeks (phase A) the subject received upper-limb
exercises as part of a regular therapeutic program at a hospital. In the second three
weeks (phase B) the subject received finger extension exercises using the
proposed glove system on regular week days in addition to the daily therapeutic
program at the hospital. Upper-limb functionality was assessed once a week
during both Phase A and B. The data obtained in phase A is used as a baseline to
see the effect of intervention with the glove system in phase B.

3.2 Subject
A patient with hemiparesis after stroke participated in this experiment. The
information of the participant is shown in Table 1.

3.3 Intervention
In the intervention phase of this experiment the subject was required to work on
finger exercises for about 15 to 20 minutes using the glove system in addition to a
daily treatment program given by therapists at a hospital. In the additional
98 S. Moromugi et al.

training, the subject conducts finger extension exercises 20 times using the glove
system. In this experiment, the glove system was trained to do an exercise similar
to flipping a coin on a table with an elliptical orbit so that the subject is required to
make an effort in order to do the exercise. In this experiment the active training
mode was selected, therefore the exercises were synchronized with the subject’s
effort. Fig. 5 shows a photo of subject working on finger exercise in the
intervention phase.

Table 1 Participants’ information


Age 87
Sex Female
Diagnosis Stroke ( 7 months after onset ),
mild dementia
Motor Right hemiplegia
function Brunnstorm Stage(I-VI),
Upper extremity:IV, Hand finger:IV,
Lower-extremity:V
Sensory Superficial sensation: Normal
function Deep sensation: Mild hypesthesia
ADL Barthel Index: 55/100, FIM:70/126

Fig. 5 Subject working on finger exercise by using the glove system

3.4 Outcome Measure


Three kinds of tests were used to assess upper-limb functionality in this
experiment.

3.4.1 Upper Extremity motor subscale of Fugl-Meyer Assessment (FMA-UE)


FMA-UE is an index for comprehensive evaluation of post-stroke impairment for
the upper-extremity including performance of motor functions, sensory functions,
their coordination, speed and range of motion [8]. The maximum score is 66.
Exotendon Glove System for Finger Rehabilitation after Stroke 99

3.4.2 10-Second Tests


10-second tests are commonly used in Japan to evaluate the dexterity of people
with hemiparesis in hand control [9] This evaluation method consists of three
types of tests, a Finger Individual Movement Test (FIMT), a Hand Pronation and
Supination Test (HPST), and a Finger Tapping Test (FTT). In each of test, the
patient is requested to sit on a chair and repetitively perform a simple hand task as
fast as possible in 10 seconds and the number of tasks completed during each
period directly provides the score. In FIMT the patient is requested to flex all five
fingers one by one from the thumb to the little finger and then extend them from
the little finger to the thumb and repeat this as fast as possible during this period.
Each finger movement of flexion and extension is counted as one point in the
score. In HPST the patient puts one hand on the thigh with the palm facing up and
is requested to tap the palm of the hand with the palm side and back side of the
other hand in turn as fast as possible. Both taps face up and down are counted as
one point in the score. In FTT the patient puts one hand on the thigh as in the
HPST. During the test period, the patient is requested to tap the palm of their hand
with four fingers of the other hand as fast as possible. The number of taps made
during the test period are counted and used as the score.
3.4.3 Simple Test for Evaluating Hand Function (STEF)
STEF consists of 10 kinds of hand tasks such as moving balls and blocks of
various shapes and sizes on the table. Each task is evaluated by measuring the time
required for the task and scored from 0 to 10. The total score is 100.

3.5 Results and Discussions


An assessment was made every 5 days through this 30 day period experiment. The
results obtained in phase A (15 days without intervention) were used as a baseline
to evaluate the effect of phase B (15 days with intervention using the glove
system). Two-standard deviation band methods were used for analysis of the
experimental results. A band representing 2SDs of the baseline data was drawn
above the mean for the baseline phase and extended into the intervention phase.
Data were considered significantly different in subsequent phases if two or more
consecutive data points were located above the 2SD band [7].

3.5.1 Upper Extremity Motor Subscale of Fugl-Meyer Assessment (FMA-UE)


Fig. 6 shows the score of FMA-UE in the experiment. It is observed that the scores
of phase B are better than any of phase A. A positive effect of the intervention is
observed however the effect is not clear using the two-standard deviation band
method. The lower horizontal line in the graph shows the mean of the scores for
the baseline phase and the upper horizontal line shows the mean + 2 standard
deviations (SDs) for the baseline phase. In phase B, one of three scores is higher
but two of them are lower. This result is assumed to be due to the fact that FMA-
UE is designed to assess general performance of the upper-limb rather than the
motor function of the fingers specifically. Therefore the influence of the finger
training using the glove system may not be reflected in the FMA-UE score.
100 S. Moromugi et al.

㻡㻜
Baseline (A) Intervention (B)
㻠㻤

㻠㻢 Mean+2SDs

Score
㻠㻠

㻠㻞 Mean

㻠㻜

㻟㻤
㻜 㻝 㻞 㻟 㻠 㻡 㻢 㻣
Number of assessment

Fig. 6 Upper-extremity functionality FMA scores

3.5.2 The 10-Second Tests


Fig. 7 (a), (b) and (c) show the scores of FIMT, HPST and FTT of the 10 second
tests in the experiment, respectively. It is observed that two of the three FIMT
scores and all three FTT scores in the intervention phase are higher than the mean
+2SDs of the baseline. While almost no effects are observed in HPST. Through the
10 second tests, significant improvements are shown in FIMT and FTT which are
related to finger functionality but not in HPST which is not directly related to
finger functionality.
3.5.3 Simple Test for Evaluating Hand Function (STEF)
Fig. 8 shows the STEF score in the experiment. It is observed that all three scores
in the intervention phase are significantly higher than the mean +2SDs of the
baseline. The STEF results reflect significant improvement of upper-limb
functionality. The effect of the intervention is more clearly defined in the STEF
scores than FMA-UT scores. One of the reasons could be that all the tasks
required in STEF directly use the fingers.
Through this experiment, it is shown that the finger training using the proposed
glove system could be effective toward improving upper-limb functionality
particularly for finger related tasks.
㻡㻡
㻡㻜
Baseline (A) Intervention (B)
㻠㻡
㻠㻜
Score

㻟㻡
㻟㻜
㻞㻡 Mean+2SDs

㻞㻜 Mean
㻝㻡
㻜 㻝 㻞 㻟 㻠 㻡 㻢 㻣
Number of assessment
(a) FIMT scores
Fig. 7 Upper-limb functionality evaluated by STEF
Exotendon Glove System for Finger Rehabilitation after Stroke 101

㻡㻡
㻡㻜 Baseline (A) Intervention (B)
㻠㻡
㻠㻜

Score
㻟㻡 Mean+2SDs
㻟㻜
㻞㻡 Mean
㻞㻜
㻝㻡
㻜 㻝 㻞 㻟 㻠 㻡 㻢 㻣
Number of assessment
(b) HPST scores

㻡㻡
㻡㻜 Baseline (A) Intervention (B)
㻠㻡
㻠㻜
Score

㻟㻡
㻟㻜 Mean+2SDs
㻞㻡
Mean
㻞㻜
㻝㻡
㻜 㻝 㻞 㻟 㻠 㻡 㻢 㻣
Number of assessment
(c) FTT Scores

Fig. 7 (continued)

㻤㻜
㻣㻜 Baseline (A) Intervention (B)
㻢㻜
Score

㻡㻜
㻠㻜
㻟㻜 Mean+2SDs
㻞㻜
Mean
㻝㻜
㻜 㻝 㻞 㻟 㻠 㻡 㻢 㻣
Number of assessment

Fig. 8 Upper-limb functionality evaluated by STEF


102 S. Moromugi et al.

4 Conclusions

An innovative electric-powered glove system for upper-limb rehabilitation was


proposed. Its efficiency in regard to recovery of upper-limb functionality was tested
through a 30 day clinical experiment based on a single subject study. It was shown
that the finger training provided by the proposed glove system was effective in
improving upper-limb functionality particularly for finger-related tasks.

References
[1] Riener, R., Nef, T., Colombo, G.: Robot-aided neurorehabilitation of the upper
extremities. Med. Biol. Eng. Comput. 43, 2–10 (2005)
[2] Aoyagi, D., Ichinose, W.E., Harkema, S.J., Reinkensmeyer, D.J., Bobrow, J.E.: A
robot and control algorithm that can synchronously assist in naturalistic motion during
body weight supported gait training following neurologic injury. IEEE Trans. Neural
Syst. Rehabil. Eng. 15(3), 387–400 (2007)
[3] Banala, S.K., Agrawal, S.K., Seok, H.K., Scholz, J.P.: Novel gait adaptation and
neuromotor training results using an active Leg exoskeleton. IEEE/ASME Trans.
Mechatronics 15, 216–225 (2010)
[4] Mouri, T., Kawasaki, H., Nishimoto, Y., Aoki, T., Ishigure, Y., Tanahashi, M.: Robot
Hand Imitating Disabled Person for Education/Training of Rehabilitation. Journal of
Robotics and Mechatronics 20(2), 280–288 (2008)
[5] Connelly, L., Jia, Y., Toro, M.L., Stoykov, M.E., Kenyon, R.V., Kamper, D.G.: A
pneumatic glove and immersive virtual reality environment for hand rehabilitative
training after stroke. IEEE Trans. Neural Syst. Rehabil. Eng. 18(5), 551–559 (2010)
[6] Moromugi, S., Koujina, Y., Ariki, S., Okamoto, A., Tanaka, T., Feng, M.Q., Ishimatsu,
T.: Muscle stiffness sensor to control an assistance device for disabled. Artificial Life
and Robotics 8, 42–45 (2004)
[7] Nourbakhsh, M.R., Ottenbacher, K.J.: The Statistical Analysis of Single-Subject Data:
A Comparative Examination. Physical Therapy 74, 768–776 (1994)
[8] Fugl-Meyer, A.R., Jaasko, L., Leyman, I., Olsson, S., Steglind, S.: The post stroke
hemiplegic patient. I. A method for evaluation of physical performance. Scand. J.
Rehabil. Med. 7, 13–31 (1975)
[9] Hatanaka, T., Koyama, T., Kanematsu, M., Takahashi, N., Matsumoto, K., Domen, K.:
A new evaluation method for upper extremity dexterity of patients with hemiparesis
after stroke: the 10 second tests. International Journal of Rehabilitation Research 30(3),
243–247 (2007)
Stretch Reflex Conditioning in Humans –
Implications for Function

Natalie Mrachacz-Kersting1, Priscila de Brito Silva1, Yukiko Makihara1,


Lars Arendt-Nielsen1, Thomas Sinkjær2, and Uwe G. Kersting1
1
Department of Health Science and Technology,
Aalborg University, 9220 Aalborg Ø, Denmark
{nm,pribsilva,ym,lan,uwek}@hst.aau.dk
2
Danish National Research Foundation, Copenhagen, Denmark
ts@dg.dk

Abstract. Based on evidence from animal experiments and work on spinal cord
injured patients, we have been developing a protocol to train healthy subjects to
alter the size of their stretch reflex. As reflexes to a sudden stretch of a muscle
mark an automated response it is conceivable that by this an increased
contribution of afferent feedback to joint stiffness may occur. This may be
particularly advantageous in recreational as well as elite athletes where joint
stiffness and in particular its reduction induced by fatigue has been suggested as a
possible risk factor leading to injury. We have to date trained eight subjects to up-
regulate their soleus reflex response of which six were successful. Data show that
indeed afferent feedback is enhanced leading to increased stiffness around the
ankle joint. Further, regulation of center of pressure (CoP) excursions when
landing on one leg following a drop jump from a 30 cm height were substantially
reduced. These results imply that ankle safety in injury prone situations may be
improved and may help to reduce injury rates in sports.

1 Introduction

In previous work, our collaborators at the Wadsworth Center in New York have
successfully demonstrated that training of a simple reflex pathway for the muscles
of the calf can alter the reflex size and also leads to functionally beneficial
alterations in the modulation of reflexes during dynamic activities in both healthy
and spinal cord injured individuals [1;2]. This latter result is of particular
importance when considering the role that reflexes have during dynamic
movements. Here they not only contribute to the overall stiffness of a joint, but
their function changes dynamically throughout activities such as walking, running
and sprinting. For example, the calf muscles are stretched under the weight of the
body during the stance phase of locomotion and the stretch reflex may assist the

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 103
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_20, © Springer International Publishing Switzerland 2014
104 N. Mrachacz-Kersting et al.

force production during this phase. However, the muscles are also stretched during
the swing phase, and without suppression, the stretch reflex would extend the
ankle and may cause foot drop [3-5]. Phase-dependent modulation of spinal
reflexes is thus necessary during dynamic tasks.
Training these reflexes in humans as described above, is a completely novel
approach as a possible therapeutic intervention, yet based on 30 years of
successful animal studies [6-10]. Since afferent feedback generated by the
activation of muscle receptors can contribute substantially to overall joint stiffness
[11;12], we aimed to investigate if using the conditioning protocol developed at
the Wadsworth Center may be implemented in healthy subjects to alter joint
stiffness. This is of particular interest in the sports injury field since a low joint
stiffness has been suggested as a mechanical factor leaving an athlete at a higher
risk for injury in critical situations [13]. Fatigue-induced impairments in
neuromuscular control may adversely alter joint proprioception [14;15] and joint
stiffness and are believed to be a potential cause for the increased injury rates
during the later stages of athletic competition [16;17].
If conditioning of these simple reflex pathways can induce an increased
contribution of afferents to joint stiffness, possible new training paradigms may be
developed that contribute to reducing the injury rate in both elite and recreational
athletes.

2 The Soleus Stretch Reflex Conditioning Protocol

Understanding the role of reflex pathways during human movement has been
conducted ever since the time of Sherrington in the 1900s where the simple stretch
reflex was first described. However, until recently it has not been believed that
such a simple, monosynaptic response can be trained voluntarily, or that this
would lead to functional benefits in a trained person. In 2009, Thompson et al.
[18] provided the first proof that indeed, in healthy humans, the size of the
Hofmann reflex (H-reflex) of the calf muscle Soleus (SOL) can be changed
through training as had been shown in animal studies over the past 30 years and
that this was functionally useful. Together with our collaborators in New York we
have developed a conditioning protocol for the training of the human soleus
stretch reflex in our laboratory based on [1].

2.1 The Training Protocol


The protocol is comprised of six baseline and 24 conditioning sessions. Baseline
and conditioning sessions occur three times a week over 10 weeks. In each
session, the sitting subject provides a stable level of soleus background EMG
while the stretch reflex is elicited by an unexpected movement of the ankle joint
using the device depicted in Figure 1.
Stretch Reflex Conditioning in Humans – Implications for Function 105

Fig. 1 The unique ankle perturbator. Subjects are seated comfortably with both feet on
separate foot plates. The target foot is firmly fixated so that any rotation imposed is directly
transferred to the ankle joint.

Baseline Conditioning
Sessions

B C C
1 1 24

Trials Mmax 75 conditioned 75 conditioned 75 conditioned Mmax


stretch reflexes stretch reflexes stretch reflexes

600
Rectified EMG (uV)

Single Trial
400

200

0
0 50 100
Time after stretch (ms)

Fig. 2 Subjects attend six baseline sessions during which they are exposed to 245 single
trails consisting of imposed ankle dorsi-flexion movements. They only receive feedback on
the background level of soleus activity which they maintain at approximately 5% of the
maximum activation. In the following 24 sessions, subjects are conditioned to increase (up-
condition) the size of the soleus stretch reflex following the imposed ankle dorsiflexions.
The activity of the soleus muscle following a single imposed dorsi-flexion is depicted in the
lower trace. Several peaks may be seen that are separated by the vertical dashed lines.
Subjects receive feedback on only the first burst.
106 N. Mrachacz-Kersting et al.

Pre Up-conditioning
Post Up-conditioning

Successful training

200 μV

20 ms

Non-successful training

Fig. 3 (A) The soleus stretch reflex prior to (black trace) and following (blue trace) 24
sessions of up-conditioning in one successful subject. The grey shaded area represents the
duration of the short latency component of the soleus stretch reflex which was the target for
the conditioning, (B) as in (A) but for an unsuccessful subject.

Each session includes three blocks of 75 such imposed movements (Figure 2).
In all the trials of the baseline sessions and in the first 20 trials of the training
sessions, the stretch reflex size is simply measured (i.e., control reflexes, see
Figure 2, single trial). In three blocks of 75 conditioning trials of the training
sessions (i.e., conditioned reflexes), visual feedback after each stimulus will show
the subject whether the reflex was larger than a criterion value. Good performance
will earn a positive feedback reward while background EMG is maintained stable
throughout.

2.2 Preliminary Results from Up-Conditioning


Figure 3 depicts the size of the SOL stretch reflex in one successfully up-
conditioned subject (Figure 3A) and one non-successful subject (Figure 3B). The
grey shaded area represents the duration of the short latency component of the
soleus stretch reflex which was the target for the conditioning. Out of eight
subjects tested to date, six have been able to successfully increase the size of their
Stretch Reflex Conditioning in Humans – Implications for Function 107

SOL short latency stretch reflex following 24 training sessions while two have
failed to show any significant alterations in reflex size.

3 Functional Implications

In previous studies, successful down-conditioning of the SOL H-reflex resulted in


significant modifications in function in spinal cord injured patients [19;20]. In the
ongoing study presented here, we were interested to investigate if up-conditioning
of the SOL stretch reflex may enhance the afferent contribution to the overall
stiffness around the ankle joint and if this would result in adaptations of body
control strategies, as assessed through alterations in the center of pressure
excursion, during a functional task often encountered during various sports.

3.1 Afferent Contribution to Stiffness around the Ankle Joint


To assess the afferent contribution to the stiffness around the ankle joint, both the
intrinsic and reflex generated torque to an imposed ankle joint rotation were
quantified.
Initially, subjects were asked to voluntarily produce various levels of
background torque (range from 0-100% of a maximum contraction performed by
the subjects voluntarily, previous to the test) preset on an oscilloscope and to
maintain these without interfering with the imposed stretch. For each level of pre-
contraction, 10 stretches were imposed [11;12]. Next, the posterior tibial nerve
innervating the SOL was stimulated electrically (frequency of 20 Hz) at an
intensity to reproduce the torques generated voluntarily. Based on the knowledge
that all reflex activity is abolished during electrical stimulation high enough to
produce a tetanic contraction (Hoffer and Andreassen 1981) the resulting measure
of torque can be attributed to the intrinsic properties of the contracting muscle.
Again, 10 stretches were imposed for each level of torque. Figure 4 shows results
for the same successful subject as in Figure 3A for one level of pre-contraction at
60% of the subject’s maximum voluntary contraction. The total stiffness (4B) and
the intrinsic stiffness (not shown) increased following the successful up-
conditioning. However, the difference between these two, known as the reflex
stiffness, also increased indicating that the total stiffness change was mainly
attributable to the greater contribution of afferent feedback to the stiffness around
the ankle joint. The response of the SOL to the imposed stretch was greater
following the training (Fig 4C blue vs black trace).

3.2 Center of Pressure during Drop-Jump Landings


To assess drop landing performance, the subjects initially performed 9 to 12
familiarization trials prior to the measurements. They were instructed to drop from
108 N. Mrachacz-Kersting et al.

a 30 cm step looking straight to a mark on the wall, after a ‘go’ command, land
with the right leg, maintain one leg standing as still as possible for 3 seconds and
not to anticipate any of three different landing conditions. Subsequently, subjects
performed 15 single-leg drop landings (DL) on a moveable force platform. Three
surface inclinations were randomly produced: flat, 5-degrees forward inclination
or 5-degrees backward inclination. Results from the same successfully up-
conditioned subject as in Figure 3 are shown in Figure 5.

A Ankle Angle

4ο

200ms

B Ankle Stiffness
pre Up-conditioning
post Up-conditioning

0.02 N.m/deg

200ms
C SOL EMG

50 μV

200ms

Fig. 4 (A) Ankle angle. (B) Time course of the total stiffness of the ankle plantar flexors in
response to a 6º stretch prior to and following the up-conditioning training. Data are
averages over 10 trials for one subject. (C) The corresponding SOL EMG response.
Stretch Reflex Conditioning in Humans – Implications for Function 109

50

Anterior-posterior CoP displacement [mm]


40

30

20

pre Up-conditioning
10 post Up-conditioning

-10

-20

-30
-30 -20 -10 0 10 20 30

Medio-lateral CoP displacement [mm]

Fig. 5 Excursions of the Center of Pressure (CoP) during landing on one leg from a height
of 30 cm. Data are the best of three trials in n=1 prior to (black trace) and following (blue
trace) successful up-conditioning.

4 Discussion

In this paper we suggest and successfully applied an up-conditioning training


protocol to alter the stretch reflex response in healthy athletes. We assessed
possible functional implications by confirming that intrinsic and total stiffness of
the ankle joint were enhanced, and were accompanied by an improved landing
stability after drop landings.
A recent review on assessing the causation in sports injury suggested that
current research is too focused on the risk factors far away from the inciting event,
while only limited information is available on specific training effects as well as
the joint biomechanics during injury prone situations[13]. In this ongoing study
we are using a conditioning approach to train subjects to alter the size of their
soleus stretch reflex. To date six of the eight subjects have successfully increased
the size of their reflex following 24 sessions spaced across eight weeks.
Importantly, functional adaptations were also evident as quantified by an
increased contribution of afferent mediated feedback to the total ankle joint
stiffness as well as a decreased excursion of the CoP during landing on one leg
following drop jumps.
To date, conditioning of reflexes and thus any functional benefits have mainly
focused on impaired populations suffering from spasticity [2] [21] or elderly
populations [22]. In all of these, down-conditioning has been implemented as a
way to reduce the size of the soleus H-reflex and thus to reduce the spasticity
often observed in the former population. Somewhat surprising is that Koceja and
110 N. Mrachacz-Kersting et al.

colleagues used down-conditioning to address the problem of falls in the elderly


[22]. This target group would likely benefit from an up-regulation of reflex
function to increase joint stiffness as proposed in the current study.
If our approach of using up-conditioning would be proven successful for
athletes in injury prone situations it could be taken as an indication for using the
same approach for the elderly or patient populations at risk for falling.

5 Conclusion
Conditioning of reflex responses in sports populations is promising and opens a
pathway for a whole new research branch in injury prevention research in sports.
In particular, the link of successful reflex conditioning to beneficial functional
outcomes with the potential to protect the ankle joint under dynamic loading is
crucial. A demonstration of the possibility of conditioning the soleus muscle in
humans will set a milestone in this line of research by translating findings from
fundamental animal studies to humans. This will open the path for numerous
applied research studies on comparing human experiments to the basic animal
research work being done already. Based on the results presented in this paper the
approach can be used to alter joint stiffness including other joints than the ankle. It
needs to be addressed if the observed changes would also affect joint safety in
fatigued situations. If this approach is proven successful applied researchers will
have to search for possible ways of implementing such conditioning strategies into
suitable training programs for athletes and possibly patients suffering from
diseases affecting the musculoskeletal system.

Acknowledgment. The authors would like to acknowledge funding from the


Obelske Familiefonden and the Villum Kann Rasmussen Fonden.

References
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locomotion in people with chronic incomplete spinal cord injury. In: Abstract Viewer,
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Acta Physiologica 189(2), 155–169 (2007)
[11] Mrachacz-Kersting, N., Sinkjaer, T.: Reflex and non-reflex torque responses to stretch
of the human knee extensors. Exp. Brain Res. 151(1), 72–81 (2003)
[12] Sinkjaer, T., Toft, E., Andreassen, S., Hornemann, B.C.: Muscle stiffness in human
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[13] Meeuwisse, W.H., Tyreman, H., Hagel, B., Emery, C.: A dynamic model of etiology
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[14] Voight, M.L., Hardin, J.A., Blackburn, T.A., Tippett, S., Canner, G.C.: The effects of
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J. Orthop. Sports. Phys. Ther. 23(6), 348–352 (1996)
[15] Miura, K., Ishibashi, Y., Tsuda, E., Okamura, Y., Otsuka, H., Toh, S.: The effect of
local and general fatigue on knee proprioception. Arthroscopy 20(4), 414–418 (2004)
[16] Yu, B., Garrett, W.E.: Mechanisms of non-contact ACL injuries. Br. J Sports.
Med. 41(suppl. 1), i47–i51 (2007)
[17] Chappell, J.D., Herman, D.C., Knight, B.S., Kirkendall, D.T., Garrett, W.E., Yu, B.:
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J. Neurosci. 29(18), 5784–5792 (2009)
[19] Thompson, A.K., Wolpaw, J.R.: Restoring Walking after Spinal Cord Injury: Operant
Conditioning of Spinal Reflexes Can Help. Neuroscientist (March 2014)
[20] Thompson, A.K., Pomerantz, F.R., Wolpaw, J.R.: Operant conditioning of a spinal
reflex can improve locomotion after spinal cord injury in humans. J. Neurosci. 33(6),
2365–2375 (2013)
[21] Hoseini, N., Koceja, D.M., Riley, Z.A.: The effect of operant-conditioning balance
training on the down-regulation of spinal H-reflexes in a spastic patient. Neurosci.
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[22] Mynark, R.G., Koceja, D.M.: Down training of the elderly soleus H reflex with the
use of a spinally induced balance perturbation. J. Appl. Physiol. 93(1), 127–133
(2002)
The Role of Spinal Manipulation in Modulating
Neuroplasticity and Sensorimotor Integration

Bernadette Murphy1,* and Heidi Haavik2


1
Faculty of Health Sciences, University of Ontario Institute of Technology
Ontario, Canada
2
Centre for Chiropractic Research, New Zealand College of Chiropractic,
Auckland, New Zealand PO Box 113-044 Newmarket

Abstract. Patients with upper limb paresis and prostheses undergo prolonged
alterations in neck posture and the potential for fatigue, which is highly likely to
impair upper limb sensorimotor integration. Additionally, these postural stressors
are likely to lead to restricted mobility and pain in the neck region. This paper
describes a series of experiments using somatosensory evoked potentials (SEPs),
transcranial magnetic stimulation (TMS), electromyography (EMG) combined
with functional performance measures, which demonstrate neurophysiological
changes following spinal manipulation in patients with neck pain and dysfunction.
This emerging work may help to explain how critical it is to ensure that neck and
spine issues are identified and treated in patients attempting to reestablish correct
sensorimotor integration during rehabilitation.

1 Introduction

Sensorimotor integration (SMI) is the ability of the central nervous system (CNS)
to integrate afferent (incoming) information from different body parts and
formulate appropriate motor outputs to muscles. We each have an internal
representation of our body that allows us to perform motor tasks by perceiving the
location of our limbs in space (kinesthesia), and in different postural positions.
The internal body map facilitates motor function by integrating incoming sensory
information in relation to this internal map so that appropriate motor responses can
be formulated. The neck is linked biomechanically and neurologically to the upper
limb and yet we know very little about how altering feedback from the neck may
affect SMI from the upper limbs.
Patients with upper limb paresis and prostheses often undergo prolonged
alterations in neck posture and the potential for fatigue, which is highly likely to
impair upper limb sensorimotor integration. Additionally, these postural stressors
are likely to lead to restricted mobility and pain the neck region. There is a
growing body of evidence for impaired neuromuscular and proprioceptive

*
Corresponding author.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 113
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_21, © Springer International Publishing Switzerland 2014
114 B. Murphy and H. Haavik

function in patients with back and neck pain which may explain why what starts as
small areas of restricted movement and/or mild pain becomes chronic pain [1-11].
There is also accumulating evidence that neck manipulation can induce changes in
central nervous system (CNS) function including reflex excitability, cognitive
processing, sensory processing and motor output [12-15] suggesting that spinal
manipulation may have a positive neuromodulatory effect that plays a role in far
more than just pain management. A recent review, by Haavik-Taylor and Murphy
[16], presented evidence suggesting that altered sensory feedback from areas of
joint dysfunction could lead to faulty sensorimotor integration due to central
neuroplastic changes. We further hypothesised that improving spinal dysfunction
would normalize afferent input, which in turn would normalize sensorimotor
integration.
Taken together this growing body of work suggests that altered afferent
(sensory) feedback from a dysfunctional neck or spine affects the way that other
somatosensory feedback from the spine and limbs is received and processed, thus
leading to altered sensorimotor integration (SMI) of the input.

2 Methods

This presentation presents emerging research on the effects of spinal manipulation


on sensory processing, motor output, functional performance and sensorimotor
integration. It discusses a series of experiments using somatosensory evoked
potentials (SEPs), transcranial magnetic stimulation (TMS), electromyography
(EMG) combined with functional performance measures, which demonstrate
neurophysiological changes following spinal manipulation.

3 Conclusion

Spinal manipulation of dysfunctional areas of the neck has been to enhance motor
learning as well as changing the degree of cerebellar inhibition in response to a
motor learning task. This emerging work may help to explain how an initial
episode(s) of back or neck pain may lead to ongoing changes sensorimotor
integration which affect performance.

Acknowledgment. This study was partially funded by the Australian Spinal Research
Foundation, Natural Sciences and Engineering Research Council of Canada, the Canada
Foundation for Innovation and the Ontario Ministry of Research and Innovation.

References
[1] Branstrom, H., Malmgren-Olsson, E.B., Barnekow-Bergkvist, M.: Balance
performance in patients with Whiplash Associated Disorders and Patients with
prolonged Musculoskeletal Disorders. Advances in Physiotherapy 3, 120–127 (2001)
The Role of Spinal Manipulation in Modulating Neuroplasticity 115

[2] Karlberg, M., Persson, L., Magnusson, M.: Reduced postural control in patients with
chronic cervicobrachial pain syndrome. Gait and Posture 3, 241–249 (1995)
[3] Michaelson, P., et al.: Vertical Posture and Head Stability in Patients with Chronic
Neck Pain. Journal of Rehabilitation Medicine 35(5), 229–235 (2003)
[4] Persson, L., Karlberg, M., Magnusson, M.: Effects of different treatments on postural
performance in patients with cervical root compression: A randomized prospective
study assessing the importance of the neck in postural control. Journal of Vestibular
Research 6(6), 439–453 (1996)
[5] Rubin, A.M., et al.: Postural stability following mild head or whiplash injuries. The
American Journal of Otology 16(2), 216–221 (1995)
[6] Stapley, P.J., et al.: Neck muscle fatigue and postural control in patients with
whiplash injury. Clinical Neurophysiology 117(3), 610–622 (2006)
[7] Barton, P., Hayes, K.: Neck flexor muscle strength, efficiency, and relaxation times in
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[8] Falla, D., Bilenkij, G., Jull, G.: Chronic neck pain patient demonstrate altered patterns
of muscle activation during performance of a functional upper limb task. Spine 29, 13
(2004)
[9] Falla, D., et al.: Neuromuscular efficiency of the sternocleidomastoid and anterior
scalene muscles in patients with chronic neck pain. Disability and Rehabilitation
26(12), 712–717 (2004)
[10] Falla, D., et al.: Myoelectric Manifestations of Sternocleidomastoid and Anterior
Scalene Muscle Fatigue in Chronic Neck Pain Patients. Clin. Neurophysiol. 114, 488–
495 (2003)
[11] Gogia, P.P., Sabbahi, M.A.: Electromyographic analysis of neck muscle fatigue in
patients with osteoarthritis of the cervical spine. Spine 19(5), 502–506 (1994)
[12] Herzog, W., Scheele, D., Conway, P.J.: Electromyographic responses of back and
limb muscles associated with spinal manipulative therapy. Spine 24(2), 146–153
(1999)
[13] Murphy, B., Dawson, N., Slack, J.: Sacroiliac joint manipulation decreases the H-
reflex. Electromyography and Clinical Neurophysiology 35(2), 87–94 (1995)
[14] Suter, E., et al.: Decrease in quadriceps inhibition after sacroiliac joint manipulation
in patients with anterior knee pain. Journal of Manipulative & Physiological
Therapeutics 22(3), 149–153 (1999)
[15] Suter, E., et al.: Conservative lower back treatment reduces inhibition in knee-
extensor muscles: a randomized controlled trial. Journal of Manipulative &
Physiological Therapeutics 23(2), 76–80 (2000)
[16] Haavik, H., Murphy, B.: The role of spinal manipulation in addressing disordered
sensorimotor integration and altered motor control. Journal of Electromyography and
Kinesiology 22(5), 768–776 (2012)
Mathematical Modeling in Neuromodulation
for Pain Relief

Carsten Dahl Mørch

Center for Sensory-Motor Interaction,


Aalborg University, Aalborg, Denmark

Abstract. Neuromodulation has been used for activation of the nervous system to
cause pain relief for more than a half century. Mathematical modelling is being
used gain better understanding of the neuromodulatory methods and to facilitate
electrode design. Here the well-known method of spinal cord stimulation and the
more resent method of peripheral nerve field stimulation will be discussed in
relation to relief of low-back pain.

1 Introduction

Several neural targets have been approached for electrical activation of the central
nervous system aiming causing pain relief. This form of neuromodulation for pain
relief dates back to the formulation of the gate control theory proposed by
Melzack and Wall in 1965 [1]. Despite the fact that neuromodulation methods
have proven clinically effective for pain relief only little is known about the
mechanisms of action. Therefore, mathematical modelling has been used to
investigate the possible neural target of the electrical stimulation, how the
nerve fibers are activated by the stimulation, and to some extent, the impact on the
CNS.

2 Principles of Modeling Neuromodulation

Mathematical models of electrical stimulation of the nervous system are most


often done by two step approach. Initially, the current flow and thus the electrical
field are estimated in the tissue in which the nerve fibers are embedded. These
volume conductor estimations are often performed by finite element models. From
these models the extracellular potentials at the nodes of Ranvier along the nerve
fiber can readily be extracted. As the second step a model for nerve fiber
activation is established and neural responses such as the activation threshold of
particular fiber types are estimated. Several types of nerve fiber models have been
used, ranging from passive cable models [2] to models explicitly describing the
ion currents both in the nodes of Ranvier and the internodes [3].

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 117
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_22, © Springer International Publishing Switzerland 2014
118 C.D. Mørch

2.1 Spinal Cord Stimulation


Neuromodulation for low-back pain relief is often performed by placing the
electrode dorsal to the spinal cord [4]. The pain-relieving mechanisms remains
unclear but several mechanisms may play a role e.g.: a gating effect of incoming
nociceptive stimuli in the dorsal horn of the spinal cord [5] and an activation of
descending pain inhibitory pathways via supraspinal mechanisms [6]. To estimate
the neural targets activated by spinal cord stimulation, mathematical models have
been established. The models have helped clarifying several aspects of the
method, e.g. which fibers are activated [7], and the importance of stimulation
settings such as the pulse width selected during spinal cord stimulation for relief
of low-back pain [8].

2.2 Peripheral Nerve Field Stimulation


While spinal cord stimulation often alleviates pain radiation to the legs the axial
low-back pain sometimes prove more resilient to the treatment. It has therefore
been proposed to implant the electrodes in the subcutaneous tissue at the focal site
of the experienced pain [9]. A specific nerve is not targeted during this procedure
but the smaller branches of the cutaneous nerve fibers appears to be the neural
target, thus the name peripheral nerve field stimulation. While the mechanisms of
peripheral nerve field stimulation remain unclear, mathematical modeling has
described the nerve fibers being activated and proposed the optimal depth of
implantation [10].

3 Conclusion
Mathematical modelling of neuromodulation for pain relief has proven useful,
especially in the design of electrical leads, but also for the understanding of the
nerves being activated during the stimulation. However, it should be stressed that
the accuracy of the models are reliant on accuracy of many parameters in the
models, such as the conductivity of the tissue, the location and anatomy of the
targeted nerves, and membrane properties of the nerve fibers.

Acknowledgment. The author acknowledges the support from Medtronic Inc.

References
1. Melzack, R., Wall, P.D.: Pain mechanisms - A new theory. Science 150(3699), 971–
979 (1965)
2. Mørch, C.D., Hennings, K., Andersen, O.K.: Estimating nerve excitation thresholds to
cutaneous electrical stimulation by finite element modeling combined with a stochastic
branching nerve fiber model. Medical and Biological Engineering and
Computing 49(4), 385–395 (2011)
Mathematical Modeling in Neuromodulation for Pain Relief 119

3. McIntyre, C.C., Richardson, A.G., Grill, W.M.: Modeling the excitability of


mammalian nerve fibers: Influence of afterpotentials on the recovery cycle. J.
Neurophysiol. 87(2), 995–1006 (2002)
4. Kumar, K., Taylor, R.S., Jacques, L., Eldabe, S., Meglio, M., Molet, J., et al.: Spinal
cord stimulation versus conventional medical management for neuropathic pain: A
multicentre randomised controlled trial in patients with failed back surgery syndrome.
Pain 132(1-2), 179–188 (2007)
5. Linderoth, B., Meyerson, B.A.: Spinal cord stimulation: Exploration of the
physiological basis of a widely used therapy. Anesthesiology 113(6), 1265–1267
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6. Song, Z., Ultenius, C., Meyerson, B.A., Linderoth, B.: Pain relief by spinal cord
stimulation involves serotonergic mechanisms: An experimental study in a rat model
of mononeuropathy. Pain 147(1), 241–248 (2009)
7. Struijk, J.J., Holsheimer, J., van der Heide, G.G., Boom, H.B.K.: Recruitment of dorsal
column fibers in spinal cord stimulation: influence of collateral branching. IEEE
Transactions on Biomedical Engineering 39(9), 903–912 (1992)
8. Lee, D., Hershey, B., Bradley, K., Yearwood, T.: Predicted effects of pulse width
programming in spinal cord stimulation: a mathematical modeling study. Medical and
Biological Engineering and Computing 49(7), 765–774 (2011)
9. Kloimstein, H., Likar, R., Kern, M., Neuhold, J., Cada, M., Loinig, N., et al.:
Peripheral Nerve Field Stimulation (PNFS) in Chronic Low Back Pain: A Prospective
Multicenter Study. Neuromodulation (in press)
10. Mørch, C.D., Nguyen, G.P., Wacnik, P.W., Andersen, O.K.: Mathematical model of
nerve fiber activation during low back peripheral nerve field stimulation: Analysis of
electrode implant depth. Neuromodulation (in press)
Chiropractic, Cortical Excitability and BCI

Imran Khan Niazi1,2,*, Mads Jochumsen2, Jens Duehr1, Mat Kingett1,


Kim Dremstrup2, and Heidi Haavik1
1
Centre for Chiropractic Research, New Zealand College of Chiropractic,
Auckland, New Zealand PO Box 113-044 Newmarket
2
Department of Health Science and Technology, Aalborg University, Denmark

Abstract. Utilizing transcranial magnetic stimulation (TMS) protocols prior to


and after spinal manipulation, alterations in the activity within specific
intracortical facilitatory and intracortical inhibitory pathways have been observed
to an upper limb muscle (abductor pollicis brevis; APB). This study sought to
investigate whether the previously shown motor control changes could be due to
alterations in recruitment patterns of the APB motor neuron pool following spinal
manipulation. This study also sought to explore whether such neuroplastic
changes in motor control observed following spinal manipulation occur for a
lower limb muscle (Tibialis anterior, TA), and whether at least in part such
changes occur at the cortical level. The preliminary results of this study show that
spinal manipulation leads to lasting changes in cortical excitability, as measured
by a significantly larger MEPmax for TMS induced input output curves in both
the upper and lower limb. These preliminary results also suggest that spinal
manipulation can enhance BCI protocols by increasing movement related cortical
potential (MRCP) amplitudes.

Keywords: Spinal Manipulation, Neural plasticity, BCI.

1 Introduction

Clinical trials and systematic reviews have shown that spinal manipulation is an
effective, low cost treatment option for low back pain [1, 3], neck pain [1, 2] and
headaches (4). However, the mechanism that underpins the functional recovery
and amelioration of painful conditions remains poorly understood. Scientists use
to believe spinal manipulation was a biomechanical treatment option for spinal
pain conditions. Yet the growing basic science evidence suggests there may be
more of a neurophysiological effect following spinal manipulation than previously
realized [5, 6, 7]. Several basic science studies have suggested that these
neurophysiological (plastic) changes observed following manipulation occur at the
cortical level [8-15].

*
Corresponding author.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 121
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_23, © Springer International Publishing Switzerland 2014
122 I.K. Niazi et al.

If manual spinal manipulation does result in lasting increases in cortical


excitability, this could have far-reaching consequences for a variety of patient
populations. It may for example be used in conjunction with other
neuromodulatory techniques such as transcranial direct current stimulation (tDCS)
and paired associated stimulation (PAS) and brain computer interface (BCI) based
paradigms for rehabilitation.
Recently a new method has been proposed to induce changes in cortical
excitability of TA muscle using a BCI protocol [16-17] A BCI system is one that
enables the signal from the brain to control the external device directly, and thus
by-passing the normal pathways. A BCI system proposed by Niazi et al [17] for
induction of changes in cortical excitability is based on precise timing of afferent
feedback from periphery to the most negative part of the brain potential called
movement related cortical potential (MRCP). This initial negative phase of
MRCP is also known as bereitschafts potential (BP) or readiness potential. The BP
consists of a slow decrease in EEG amplitude starting approximately 1500 ms
prior to the onset of the movement, and is considered a cortical representation of
motor preparation [18]. It is also believed that BP may reflect an intention to act
[19] or an index of resource mobilization [20]. Therefore, it has been suggested
that these motor areas are active even if the movement is not executed but only
imagined. BP can be influenced by various factor such as level of intention,
preparatory state, movement selection as to freely selected versus fixed, learning
and skill acquisition, pace of movement repetition, praxis movement, perceived
effort, force exerted, speed and precision of movement, discreteness and
complexity of movement, and pathological lesions of various brain structures. For
Planning and execution of motor commands requires good sensorimotor
integration. Multiple studies have shown that spinal manipulation alters
sensorimotor integration [8-15].We therefore hypothesized that if spinal
manipulation can improve sensorimotor integration this may be reflected in altered
morphology of the MRCP and improved integration of afferent feedback,which
was a crucial element in the MRCP based BCI protocol described [16-17].
This study therefore sought to investigate 1) whether the previously shown
motor control changes could be due to alterations in recruitment patterns of the
APB motor neuron pool following spinal manipulation; 2) whether such changes
would also be seen in TA after spinal manipulation 3) whether such neuroplastic
changes in motor control observed following spinal manipulation at least in part
occur at the cortical level; and 4) whether spinal manipulation can be used in
conjunction with previous BCI protocols based on MRCP to enhance outcomes.

2 Methods

The preliminary study group consisted of 24 subjects (14 male, with 23.7+2.7
years old).To be included, subjects could not have a history of neurologic disease,
or any known contraindications to either spinal manipulation or magnetic
Chiropractic, Cortical Excitability and BCI 123

stimulation. The Northern Y Regional Ethics Committee approved this study (ref:
NTY/07/05/054) in accordance with the Declaration of Helsinki.
Subjects were divided in three groups. In first group (N=8) motor evoked
potentials (MEPs) were recorded from APB of the dominant limb following single
pulse TMS of the contra-lateral motor cortex before and after either a spinal
manipulation intervention or a control intervention. F waves were also recorded in
this group pre and post spinal adjustment and control session also to assess the
spinal pathways. In second group (N=8) motor evoked potentials (MEPs) were
recorded from the right tibialis anterior (TA) following single pulse TMS before
and after a spinal manipulation intervention. In third group (N=8 movement
related cortical potential (MRCP) were recorded for morphological analysis prior
to and following a spinal manipulation intervention. The amplitude of the early
bereitschafts potential (EBP), the amplitude of the late bereitschafts potential
(LBP) and the amplitude of peak negativity (PN) alongside their latency with
respect to onset of task was calculated .Rebound rate of movement monitoring
potential (last part of MRCP) were analyzed as a control parameter also.
Participants were randomly allocated to groups.
TMS recruitment curves were compiled from the averages of ten MEP
amplitudes recorded at each of five different stimulus intensities (90%, 100%,
110%, 120% and 130% of rest threshold; RTh). A three-way repeated measures
ANOVA with factors intervention (cervical spinal manipulation and PHM), ‘time’
(pre, and post0), and ‘stimulus intensity’ (90%, 100%, 110%, 120% and 130%
RTh) was used to investigate the effects of the interventions on the changes in the
MEP amplitude on upper limb muscle (ABP). A two-way ANOVA with factors
‘time’ (pre and post), and ‘stimulus intensity’ (90%, 100%, 110%, 120% and
130% RTh) was used to investigate changes in MEP size prior to and following a
full spinal manipulation on lower limb muscle (TA). One way ANOVA were used
to find the changes in M-wave and F-wave parameters (amplitude and persistence)
with ‘intervention’ (spinal manipulation vs control) as factor. Also for MRCP
morphological parameters (amplitudes and latencies) one way ANOVA was used.
Paired t-tests were used to assess changes in the parameters of the input-output
curve (MEPmax, S50, the slope and the r2 value). For all experiments, statistical
significance was set to P < 0.05.

3 Preliminayry Results

Following spinal manipulations on average across subjects MEPmax for ABP was
significantly increased by 89±95% (P=0.01) whereas control session showed no
significant changes. Similarly for lower limb MEPmax of TA muscle was
significantly increased by 53±46% (P=0.01). The S50-variable and the slope
parameter k of the Boltzmann-fitted data remained unchanged. No changes were
observed following the control intervention. No changes in F-wave parameters
were observed for either intervention. All parameters of latencies of MRCP were
non-significant prior to and after the intervention session. But significant
124 I.K. Niazi et al.

difference (P<0.05) were found for the amplitudes of early BP, the late BP and
also for peak negativity.

4 Discussion

The preliminary results of this study add to the growing body of evidence that
shows spinal manipulation leads to neuroplastic changes in cortical excitability of
both upper and lower limb muscles. As MEPmax reflects the plateau of the
recruitment curve, which is thought to represent the balance of complex excitatory
and inhibitory components of the corticospinal volley, the results therefore
suggests that spinal manipulation alters the balance between excitatory and
inhibitory components of the corticospinal volley. This is in accordance with an
earlier TMS study that found muscle specific changes in intracortical inhibitory
and excitatory pathways following spinal manipulation [9]. These results also
suggest that spinal manipulation has lead to neuroplastic changes that at least in
part occur at the cortical level, as the amplitude of the early BP is known to reflect
processing in supplementary motor cortex (SMA) and that of late BP in premotor
cortex. It has been suggested that an increase in the amplitude of the MRCP is an
indication of increased cortical drive to the muscle [21]. A stronger central
command could recruit the motor units that otherwise would be inactive in an
untrained state and/or drive the active motor units to higher intensities (i.e. higher
discharge rate), leading to greater muscle forces [21].
In conclusion spinal manipulation appears to increase corticospinal excitability
for both upper and lower limb muscles, these changes at least in part occur at the
cortical level, and it appears that spinal manipulation can also be used in
conjunction with BCI based on MRCP to improve outcomes.

Acknowledgment. This study was partially funded by the Australian Spinal Research
Foundation, Hamblin Chiropractic Research Fund Trust, the New Zealand College of
Chiropractic and the New Zealand College of Chiropractic Research Supporters
Programme.

References
[1] Bronfort, G., Haas, M., Evans, R.L., Bouter, L.M.: Efficacy of spinal manipulation
and mobilization for low back pain and neck pain: a systematic review and best
evidence synthesis. Spine J. 4, 335–356 (2004)
[2] Bronfort, G., Evans, R., Anderson, A.V., Svendsen, K.H., Bracha, Y., Grimm, R.H.:
Spinal manipulation, medication, or home exercise with advice for acute and subacute
neck pain: a randomized trial. Ann. Intern. Med. 156, 1–10 (2012)
[3] Kuczynski, J.J., Schwieterman, B., Columber, K., Knupp, D., Shaub, L., Cook, C.E.:
Effectiveness of physical therapist administered spinal manipulation for the treatment
of low back pain: a systematic review of the literature. Int. J. Sports Phys. Ther. 7,
647–662 (2012)
Chiropractic, Cortical Excitability and BCI 125

[4] Gross, A., Miller, J., D’Sylva, J., Burnie, S.J., Goldsmith, C.H., Graham, N., Haines,
T., Bronfort, G., Hoving, J.L.: Manipulation or mobilisation for neck pain. Cochrane
Database Syst. Rev. 15, 315–333 (2010)
[5] Pickar, J.G.: Neurophysiological effects of spinal manipulation. Spine J. 2, 357–371
(2002)
[6] Haavik, H., Murphy, B.: The role of spinal manipulation in addressing disordered
sensorimotor integration and altered motor control. J. Electromyogr. Kinesiol. 22,
768–776 (2012)
[7] Henderson, C.N.: The basis for spinal manipulation: Chiropractic perspective of
indications and theory. J. Electromyogr. Kinesiol. 22(5), 632–642 (2012)
[8] Haavik Taylor, H., Murphy, B.: Transient modulation of intracortical inhibition
following spinal manipulation. Chiropractic J. Australia 37, 106–116 (2007)
[9] Haavik Taylor, H., Murphy, B.: Altered sensorimotor integration with cervical spine
manipulation. J. Manipulative Physiol. Ther. 31, 115–126 (2008)
[10] Haavik, H., Murphy, B.: Subclinical neck pain and the effect of cervical manipulation on
elbow joint position sense. Journal of Manipulative and Physiological Therapeutics 34,
88–97 (2011)
[11] Haavik Taylor, H., Murphy, B.: Cervical spine manipulation alters sensorimotor
integration: A somatosensory evoked potential study. Clinical Neurophysiology 118(2),
391–402 (2007)
[12] Haavik Taylor, H., Murphy, B.: Altered Central Integration of Dual Somatosensory
Input Following Cervical Spine Manipulation. Journal of Manipulative &
Physiological Therapeutics 33(3), 178–188 (2010)
[13] Haavik Taylor, H., Murphy, B.: The effects of spinal manipulation on central
integration of dual somatosensory input observed following motor training: A
crossover study. Journal of Manipulative & Physiological Therapeutics 33(4), 261–
272 (2010)
[14] Marshall, P., Murphy, B.: The Effect of Sacroiliac Joint Manipulation on Feed-
Forward Activation Times of the Deep Abdominal Musculature. Journal of
Manipulative and Physiological Therapeutics 29(3), 196–202 (2006)
[15] Haavik, H., Murphy, B.: The role of spinal manipulation in addressing disordered
sensorimotor integration and altered motor control. Journal of Electromyography and
Kinesiology 22(5), 768–776 (2012)
[16] Mrachacz-Kersting, N., Kristensen, S.R., Niazi, I.K., Farina, D.: Precise temporal
association between cortical potentials evoked by motor imagination and afference
induces cortical plasticity. J. Physiol (Lond.) 590, 1669–1682 (2012)
[17] Niazi, I.K., Mrachacz-Kersting, N., Jiang, N., Dremstrup, K., Farina, D.: Peripheral
electrical stimulation triggered by self-pace detection of motor intention enhances
corticospinal excitability. IEEE Transaction on Neural Systems and Rehabilitation
Engineering 20, 595–604 (2012)
[18] Jahanshahi, M., Hallett, M.: The Bereitschaftspotential, 1st edn. Springer (2003)
[19] Libet, B., Gleason, C.A., Wright, E.W., Pearl, D.K.: Time of conscious intention to
act in relation to onset of cerebral activity (readiness-potential). The unconscious
initiation of a freely voluntary act. Brain 106, 623–642 (1983)
[20] McCallum, W.C., Curry, S.H.: Slow Potential Changes in the Human Brain. Springer
(1993)
[21] Ranganathan, V.K., Siemionow, V., Liu, J.Z., Sahgal, V., Yue, G.H.: From mental
power to muscle power–gaining strength by using the mind. Neuropsychologia 42(7),
944–956 (2004)
Abstract: Technical Device for Measurement
of Spasticity, Developed for Bedside Use

Tue Hvass Petersen

Research Unit on Brain Injury Neurorehabilitation Copenhagen


Copenhagen, Denmark
www.rubric.info

Spasticity, contractures and dystonia contribute to the overall increase in joint


stiffness, abnormal posture and decreased joint mobility observed in neurological
patients during clinical rehabilitation. In the clinical setting, these symptoms are
currently treated with intensive physiotherapy, by means of early mobilization of
the patient to prevent contractures, spasticity reducing medication such as
baclofen to reduce stretch reflex sensitivity, and botulinum toxin to reduce
intermittent or sustained (dystonic) muscle activation, which eventually may lead
to abnormal postures. Some challenges, however, exist for the correct diagnosis,
choice of treatment strategies, and measuring the outcome of such strategies.
Scales such as the Modified Ashworth Scale (MAS) and the Modified Tardieu
Scales (MTS) are widely used in the clinic to assess spasticity. Both scales rely on
stretches of the affected muscle at one or more velocities to determine the velocity
dependent increase in reflex stiffness. The reliability of both the MAS and MTS
for measuring spasticity in both upper and lower limb muscles has been
investigated in a number of studies (Yam and Leung, 2006, Tederko et al., 2007,
Ansari et al., 2008, Craven and Morris, 2010, Ghotbi et al., 2011). The results are
largely varying and likely confounded by a number of factors such as the patient
group selected, experience of the rater etc. In adult patients with severe brain
injuries, the test-retest reliability has been found to be good, however with limited
inter-rater reliability(Mehrholz et al., 2005a, Mehrholz et al., 2005b)
One important problem with the current scoring scales is, however, their
inability to adequately measure and distinguish the underlying neural and
muscular components that contribute to the overall increase in joint stiffness in
neurological patients. For example, it was demonstrated two decades ago using a
biomechanical device to evaluate spasticity, that the stretch reflex stiffness seen in
patients with spastic hemiparesis was within the limits of the reflex stiffness found
in healthy controls(Sinkjaer et al., 1993, Sinkjaer and Magnussen, 1994). On the
other hand these patients had a significantly larger passive stiffness (related to
changes in tendon and muscle tissue) than did control subjects. However, treating
these patients with anti-spastic medication would be of little value, yet it depends
on the correct diagnosis. Measurements were performed using a stationary
apparatus. In patients with severe brain lesions due to traumatic brain injury stroke

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 127
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_24, © Springer International Publishing Switzerland 2014
128 T.H. Petersen

or other conditions, it is however not possible to perform these types of


assessments and therefore a portable biomechanical device to measure joint
stiffness at bedside would be valuable for clinicians in neurological settings.
In this talk, I will present the background, thoughts and ideas behind a newly
developed portable spasticity assessment device developed by Movotec
(Denmark), The Helene Elsass Center and The Department of Traumatic Brain
Unjury at Glostrup Hospital. I will present preliminary data from reliability tests
of the device together with data from patients suffering from severe traumatic
brain injury.

References
Ansari, N.N., Naghdi, S., Arab, T.K., Jalaie, S.: The interrater and intrarater reliability of
the Modified Ashworth Scale in the assessment of muscle spasticity: limb and muscle
group effect. NeuroRehabilitation 23, 231–237 (2008)
Craven, B.C., Morris, A.R.: Modified Ashworth scale reliability for measurement of lower
extremity spasticity among patients with SCI. Spinal Cord 48, 207–213 (2010)
Ghotbi, N., Nakhostin Ansari, N., Naghdi, S., Hasson, S.: Measurement of lower-limb
muscle spasticity: intrarater reliability of Modified Modified Ashworth Scale. Journal of
Rehabilitation Research and Development 48, 83–88 (2011)
Mehrholz, J., Major, Y., Meissner, D., Sandi-Gahun, S., Koch, R., Pohl, M.: The influence
of contractures and variation in measurement stretching velocity on the reliability of the
Modified Ashworth Scale in patients with severe brain injury. Clinical Rehabilitation 19,
63–72 (2005a)
Mehrholz, J., Wagner, K., Meissner, D., Grundmann, K., Zange, C., Koch, R., Pohl, M.:
Reliability of the Modified Tardieu Scale and the Modified Ashworth Scale in adult
patients with severe brain injury: a comparison study. Clinical Rehabilitation 19, 751–
759 (2005b)
Sinkjaer, T., Magnussen, I.: Passive, intrinsic and reflex-mediated stiffness in the ankle
extensors of hemiparetic patients. Brain: A Journal of Neurology 117(Pt. 2), 355–363
(1994)
Sinkjaer, T., Toft, E., Larsen, K., Andreassen, S., Hansen, H.J.: Non-reflex and reflex
mediated ankle joint stiffness in multiple sclerosis patients with spasticity. Muscle &
Nerve 16, 69–76 (1993)
Tederko, P., Krasuski, M., Czech, J., Dargiel, A., Garwacka-Jodzis, I., Wojciechowska, A.:
Reliability of clinical spasticity measurements in patients with cervical spinal cord
injury. Ortopedia, Traumatologia, Rehabilitacja 9, 467–483 (2007)
Yam, W.K., Leung, M.S.: Interrater reliability of Modified Ashworth Scale and Modified
Tardieu Scale in children with spastic cerebral palsy. Journal of Child Neurology 21,
1031–1035 (2006)
Game Engines and Exergames to Guide
Rehabilitation at Home

Michele Pirovano1,2, Renato Mainetti1, Pier Luca Lanzi2,


and Nunzio Alberto Borghese1
1
Applied Intelligence Laboratory (ais-lab-di.unimi.it),
Department of Computer Science, University of Milano, Milan, Italy
{miche le.pirovano,renato.mainetti,
alberto.borghese}@unimi.it
2
Dipartimento di Elettronica, Informatica e Bioingegneria, Politecnico di Milano,
Milan, Italy
pierluca.lanzi@polimi.it

Abstract. Rehabilitation is now more costly than ever and novel solutions are
needed to cope with such increasing costs. Exergames at home can be a viable
solution, allowing the patients to exercise in the comfort of their own home while
playing simple games. However, to provide all the functionalities that a traditional
therapy would, an adequate architecture is needed: the exergames should provide,
in addition to the game itself, monitoring, tracking, configuration, adaptation and
motivation. We show how integrating computational intelligence inside a game
engine, full gamification of rehabilitation sessions can be achieved.

1 Introduction

Physical and cognitive rehabilitation asks patients to perform prolonged and


straining efforts in order to improve or stabilize their condition. This has the form
of repetitive exercises that are aimed to stimulate the Central Nervous System at
restoring functional circuits damaged by a stroke, a trauma or a disease. Such
exercises should be performed on a regular basis, possibly daily, to recover lost
functionalities also months after the stroke event [3, 7]. On the other hand, costs of
rehabilitation have risen considerably in the last years and, given the increase of
elder population, figures projections are not favorable: more and more people
nowadays are in need of rehabilitation and the health providers cannot cope with
the costs. For this reason, new ways to provide rehabilitation to patients are
needed.
One way to reduce the costs, while maintaining or even improving the service
level, is moving rehabilitation at home and making the patient autonomous: the
patient will perform the exercises needed to regain her lost functionality in her
own house autonomously, integrating the exercises in a daily schedule, thus
reducing the need of one-to-one sessions with the therapist. If possible, this

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 129
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_25, © Springer International Publishing Switzerland 2014
130 M. Pirovano et al.

solution would also allow patients to perform intensive rehabilitation without


being subjugated to the hassle of frequent commuting to a rehabilitation center [6].
We describe here the functionalities, based on computational intelligence, that
we have developed and integrated inside a game engine do provide the patient
with the capability to exercise at home safely and effectively, in a still supervised
way. The novel game engine, named IGER (Intelligent Game Engine for
Rehabilitation) has been already used to develop twenty exer-games that address
posture, arm and neglect rehabilitation.

2 Methodology
Traditional rehabilitation requires a therapist to suggest the exercises to the
patient, configure them at the proper difficult level, monitor the patient’s
movements and motivate her, especially to complete the most difficult exercises.
These features need to be present in some form also when rehabilitation is carried
out at home, without the physical presence of the therapist; otherwise exercising
could become easily ineffective or, even worse, dangerous. For this reason,
monitoring, configuration and motivation should be on the podium when
designing a rehabilitation-at-home architecture. The therapist needs to be inserted
into the loop, to schedule an adequate rehabilitation program for a given patient
and evaluate the patient performance.
Motivation is also an important issue in rehabilitation, and even more so in at-
home rehabilitation, as the lack of a physical person helping out could kill the
motivation of the patient very quickly. For this reason, experts have been scouting
other fields in order to find alternative sources of motivation. The now so popular
trend of gamification [4] proposes a solution to this problem through exergames.
Exergames are exercises, in our case rehabilitation exercises, hidden under the
coat of fun and compelling games. Since exercising requires large efforts from
the patient, and it may even be outright boring, the added gaming aspects can tip
the scales of motivation.
Fun and play are not the sole ingredients that we can borrow from the gaming
field. From videogames, we acquire the concept of game engine: a set of tools
that, on one end, make the games run on the machine they are designed for and, on
the other end, help the developer in creating games that share the same features.
Since rehabilitation exercises can be very different, and the patients may vary
greatly in their skills and needs, an integrated engine that can be used to create
multiple game versions, while maintaining a set of shared features that validate
such games from a therapeutic point of view, can make all the difference.
The hereabove elements have been incorporated in the design of the IGER
system [1] developed inside the REWIRE project, aimed at bringing rehabilitation
to the patient’s home. IGER provides the patient with an integrated environment
to play a set of rehabilitation exergames, specifically designed for the patient’s
condition.
IGER works in combination with a scheduling and assessment system, installed
at the hospital site. Such system will provide the definition of rehabilitation
Game Engines and Exergames to Guide Rehabilitation at Home 131

sessions in terms of exer-games mix and duration, and of their parameters and will
allow to review the exercise data for assessment and tuning the therapy.
To design the exer-games we have started from the exercises defined by the
therapists and built upon them suitable games that can guide the patient through
the exercise [2]. A set of parameters are identified (e.g. amplitude of motion, pace)
that are linked to game parameters. Such parameters can be configured by the
therapist in the hospital, thus providing a proper challenge level on one side, and
an exercise difficulty adequate to the patient’s state on the other. Such parameters
can be further adapted during gaming itself, by monitoring the success rate, thus
making the game easier if patient’s success is low and vice-versa. This allows the
patient to keep motivation on one side and to fine tune the difficulty level to the
current patient state.
A large effort has been developed to provide an effective and clear monitor.
This requires the development of a system to define which are the rules and
conditions that the patient has to satisfy while exercising and how to provide her a
visual feed-back while gaming. Fuzzy systems have been selected for the first
task, because of their natural way of transferring structured knowledge into rules
when no clear boundaries on the conditions can be set. The therapist will set
constraints on the movements inside the hospital when programming the
exercises, according to patient’s idiosyncrasies and needs. Such rules can be
provided through a graphical interface to make the work of the therapist easier.
They are then automatically transferred into fuzzy rules that are associated to an
alarm level that increases the closest the patient gets to the rule boundary. For
instance, if the maximum right lateral bending is set to 30 degrees, the alarm level
increases with bending and reaches a maximum at 30 degrees. Several solutions
have been tested to provide a feed-back on the alarm level: smileys or other
cartoon-like feed-back shown in a given position of the display turned out not
particularly effective as they go unnoticed. The most effective and compliant
solution is to transform the alarm level into a color that is used to paint the avatar
that represents the patient inside the exer-game. This has a double result: to
provide an informative feed-back on which body segment is moving wrongly as
the patient can see that particular body segment changing color, and a clear feed-
back as the feed-back is provided on the avatar that is always on the patient focus.
Monitors can be prioritized so that some will be associated to a maximum
alarm at mild level, while others are more critical and will produce an alarm at
maximum level. In this latter case a virtual therapist is shown on the screen. It will
advise the patient on how to perform the correct movements through audio-visual
feed-back and then allow her to resume exercising.
The virtual therapist is the first element of gamification, while rewards and a
balanced scoring system, as well as a surprise element that is issued upon correctly
completing the exercises, are the other critical elements that allow patients to be
attracted to exercising.
To allow most different rehabilitation needs that call for different tracking
devices, we have designed a specific middleware between the game engine and
the input devices that allows to integrate the most different input devices, provided
132 M. Pirovano et al.

that they can provide the data flow required for monitoring, gameplay and
assessment. In this way, the same game can be played for posture rehabilitation
(through shifting the body weight laterally) or for arm and neglect rehabilitation
(moving the arm). Such exer-game is for instance the “Bubbles” game that
requires popping bubbles inside a boiling cauldron (Fig. 1a). In the first case a
balance board and Kinect are used as input devices, in the second case a robot arm
or a haptic input device has been adopted.
Lastly a fully Natural Interfacing modality has been fostered: after switching on
the PC, the IGER system is automatically started and the patient can forget about
the PC and use gestures or voice to exercise with a more natural interfacing with
the system. She even forgets that there is a PC controlling all the operations.

3 Discussion and Conclusion

A set of twenty exer-games has been fully developed and they are presently under
testing with patients inside the REWIRE system at Virgin de Rocìo hospital in
Seville and at Cereneo clinic in Vitznau (Zurich). Figure 1 reports three of these
games: the first one is Bubbles, the second one, Firefighter, requires that the patient
does steps over 360 degrees to extinguish a virtual fire. Horse Running guides the
patient to do sit to stand movements and monitors that force is equally distributed
among the two legs. All games have a light-hearted cartoon style to make them
pleasant and enjoyable on one side and provide a low cognitive load on the other
side. Moreover, music upon choice of the patient is played in the background.
Preliminary tests on elders and patients that accepted to use the system on a
voluntary basis to provide feed-back on usability and compliance have shown a
large interest from patients and all the potentiality.
Monitoring has the critical role to guarantee safety to the patient. Recently, a
few studies have explored autonomous rehabilitation at home and they report
drop-outs because of pain and similar issues developed during the system use [5].
These are likely due to excessive loading of the unimpaired limb. This is one of
the main limitations of the use of exer-games developed for fitness. In fact, they
guide the users through exercises by providing cues for actions, but do not care on
the reason why the exercises are carried out. Indeed, healthy people are likely to
produce the elicited movements in a “correct” way. This is not the case of
impaired people, who tend to use and trust more their unimpaired body segments
especially in the challenging situations like those required to rehabilitate.
Therefore, on one side, we need challenging exer-games, on the other side
challenging exer-games would induce patients to excessively use their unimpaired
body parts with two nasty results: maladaptation (learning unhealthy motor
strategies) and wearing of joints. This should clearly be avoided to avoid that
rehabilitation becomes harmful. This is the role of the monitoring system
developed inside IGER. This works in combination with the adaptation module:
whenever the monitoring system detects wrong movements, it intervenes warning
the patient on one side and decreasing the difficulty level on the other, to allow the
patient to do slower movements but more appropriately.
Game Engines and Exergames to Guide Rehabilitation at Home 133

Fig. 1 Three of the exer-games implemented with IGER and currently tested with patients.
On the top “Bubbles” (a) guides the patient to explore the 3D space. It can be played either
by moving the body around (body shift). In this case, a balance board can be used to track
accurately the center of pressure. Kinect could be used for monitoring for instance that the
back is not tilt or that knees are not bent. Bubbles can be played also with a haptic device
like the Novint Falcon. The patient sits in front of the TV and guides the stick to bump into
the balls to pop them. This allows both eliciting arm movements and exploring the
(neglected) space In the middle (b) “Firefighter” guides the patient to do steps in all
directions. The stability of the step, the time required to complete the movement are all
parameters used for assessment. In the bottom table (c) “Horse running” is shown. This exer-
game guides the patient in sit-to-stand movements. The patient sits on a chair in front of the
monitor: if he stands up the horse runs faster and he is able to catch more honey bottles.
However, he must be careful not to hit tree branches on the course and has to sit down in
time. This game hides the effort in standing up with the game reward and challenge.
Nevertheless standing up should be carried out using the two sides of the body most equally.
134 M. Pirovano et al.

Fig. 1 (continued)

Acknowledgment. This work has been partially supported by the FP7 Project REWIRE,
grant N. 287713, of the European Union (EU).

References
[1] Pirovano, M., Mainetti, R., Baud-Bovy, G., Lanzi, P.L., Borghese, N.A.: Self-Adaptive
Games for Rehabilitation at Home. IEEE Trans. on CIAIG (under revision)
[2] Borghese, N.A., Pirovano, M., Lanzi, P.L., Wüest, S., De Bruin, E.: Computational
Intelligence and Game Design for Effective At-Home Stroke Rehabilitation. Games
For Health Journal (April 2013)
[3] Feys, H.M., De Weerdt, W.J., Selz, B.E., Cox Steck, G.A., Spichiger, R., Vereeck,
L.E., Putman, K.D., Van Hoydonck, G.A.: Effect of a therapeutic intervention for the
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[4] Deterding, S., Sicart, M., Nacke, L., O’Hara, K., Dixon, D.: From Game Design
Elements to Gamefulness: Defining ‘Gamification’. In: Proceedings of the 15th
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[5] Prosperini, L., Fortuna, D., Giannì, C., Leonardi, L., Marchetti, M., Pozzilli, C.: Home-
based Training Using the Wii Balance board: a Randomized, Corssover Pilot Study in
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[6] Ruiva, J.A., Exergames, J.A.: cardiac rehabilitation: a review. J. Cardiopulm. Rehabil.
Prev. 34(1), 2–20 (2014)
[7] Langhorne, P., Coupar, F., Pollock, A.: Motor recovery after stroke: a systematic
review. The Lancet Neurology 8, 741–754 (2009)
[8] Wüest, S., Borghese, N.A., Pirovano, M., Mainetti, R., van de Langenberg, R., de
Bruin, E.D.: Usability and Effects of an Exergame-Based Balance Training Program.
Games for Health Journal 3(2), 106–114 (2014), doi:10.1089/g4h.2013.0093
Mechanims

Mechanism of Spinal Cord and Peripheral


Nerve Stimulation: More than the Gate Control
Theory

Louis Vera-Portocarrero

Global Research, Medtronic Neuromodulation


Minneapolis, Minnesota, USA

1 Introduction

The use of electricity for the treatment of pain has been around since ancient
times. It was not until the second half of the 20th century with the advent of the
gate control theory that an explanation for its effects was put forward [1]. In the
time since the postulation of this theory, there have been several advances using
animal models of pain and neuromodulation that are shedding more light into the
neurobiology of electrical stimulation for pain. The work has revealed that there
are more mechanisms and areas of the nervous system involved in the effects of
electrical stimulation than what would be predicted by the gate control theory.
Higher brain centers are activated when stimulation is applied to the dorsal
columns as in spinal cord stimulation [2]. Likewise, SCS influences peripheral
targets by antidromic pulses traveling in the dorsal columns and into peripheral
afferents [3]. These same pulses can influence intrinsic pain process in the dorsal
horn by modulating the release of different neurotransmitters [4] (Figure 1). The
mechanisms behind the effects of subcutaneous electrical stimulation are much
less understood than the mechanisms for SCS. The lack of animal models
necessary to study mechanisms has hindered this understanding until recently. A
novel model of SQS has been developed in rodents and this model has proven to
mimic some of the aspects of clinical practice. When compared with a rodent
model of transcutaneous electrical nerve stimulation (TENS), the SQS model
presented with differential effects than the TENS model, suggesting the
involvement of different mechanism of action between these two neuromodulation
therapies [5]. Future studies will concentrate in investigating optimal parameters
of stimulation with the SQS model.

2 The Presentation
The talk will give a basic overview of the mechanisms behind SCS and PNS. The
overview includes a summary of the latest pre-clinical research that has been
performed in order to elucidate mechanisms and leverage such for better pain relief.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 135
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_26, © Springer International Publishing Switzerland 2014
136 L. Vera-Portocarrero

Fig. 1 Representation of the multiple sites of action of SCS. 1) Antidromic pulses of SCS
applied to the dorsal columns have effects at this nerve fibers going into the periphery. 2) A
the same time, electrical field could spread into the spinal cord dorsal horn and modulate
different neuronal populations. 3) Stimulation of the dorsal columns sends impulses
rostrally and produces effects in the dorsal column nuclei and higher brain areas. 4) In turn,
some of these brain areas modulate pain processing at the level of the spinal cord via
enhanced descending inhibition.

Acknowledgment. The author is an employee of Medtronic Inc.

References
1. Melzack, R., Wall, P.: Pain mechanisms: a new theory. Science 150, 971–979 (1965)
2. Song, Z., Ansah, O.B., Meyerson, B.A., Pertovaara, A., Linderoth, B.: Exploration of
supraspinal mechanisms in effects of spinal cord stimulation: role of the locus coeruleus.
Neuroscience 253, 426–434 (2013)
3. Wu, M., Komori, Q.C., Farber, J.P., Linderoth, B., Foreman, R.: sensory fibers
containing vanilloid receptor-1 (VR-1) mediate spinal cord stimulation-induced
vasodilation. Brain Res. 1107(1), 177–184 (2006)
4. Cui, J.-G., O’Connor, W.T., Ungerstedt, U., Linderoth, B., Meyerson, B.: Spinal cord
stimulation attenuates dorsal horn release of excitatory amino acids in mononeuropathy
via a GABAergic mechanism. Pain 73, 87–95 (1997)
5. Vera-Portocarrero, L.P., Cordero, T., Billstrom, T., Swearingen, K., Wacnik, P.W.,
Johanek, L.: Differential effects of subcutaneous electrical stimulation (SQS) and
transcutaneous electrical nerve stimulation (TENS) in a rodent model of chronic
neuropathic or inflammatory pain. Neuromodulation 16(4), 328–335 (2013)
Lokomat: Clinical Training and Experience in a
Neurorehabiltation Hospital

Christian Gunge Riberholt

Physical Therapist, Master in Rehabilitation


Department of Neurological Rehabilitation / Traumatic Brain Injury Unit,
Glostrup University Hospital, Denmark

1 Introduction

This presentation aims to give insight into the daily work of walking rehabilitation
of patients with severe acquired brain injury (ABI) using the Lokomat© system.
The lokomat system offers a high number of repetitions (steps) pr. training session
with less physical stress on therapists compared to conventional gait training. The
effect of a high number of repetitions for functional recovery after brain injury has
become evident in studies performed during the last decade within the field of
neurorehabilitation. Yet robotic treatment for rehabilitation of gait function is still
rather new and the current literature lack randomized controlled trials in ABI.
Furthermore few trials have specifically investigated the most optimal training
strategy for different groups of neurological patients
This presentation aims at highlighting some of the strategies and clinical
challenges using an evidence-based approach to rehabilitation of gait function in
severe ABI patients using the lokomat© system.

2 Method

A brief review of the literature on robot aided walking rehabilitation and some
thoughts on motor recovery of ABI patients is presented in this talk. Practical
experience of 20 patients with severe ABI is also presented and illustrated through
video, quantitative data obtained in the Lokomat© and through clinical
measurements.

3 Results

Patients were mobilized as early as possible in the Lokomat©. A stable orthostatic


blood pressure for a minimum of 10 minutes was the main inclusion criteria
besides the contraindications stated by the manufacturer. Data presented from
these patients will include number of sessions, walking time, distance, speed, body
weight, guidance force.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 137
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_27, © Springer International Publishing Switzerland 2014
138 C.G. Riberholt

4 Discussion

Rehabilitation of gait in our opinion requires early intensive rehabilitation with


focus on the number of repetitions. Furthermore, active participation of the patient
through interactions with the robotic system is of high importance for an effective
and successful rehabilitation of gait function. Our results suggest that severe ABI
patients get a high amount of repetitive training with the Lokomat system
compared to conventional gait training. We furthermore suggest that therapists
should pay close attention to facilitate active muscle contractions as early and
intensive as possible by adjusting various parameters of the robotic system.
It is still unknown how well the robot assisted gait training translates to over
ground walking and in the end ambulation. In addition, little is known about the
active ingredients or which parameters of robotic rehabilitation to adjust to get the
most out of a promising tool in neurorehabilitation, or the most relevant clinical
question: How do we get the patient with severe ABI more actively involved in
this kind of rehabilitation?
CORBYS Project Overview: Approach and
Achieved Results

Danijela Ristić-Durrant1, Siniša Slavnić1, and Cornelius Glackin2


1
Institute of Automation, University of Bremen, NW1, Otto-Hahn-Allee 1,
28359 Bremen, Germany
{ristic,sslavnic}@iat.uni-bremen.de
2
Adaptive Systems Research Group, University of Hertfordshire, United Kingdom
c.glackin2@herts.ac.uk

Abstract. The objective of the integrated EU FP7 project CORBYS is to design


and implement a generic robot control architecture that allows the integration of
high-level cognitive modules to support the functioning of the robot in dynamic
environments including interaction with humans. As a practical application of the
control architecture, a novel cognitive mobile gait rehabilitation system is being
developed during the project’s lifetime. The system consists of a mobile platform
and a powered orthosis attached to the platform. The mobile platform will provide
mobility for a patient, and the powered orthosis will assist the patient to complete
his/her leg movements. The cognitive modules are supported by an advanced
multi-sensor system consisting of various types of sensors integrated within the
system, such as position and force sensors, as well of physiological wearable
sensors and EEG sensors. Based on the sensor measurements the CORBYS
cognitive modules will interpret the intention of the patient, and his/her physical
and psychological state, and from these create appropriate commands for the low-
level robot control. Through the cognitive robot control, the CORBYS gait
rehabilitation system will be a situationally-aware system, capable of learning and
reasoning to optimally match the requirements of the patient at different stages of
rehabilitation, in a range of gait disorders.

1 Introduction
The CORBYS architecture was developed for the control of robots functioning in
dynamic environments alongside humans. It has been designed to support robot-
human co-working with high level cognitive capabilities such as situation-
awareness and goal-setting prioritization. Specifically, the CORBYS architecture
will support optimal time-critical control in take-over/hand-over of goal-setting
initiative between the robot and an external agent based on the anticipation of
purposeful behaviour of the agent. The CORBYS control architecture will be
validated within two challenging demonstrators: a novel mobile robot-assisted gait

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 139
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_28, © Springer International Publishing Switzerland 2014
140 D. Ristić-Durrant, S. Slavnić, and C. Glackin

rehabilitation system and an existing autonomous robotic system for investigation


of an environment.
In order to fully validate the CORBYS control architecture, the robotic mobile
gait rehabilitation system is equipped with a number of degrees-of-freedom
(DoFs), which enable range of physiological patient’s movements including
turning. On the other hand, the CORBYS control architecture supports the control
of such a complex robotic system that interacts physically with a human. In this
way, the CORBYS gait rehabilitation system will bring novelty to the field as
existing state-of-the-art rehabilitation robots have limited DoFs [1]. For example,
in the commercially available rehabilitation systems Lokomat [2] and
AutoAmbulator [3], the patient’s movement is limited to the sagittal plane.
The main mechanical components of the CORBYS gait rehabilitation system
and all enabled DOFs are briefly described in the following section. In addition, a
brief description of the control architecture and the various operating modes of the
CORBYS system are given together with the first results on gait learning as
needed for the cognitive adaptation of robot control.

2 Overview of the CORBYS Mobile Robotic Gait


Rehabilitation System
Fig. 1 shows the final CAD model image of the CORBYS robot-assisted mobile
gait rehabilitation system with an associated global coordinate system. It consists
of an omnidirectional mobile platform, a powered robotic orthosis attached to the
platform via a pelvis link, and a linear unit. The mobile platform provides mobility
for a patient and enables overground walking training, whilst the powered robotic
orthosis helps the patient to complete his/her leg movements.

Fig. 1 CAD model image of the CORBYS mobile gait rehabilitation system
CORBYS Project Overview: Approach and Achieved Results 141

2.1 The Main Components of the CORBYS System


The mobile platform constitutes the central housing structure of the CORBYS
mobile gait rehabilitation system. It serves as a component carrier for the linear
unit and motors for the orthosis, as well as the central power supply system. The
mobile platform also houses a network module, and other system modules such as
the safety module and the various computers upon which the modules of the
control architecture run.
Four wheel hub motors are connected to the platform for driving, which
provide movement of the system in x-direction. Each wheel is fitted with a
steering angle motor to change its direction (rotation about z-axis) so that the
platform can drive along curves.
The linear unit enables both lifting and lowering of the patient’s body (patient’s
pelvis movement in z - direction) and side to side movement of the patient’s body
(patient’s pelvis movement in y - direction). It is equipped with two servo-
positioning motors for the actuation of the z - axis which are chosen in order to
provide partial body weight support. One servo motor is used for the actuation of
the y - axis.
The pelvis link is the connection between the linear unit, attached to the
platform, and the powered orthosis. The pelvis link ensures that the patient’s
pelvis can rotate in the frontal and transverse planes.
The force/torque sensor for measurement of the interaction force between the
patient and the CORBYS system is placed within the pelvis link. This
measurement will be used for control of the mobile platform enabling it to follow
a walking patient’s while he/she is wearing the powered orthosis.
The powered orthosis assists the patient’s lower limb joint motions. The DoFs
configuration of the CORBYS orthosis prototype follows the natural human limb
kinematics. There are 6 DoFs at each leg: 3 DoFs in the hip, 1 DoF in the knee,
and 2 DoFs in the ankle joints. The hip, knee and ankle joint motions on
the sagittal plane (i.e. flexion and extension) are selected as active DoFs based on
the biomechanical properties of human walking [4], while the hip DoFs in the
transverse and frontal planes as well as ankle DoF in the transverse plane are
passive.
The orthosis has been designed in order to satisfy the requirement of
adaptability to a particular patient’s height and weight as well as the requirement
of the biomechanical joints’ ranges of motion.
The movements of the orthosis joints in the sagittal plane are controlled by a
push-pull control (PPC) cable-based actuation system. There are three actuators
per orthosis leg that actuate the hip, knee and ankle joints in the sagittal plane. The
actuators are placed on the mobile platform while the PPC cables are flexible links
to the joints used to transfer the rotational movement of the motors to specifically
designed orthotic joints. This has the advantage of keeping the powered orthosis
weight low, whilst the necessary torques are applied through the PPC cables to the
patient’s joints.
142 D. Ristić-Durrant, S. Slavnić, and C. Glackin

2.2 Control Architecture of the CORBYS Gait Rehabilitation


System
The control architecture of the gait rehabilitation system has been developed
within the CORBYS project [5]. The architecture was preliminary integrated to
support the robotic follower presented in [6]. Here, only a brief overview of the
architecture specifically regarding control of the gait rehabilitation system is
given. As illustrated in Fig. 2, the control architecture of the CORBYS robotic gait
rehabilitation system is divided into layers based on the functionality and logic of
the sub-systems that belong to each layer.

ROS
3. Cognitive layer

2. Executive layer

RT Framework
1. Control layer

0. Physical layer

Fig. 2 Layout of the CORBYS control architecture

Strictly speaking, the robotic system itself does not belong to the control
architecture as it is a control plant and can be considered as layer 0, the Physical
layer. The Physical layer contains actuators and sensors of the mobile platform,
the powered orthosis, and the pelvis link, such as position and force/torque
sensors. The 1st layer, the Control layer is in direct connection with the Physical
layer, where it reads sensor data and provides direct commands to the actuators. It
consists of the sub-modules that are responsible for controlling the robotic system
in “real-time (RT)” such as controllers of time critical processes such as
interaction control of the mobile platform, and control of the powered orthosis and
safety functionalities. The 2nd layer is the Executive layer which is responsible for
enabling the communication between the Control layer and the Cognitive layer, as
well as for coordinating and supervising the overall system functionality. The 3rd,
highest, layer is the Cognitive layer that contains the high-level cognitive modules
that enable the robot to understand the current state of the system and the patient,
so as to generate adequate high-level commands such as orthosis joint trajectory
adaptation, and determining the level of support that the system should provide to
the patient, which it then communicates to the Control layer. These modules are
the Situation Awareness Blackboard (SAWBB) and the Self Organising
Information Anticipatory Architecture (SOIAA) and they are supported with a
multi-sensor system to facilitate dynamic environment perception.
CORBYS Project Overview: Approach and Achieved Results 143

Modules on the Control layer communicate with the Physical layer over the
real-time network (RTN), while all other modules of the control architecture
communicate over the general purpose network (GPN). The ROS (Robot
Operating System) [7] has been chosen as the communication framework for
communication over the GPN. Ethernet is used as the communication protocol of
the GPN while the EtherCAT protocol [www.ethercat.org] is used on the RTN for
real-time control. EtherCAT was chosen as a suitable communication protocol to
cope with hard real-time control loops (f ≥ 1 kHz for the powered orthosis and the
mobile platform), especially given the large numbers of sensors and actuators and
the amount of information that is to be exchanged over the RTN.

2.3 Operating Modes


The CORBYS gait rehabilitation system will be evaluated through four operating
modes which will now be briefly described.
Learning Mode. The learning operating mode will have two phases, namely the
“native gait learning phase” and the “therapist assisted gait learning phase”. In both
phases the patient walks on a treadmill while wearing the orthosis. The powered
orthosis is attached to the mobile platform which is stationary, and the treadmill is
setup between the platform’s wings. The patient walks freely, unconstrained from
the system, as the orthosis controller is implemented so that the powered orthosis
follows the patient’s movement without imposing any restrictions to the movement.
Encoder sensors placed on the orthosis measure the joint angle gait parameters.
Based on the gathered information, the cognitive modules will learn the patient’s
native gait pattern. In the second phase of the learning mode, called the “therapist
assisted gait learning phase”, the therapist provides manual corrective actions that
will change the gait pattern of a patient as they walk in cooperation with CORBYS
system. In this way the CORBYS system conforms to the general goal of the gait
rehabilitation program, but within the patient’s limitations and capabilities. The
therapist will manipulate the patient’s lower extremities while the patient is
equipped with the powered orthosis and is walking on the treadmill and the mobile
platform is stationary. Using the gathered sensor data the CORBYS cognitive
modules will learn the “corrective gait pattern” as identified in the therapist assisted
gait learning phase. This learned corrective gait pattern will be used for providing
corrective inputs to the orthosis joint controllers in different operating modes or for
generating target joint trajectories as resulting from the correction of the learned
native gait pattern according to therapist assistance.
The Corrective or straight walk mode is characterised by the patient’s over
ground walking with the CORBYS system under therapist supervision. In this
mode, the patient will be enabled to practice straight walking in a highly repetitive
way, while permanently receiving the CORBYS system’s corrective actuation. The
CORBYS system optimizes gait continually, while comparing learned gait with the
continuously measured data, by applying some corrective inputs towards the target
gait pattern.
144 D. Ristić-Durrant, S. Slavnić, and C. Glackin

The Parameter based adaptation mode is the first extension of the straight walk
mode, which is based on detection of the patient’s intentions to start, to speed up
or to turn. In this mode the cognitive system provides inputs for corrective pattern
based on intention detection.
The Adaptive walking mode is the second extension of the straight walk mode.
In this mode, the patient will be allowed to freely walk around in the rehabilitation
area, starting, stopping, and changing speed at will, whilst the corrective forces are
applied as appropriate, whenever the patient’s walking pattern deviates from the
target pattern. The CORBYS system will react like the therapist, being tolerant and
reactive to small changes in the trajectory, whilst also correcting the major changes.

3 Test Stand Set-Up for CORBYS Control


Architecture-Learning Mode

As described above, the first step in the realization of a gait rehabilitation system
which is able to reason how to optimally match the requirements and abilities of
the patient, is to first establish how the system will learn the gait of each
individual patient as well as learn the mapping between the actuators and the gait
parameters. In this contribution, the first achieved learning results are presented.
The CORBYS gait rehabilitation system is in the integration phase. Therefore,
this contribution focuses on the results of the gait learning achieved using the
CORBYS orthosis test stand. The test stand was developed to support the
development of the cognitive modules of the CORBYS architecture even in
the early integration phase. The test stand consists of one orthotic leg and three
push-pull control (PPC) cable-based actuation systems for actuation of the hip,
knee and ankle joints in the sagittal plane. The two passive joints of the hip and
adduction/abduction joint of the ankle are mechanically blocked and are not
considered in the study considered here. The test stand is shown in Fig. 3.
Beside the test stand, in order to support development of the cognitive modules
in the early integration phase a MATLAB simulation environment, and a gateway
between the simulation environment and higher layers of the CORBYS
architecture were developed. One incremental and absolute encoder is mounted on
every joint of the test stand orthosis leg. Two force cells are placed respectively on
the motor and joint sides of the PPC cable so that it is possible to measure forces
on both ends of the cable. Encoders, force cells and actuators are all interfaced
using Beckhoff EtherCAT modules. MATLAB’s xPC target software is used for
real-time acquisition of the sensor signals and control of the orthosis leg joints.
The motion data of a patient that was recorded using the VICON marker-based
motion-capture system has been used as the reference signal to the controllers of
the joints. The recorded angles in all three joints in the sagittal plane were used to
control the joints of the orthosis. In turn, the encoders’ measurements are sent via
a MATLAB/ROS gateway and further via a Real-time data server (RTDS) to a
CORBYS Project Overview: Approach and Achieved Results 145

Fig. 3 Test stand set-up for the CORBYS control architecture – Learning mode. Test stand
components: 2, 4 and 6 - actuators of the ankle, hip and knee joint; 1, 3 and 5- the
corresponding PPC cables; 7 - the xPC target computer; 8 - the EtherCAT terminal; a, b and
c - the hip, knee and ankle joint respectively.

model learner (ML). The latter is an essential part of the SOIAA cognitive
module, which is specifically responsible for learning the gait and the mapping
between the actuators and the sensors.
SOIAA uses a Gaussian Process-based model learner to learn the gait dynamics
of a patient. Once the ML is trained in the learning mode, SOIAA uses this as a
cognitive ‘internal representation’ of the patient and the orthosis in order to adapt
therapist assisted learned gait to more complicated starting, speeding up, slowing
down, and turning gait patterns. In the final operating mode, SOIAA will also
generate gait pattern in real-time based on the patients movement intentions.
The capability of the ML is illustrated here by two examples, namely the
prediction of learned gait dynamics, and the learning of the relationship between
actuation and sensors.
Fig. 4 illustrates that when the ML is presented with three consecutive time
steps of a particular gait variable, knee joint angle on the sagittal plane, it can
learn to predict the trajectory at the next time step. The first sub-figure shows the
training and testing data taken from the same patient. The data illustrates the large
variability of gait data in terms of phase and amplitude, typically resulting from
changes in walking speed. The ML uses the training data to learn the gait pattern
of the patient. The second sub-figure compares the output of the ML with unseen
testing data, shown by the green and red traces respectively. The plot demonstrates
the ability of the ML to generalise the prediction of gait for unseen testing data,
146 D. Ristić-Durrant, S. Slavnić, and C. Glackin

even when gait which deviates from the learned pattern as it does in this example
in terms of walking speed.

Fig. 4 ML prediction result for knee joint angle on sagittal plane

The initial test stand experiments were used to assess the feasibility of the ML
to learn the relationship between the actuation and the effect it has on the knee
joint angle gait variable. There were two inputs to the ML which represent the
actuator control reference and the measured actuator control. The single output of
the ML is the joint angle measurement from the test stand orthotic leg. The first
sub-figure in Fig. 5 shows the ML accuracy (the ML output compared against the
unseen testing orthosis angle), and a measure of confidence in the ML output is
shown in the second sub-figure. The measure of confidence is a feature of the
Gaussian Process Bayesian formalism [8]. The ML accuracy is good, although
some uncertainty around the peaks can be seen due to the characteristics of the
orthosis actuation system. In particular some non-linearities result from the minor
degree of ‘play’ in the orthosis joints which manifests as some minor differences
in amplitude, as can be seen at the peaks and troughs of the two traces. This
difference is then reflected by minor increases in variance (confidence) in the
second sub-figure.

Fig. 5 ML prediction result for knee joint angle on sagittal plane based on learned internal
representation of the relationship between orthjosis actuation and sensor output
CORBYS Project Overview: Approach and Achieved Results 147

Presented learning results which were achieved with the CORBYS test stand
build a basis for further development of system learning capabilities. In fully
integrated system a range of additional sensor measurements will be available to
cognitive modules to understand the current state of the system and the patient, so
as to generate adequate high-level commands for cognitive adaptation of robot
control to mach the abilities of the patient.

Acknowledgment. This research was supported by the European Commission as part of the
CORBYS (Cognitive Control Framework for Robotic Systems) project under contract FP7
ICT-270219.

References
[1] Viteckova, S., Kutilek, P., Jirina, M.: Wearable lower limb robotics: A review.
Biocybernetics and Biomedical Engineering 33, 96–105 (2013)
[2] Colombo, G., Joerg, M., Schreier, R., Dietz, V.: Treadmill training of paraplegic
patients using a robotic orthosis. Journal of Rehabilitation Research &
Development 37(6), 693–700 (2000)
[3] HealthSouth’s AutoAmbulator (February 2014),
http://www.healthsouth.com
[4] Winter, D.: Biomechanics and Motor Control of Human Movement, 4th edn. Wiley
(2009)
[5] CORBYS Project, http://www.corbys.eu
[6] Leu, A., Ristić-Durrant, D., Slavnic, S., Glackin, C., Salge, C., Polani, D., Badii, A.,
Khan, A., Raval, R.: CORBYS Cognitive Control Architecture for Robotic Follower.
In: 2013 IEEE/SICE International Symposium on System Integration (SII 2013),
Kobe, Japan (2013)
[7] Cousins, S.: Welcome to ROS Topics. IEEE Robotics & Automation Magazine 17(1),
13–14 (2010)
[8] Rasmussen, C., Williams, C.: Gaussian processes for machine learning. MIT Press,
Cambridge (2006)
Rehabilitation Robot in Primary Walking
Pattern Training for SCI Patient*

Taisuke Sakaki1, Nobuhiro Ushimi1, Koji Murakami1, Yong-Kwun Lee1,


Kazuhiro Tsuruta1, Kanta Aoki1, Kaoru Fujiie2, Ryuji Katamoto2, Atsushi Sugyo2,
Yoshimitsu Kihara3, and Kenji Tateishi4
1
Kyushu Sangyo University, Fukuoka, 813-8503 Japan
sakaki@ip.kyusan-u.ac.jp
2
Spinal Injuries Center, Iizuka, 820-8508 Japan
fujiie@sekisonh.rofuku.go.jp
3
Kihara Iron Works Co., Iizuka, 820-1111 Japan
kihara-t.k05@luck.ocn.ne.jp
4
I-Quark Corporartion, Fukuoka, 811-2207, Japan
tateishi@iquark.co.jp

Abstract. Recently, attention has been focused on incomplete-type spinal cord


injury to the central spine caused by pressure on parts of the white matter
conducting pathway such as the pyramidal tract. In this paper, we focus on a
training robot designed to assist with primary walking pattern training. The target
patient of this training robot is one who is relearning the basic functions of the usual
walking pattern, especially for patients with the incomplete type SCI to the central
spine, who are capable of standing by themselves but are not capable of performing
walking motions. From the perspective of human engineering, we monitored the
operator’s actions to the robot and investigated the movement of joints of the lower
extremities, the circumference of the lower extremities and the exercise intensity
with the machine. The concept of the device is to provide mild training without any
sudden changes in heart rate or blood pressure, which will be particularly useful for
the elderly and disabled.

1 Introduction

According to a fact-finding survey of disabled people conducted by the Ministry


of Health, Labor and Welfare, there are 1.76 million physically disabled persons,
including 54 thousand with spinal cord injuries (SCI) in Japan. Slightly more than
5 thousand peoples suffer the disease every year as a result of traffic accidents,
falling, and sports accidents. Physical therapy is designed to prevent orthostatic
hypotension, disuse born atrophy, contracture, and mental disorders.

*
A part of this research supported by The Robotics Industry Development Council,
Fukuoka, Japan.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 149
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_29, © Springer International Publishing Switzerland 2014
150 T. Sakaki et al.

Recently, attention has been focused on incomplete-type SCI to the central spine
caused by pressure on parts of the white matter conducting pathway such as the
pyramidal tract. The middle-aged and elderly patients may endure quadriplegia as a
result of injury to this area from overextension of the spinal cord, which is caused
by falling in most cases. According to epidemiological data from new patients in
2005 and 2006 in Fukuoka Prefecture in Japan collected by the Spinal Injuries
Center, the incidence rate of it has shown a decreasing trend, 33.7 and 27.6 among
million people on average, in 2005 and 2006 respectively. However, the age of
onset of it shows an increasing trend. Forty-five percent of these patients are
incomplete-type to the central spine cases. Most of them have a defective one, in
which the spinal cord is not completely severed, and the muscle power and
sensation in the extremities are poor. In this type, the paralysis may be present in the
upper extremities more strongly than in the lower ones. The muscle power of the
lower extremities will build gradually to a level sufficient for standing up and
walking. The muscle power of the hands and fingers, however, may not recover to a
level where the patient can grasp or pinch sufficiently in typical activities of daily
living.
The rehabilitation process for SCI comprises several steps, including 1) basic
training for extending the range of motion of joints and muscle strengthening, 2)
training to maintain a seating posture, 3) training in standing up and sitting down,
4) training for re-learning the primary walking pattern, and 5) training in practical
walking.

Fig. 1 The training robot for the basic walking pattern (apparatus, upper figure and
structure of sliding mechanism, lower figure)
Rehabilitation Robot in Primary Walking Pattern Training for SCI Patient 151

Over the last decade, a variety of rehabilitation robots and physically assisting
robots have been developed [1]-[4]. In particular, applying the BCI (brain
computer interface technology), neuro-rehabilitation techniques and wearable
robot technologies, and neuro-rehabilitation robotics have recently been actively
studied [5]. Recent gait rehabilitation robots, such as the Lokomat , the Lopes, the
PamPogo, the ALEX, and the GaitTrainer have been studied and used in
locomotion training for SCI or CNS (central nervous system) patients
[6][7][13]-[15]. These therapies are based on the neuroplasticity on a spinal and
supraspinal level, and achieved by physiological multisensory input to reshape the
locomotor pattern of the spinal circuitry. The physical constraints of the
conventional manual assisting training can be overcome by using robotic training
to activate the CPG (central pattern generator) [17] with the BWSTT (body weight
supported treadmill training) mechanism of the robot [8].
We have been developing a series of robots to apply to every step of training
for patients with incomplete SCI to the central spine. In this paper, we focus on
the training robot assisting the primary walking pattern training.

1.1 Conventional Methods for Walking Pattern Training


Circular walkers, canes, and parallel bars are the most popular tools used in
rehabilitation. The problems with these tools are the high risk of falling and the
difficulty in maintaining a normal body trunk posture, leading to a need for
extensive monitoring, care, and advice by a therapist. Also, the patient usually
cannot exercise for a long period of time with these rehabilitation aids, as it is very
tiring.
Several training machines for lifting the body trunk have been developed for
SCI and other types of patients. The Lokomat and the KineAssist provide partial
body weight support and postural torque on the torso [7, 10]. Its features are a
lifting mechanism for the body trunk to decrease the weight a patient must lift, a
mechanism that drives the lower extremities, and a treadmill. However, these
machines cannot train for practical walking in a real environment achieved by
voluntary motions such as body weight transfer and swing phase motion. There is
also a wearable training machine mounted on the lower extremities developed at
Tsukuba University [5]. The features of this device include a driving mechanism
to actuate the hip, knee, and ankle joints with motors, the commands for which are
calculated with sensors responding to inputs such as EMG or leg motions. The
machine, however, is not able to support a patient’s weight. The risk of falling
with this machine is greater than with other types of training machines, since a
mechanism for supporting the trunk posture is not provided.
Circular wheel type training machines with electric motor wheels have been
developed by Hitachi Co. The features of this type of machine are a maneuvering
mechanism mounted to a circular wheel, automatic control of a maneuvering
system that leads the patient to walk, and a supporting mechanism for the waist,
trunk, and upper extremities. Most of these machines do not provide a mechanism
152 T. Sakaki et al.

to directly drive the legs. The problem with the machines is that there is a risk of
falling. It is difficult to learn the right posture and walking pattern again, and there
is no mechanism for taking advantage of voluntary movements of the patient.
In summary, the conventional machines and tools have the following problems:
1) risk of falling, 2) difficulty in achieving the right posture of the body trunk and
practical walking in real environment, 3) lack of a mechanism for taking
advantage of voluntary movement of the patient, 4) fewer degrees of freedom
(d.o.f.) of movement because the patient’s body is fastened to the machine, and 5)
very large size and heavy weight.

2 Training Robot for Primary Walking Pattern

The target patient for this training robot is one who is relearning the basic
functions of the usual walking pattern, especially for patients with the
incomplete-type to the central spine who are capable of standing by him/herself
but not capable of performing walking motions. The primary walking pattern with
voluntary motion for body weight transfer and swing phase leg motion will be a
preparation to the recovery of practical walking in the real environment.
We propose a new type of training machine that assists patients in learning the
walking pattern and executing preliminary dynamic walking, as shown in Figure 1
[11, 18]. Specifically, the robot provides three kinds of assistive motions with a
sliding mechanism according to the recovery level of the patient's lower
extremities. The passive reciprocal motions of the feet are provided in the case of
poor muscle power of the lower extremities. In addition, other assistive motions
are provided while sensing the reciprocal movement of foot pressure or when
sensing the foot pressure movement and lifting motions of the foot during the
swing phase, which are slightly allowed in the foot plate. The whole mechanism
of the robot can travel forward coincident with the sliding mechanism motion,
which provides quasi-walking actions. The sliding motion does not simulate a
complete natural gait in the swing phase. The patient, however, can be trained by
the quasi-walking motions with voluntary body weight transfer and lifting of the
leg in the swing phase monitored by the machine.
This robot has both a slide mechanism and a maneuver mechanism, as shown in
Figure 2. The sliding mechanism provides the reciprocal sliding motions forward
and backward of the patient’s feet to achieve a quasi-walking pattern. Each foot is
fixed on the foot plate mounted on the belt actuated by the servo motion of the
stepping motor servo system (Cool Muscle CM1-C-23L20A, 30W, 2000rpm,
Muscle Corporation), which includes a stepping motor, an angular sensor, a servo
amplifier, and a CPU for network use. The maneuver mechanism drives the
robot’s whole body forward and/or in turn coincident with the motion of the
sliding mechanism. Due to the action of these mechanisms, the patient who is
riding on the robot can feel as if he/she is able to walk by him/herself.
Rehabilitation Robot in Primary Walking Pattern Training for SCI Patient 153

Fig. 2 The mechanical structure of the training robot for the basic walking pattern (upper
figure). The foot plate and foot cover contain a switch on the instep cover to detect the leg
lift motion and the pressure sensor the load of the foot (lower figure).

The pressure sensor mounted on the foot plate measures the pressure by the
foot. The micro switch on the top cover of the foot plate detects the swing phase
motion of the foot. According to the sensor information, the microcomputer,
Arduino, delivers the motion command to the motor. Four actuator systems of
Cool Muscle, which are connected to each other and controlled by the Arduino,
are used in the two sliding mechanisms and the two drive mechanisms for
maneuvering.
The waist pad and the belt support the patient’s body to prevent falling. The
body supporter, the waist supporter and the supporting belt allow the patient to
154 T. Sakaki et al.

move freely and safely in the small space surrounded by those supporters, and side
bars prevent falling without harnesses. To compensate for the poor muscle power
of the upper extremities, the hands can be fixed with a belt to the hand sticks if
necessary.
The robot can provide three-step training functions according to patient’s
walking ability, as follows:

• ‘Passive walking pattern training’ is the primary level. The robot will allow
for complete passive motion for the patient with severely reduced ability,
who can stand by him/herself but cannot perform any body weight transfer
motions. The foot plates move reciprocally as automatic motions.
• ‘Static walking pattern training’ is the middle level. It will be utilized for
patients who still have a poor ability to transfer their body weight. Sensing
the transfer of the load by the pressure sensor on the foot plate, the foot plate
moves reciprocally according to the load amount. The sliding motion will
stop when there is no change of the foot pressure by transferring body
weight. This function will provide feedback to the patient, thus facilitating
the voluntary body weight transfer.
• ‘Semi-dynamic walking pattern training’ is the highest level. It will be
utilized for patients with poor swing phase motion but with sufficient ability
to transfer body weight. Sensing the foot pressure and the motion of the leg
lifting in the swing phase detected by the micro switch on the top of the foot
plate, the foot plate moves reciprocally. The sliding motion will stop when
there is no change of these two motions. This function will provide feedback
to the patient, facilitating voluntary body weight transfer and swing phase
motion.

3 Preliminary Experiments

From the perspective of human engineering, we monitored the operator’s actions to


the robot and investigated the movement of joints of the lower extremities, the
circumference of the lower extremities and the exercise intensity with the machine.
The time history of the process of the operation of the machine and assistance to
patients was observed by recording the picture on a video. Figure 3 shows the
operation and assistance process. Five normal subjects joined as care-givers (3 20
yrs of age, on 40 yrs of age, and one 50) joined the experiment. They were
instructed before the experiment to operate and assist according to the procedure.
One normal subject (22 yr., 168 cm, 60 kg) participated as a patient. Wearing a
T-shirt, short pants for measurements, a cap to make clear the shape of head, and
optical markers on the acromial part and parietal area, the subject was instructed to
maintain a seating position on the wheelchair and to entrust his body movements to
the care-giver by relaxing his extremities.
By monitoring the assistance process, the patient subject took his posture,
inclining forward as his waist was pushed by the back-supporting pad. This position
Rehabilitation Robot in Primary Walking Pattern Training for SCI Patient 155

may involve some risk of the knee bending and the patient falling. The position of
the pad should be modified to the backward position. At the time of operating the
supporting pad, the user is not supported for knee bending or falling (shown as
process with a box in Fig.3). Operating the pad should occur just after standing up
or before sheeting to the wheelchair.

Fig. 3 The operation and assistance process with the training robot. At the time of operating
the supporting pad, the user is not supported for knee bending or falling (shown as process
with a box ).

The motion, the activity of muscles and the exercise intensity of the lower
extremities were measured. Using Multichannel Telemeter System WEB1000
(Nihonkoden Inc.), the joint angles of the lower extremities were observed. In order
to measure the range of motion of the femur, the Joint Angle Telemeter Picker
ZB-154H (Nihonkoden Inc.) as a sensor probe was mounted on the trochanter
major. The angles of plantar flexion and dorsiflexion of ankle joint were monitored
with the probe on the ankle point. The knee joint, which may be kept straight, was
not observed. The calf circumference was measured with the Plethysmograph EC6
(D.E.Hokanson,Inc.) as the Plethysmography device. Using that index of the
muscle spindle and tendon spindle, the activity of muscles of the calf was evaluated.
The exercise intensity was observed by measuring blood pressure and heart rate
with the Bedside Monitor BSM2353 (Nihonkoden Inc.). Figure 4 shows the three
kinds of data for five minutes of exercise. The hip joint angle vibrates at 17 degrees
as a center point. The angle extended by approximately 5 degrees and flexed by
approximately 8 degrees, which constitutes 1/3 of the walk pattern of a healthy
person. The ankle joint changes repeatedly with approximately 15 degrees of planar
flexion and approximately 8 degrees of dorsiflexion, which is almost the same
pattern as that of a healthy person. In addition, the calf circumference changes
repeatedly during the same period as the joint angle motions. The changes in blood
pressure and heart rate during exercise are small.
156 T. Sakaki et al.

Fig. 4 The three kinds of data for five minutes of exercise with the robot as the time history
of hip angle, ankle angle and calf circumference

4 Conclusions

The concept of the device is to provide mild training without any sudden changes
in heart rate or blood pressure, which will be particularly useful for the elderly and
disabled. The characteristics of this device are 1) the load by the standing position
depends on the foot bottom without supporting the load, 2) the reciprocal stepping
motion of both legs is available, 3) assistance is provided when detecting the center
of gravity movement to the right and left, 4) the swing phase motion of the leg is
partially realized, 5) the range of motion of the hip is 1/3 that of a healthy person
and that of the ankle is the same as that of a healthy person, 6) the flexion and
extension of the muscle spindle and tendon spindle of the calf is expected to affect
the afferent deep reflex.
The development target is a device with simple functions and low cost that is
small and light weight for home-use exercise to make possible the recovery of
walking functions. Considering these experimental results, the comments of staff
such as physical therapists, and medical science papers, some of the current
technical problems are being addressed as follows: 1) a swing phase leg motion
that is closer to the movement of a healthy person should be implemented, in
particular the pulling-up motion of the toes, as emphasized by the therapists, 2) the
transfer process should be modified to make it easier and more certain, 3) the
feedback system to provide information regarding the results of training to
the user should be improved, 4) The operation panel should be easy for the elderly
to utilize.
Rehabilitation Robot in Primary Walking Pattern Training for SCI Patient 157

References
[1] Hanafusa, A., Sasaki, J., Fuwa, T., Ikeda, T.: Self-Aided Manipulator System for
Bed-Ridden Patients -Evaluation of Psychological Influence for the Generated
Approach Motion-. In: Proc. of 2009 IEEE 11th Int. Conf. on Rehabilitation Robotics,
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[2] Peng, S., Lian, F., Fu, L.: Development of Multi-Functional Robotic Test-Bed for
Post-Surgical Healthcare Room. In: Proc. of 2009 IEEE 11th Int. Conf. on
Rehabilitation Robotics, USB memory (2009)
[3] Rofer, T., Mandel, C., Laue, T.: Controlling an Automated Wheelchair via
Joystick/Head-Joystick supported by Smart Driving Assistance. In: Proc. of 2009 IEEE
11th Int. Conf. on Rehabilitation Robotics, USB memory (2009)
[4] Sakaki, T., Iribe, T., Kurogi, T., Koga, T., Ushijima, K., Sakuragi, M., Miyanaga, K.:
Robotic Stretcher for SMA Patient: Preliminary Tests on Controllability and Safety. In:
Proc. of IFAC World Congress, CD-ROM (2011)
[5] Sankai, Y., et al.: Study on Hybrid Power Assist HAL-1 for Walking Aid using EMG.
In: Proc. of the JME on Ibaraki Symp., pp. 269–272 (2000)
[6] Stauffler, Y., Allemand, Y., Bouri, M., Fournier, J., Clavel, R.: Pelvic Motion
Measurement During Over Ground Walking, Analysis and Implementation on the
WalkTrainer Reeducation Device. In: Proc. IEEE Int. Conf. Intel. Rob. Syst. (IROS),
pp. 2362–2367 (2008)
[7] Konig, A.: Design principles to transfer basic neuroscience into gait rehabililation
rehabilitation robots. In: Proc. 2011 IEEE 11th Int. Conf. on Rehabilitation Robotics,
CD-ROM (2011)
[8] Rupp, R.: Engineering robots for an effective locomotion therapy – There’s more than
joint angles! In: Proc. 2011 IEEE 11th Int. Conf. on Rehabilitation Robotics, CD-ROM
(2011)
[9] Hesse, S., Uhlenbrock, D., Sarkodie-Gyan: Gait pattern of severely disabled
hemiparetic subjects on a new controlled gait trainer as compared to assisted treadmill
walking with partial body weight support. Clin. Rehabil. 13(5), 401–410 (1999)
[10] Peshkin, M., et al.: KineAssist: A robotic overground gait and balance training device.
In: Proc. 2005 IEEE 11th Int. Conf. on Rehabilitation Robotics, CD-ROM (2005)
[11] Sakaki, T., Ushimi, N., Aoki, K., Fujiie, K., Katamoto, R., Sugyo, A., Kihara, Y.:
Rehabilitation robots assisting in walking training for SCI patient. In: IFAC BMS 2012,
CD-ROM (2012)
[12] Hachisuka, K., et al.: A prototype walking assist robot and its clinical application for
stroke patients with severe gait disturbance. In: Advances in Physical and
Rehabilitation Medicine, pp. 23–26 (2003)
[13] Dobkin, B.H.: Strategies for stroke rehabilitation. Lancet Neul. 3, 528–536 (2004)
[14] Langhone, P., et al.: Motor recovery after stroke: a systematic review. Lancet Neurol. 8,
741–754 (2009)
[15] Hidler, J., et al.: Multicenter randomized clinical trial evaluating the effectiveness of
the Lokomat in subacute stroke. Neurorehabil. Neural Repair 23, 5–13 (2009)
[16] Colombo, G., Matthias, J., Reinhard, S., Volker, D.: Treadmill training of paraplegic
patients using a robotic orthosis. J. Rehabil. Res. Dev. 37(6), 693–700 (2000)
[17] Dimitrijevic, M.R., Gerasimenko, Y., Pinter, M.M.: Evidence for a spinal central
pattern generator in humans. Ann. NY Acad. Sci. 860, 360–376 (1998)
[18] Sakaki, T., Ushimi, N., Aoki, K., Fujiie, K., Katamoto, R., Sugyo, A., Kihara, Y.:
Rehabilitation robots assisting in walking training for SCI patient. In: Proc. of Ro-Man
2013, USB memory (2013)
Effect of Transcranial and Spinal Direct
Current Stimulation on Gait

Giorgio Sandrini and C. Mondino

National Neurological Institute and Department of Brain and Behaviour Sciences,


University of Pavia, Pavia, Italy

Neuromodulation field, induced by Direct Current Stimulation, has been largely


investigated in the last years in relation to promising results in neurological
diseases.
Direct Current Stimulation is a non-invasive technique based on the
application, by means of surface electrodes, of an electrical current flow (Direct
Current Stimulation - DCS) at the level of the scalp or the rachis (respectively
Transcranical or Spinal Direct Current Stimulation – t-DCS and s-DCS) or the
peripheral level (neurostimulation of nerves plexus). In relation to the stimulation
parameters applied (intensity and orientation of the current field), DCS can
influence, even with prolonged effect, the excitability of the Central Nervous
System, including areas not directly affected by the stimulation. This effect is
mediated initially by a polarization of the neuronal membrane (short-term effect)
and then by the modulation of neurotransmitter –related processes of synaptic
plasticity, such as glutamate and GABA (long term effect). These long term effect
suggested the application of DCS treatment in neuro-rehabilitation; particularly,
it’s reported, after DCS treatment, an improvement of gait disorder in many
neurological diseases.
T-DCS, applied on the motor and premotor area, has shown effective, for a
period of more than three months, in changing freezing and bradykinesia in
patients suffering from Parkinson's disease, an effect also confirmed by studies in
animal models. T-DCS, applied on the motor and premotor area in post-stroke
patients, have been shown an improvement on paretic lower limb, with consequent
gait improvement.
Several evidences suggest that cerebellum plays a critical roles in motor
adaptation; so, it’s reported that anodal t-DCS applied on cerebellum during
walking improve locomotor adaptation. Investigators supposed that t-DCS acts on
cerebellum in different ways: it could broaden the Purkinje cell populations that
are available for learning or increase their dynamic range.
Spinal Direct Current Stimulation has interesting effects on gait improvement
in patients with Parkinson disease. In fact, electrical stimulation of the posterior
column of spinal cords was able to restore a locomotor pattern similar to the

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 159
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_30, © Springer International Publishing Switzerland 2014
160 G. Sandrini and C. Mondino

physiological gait in animal models of Parkinson's disease, with acute and chronic
depletion of dopamine. It’s possible that s-DCS, applied at the spinal level, has an
impact also on higher neuronal areas, modulating SNC activity. In particular,
some evidences suggest that s-DCS modulates the Central Pattern Generator
(CPG), a complex network of interneuron spread over several vertebrae, involved
in the generation of gait control. Among the regions involved in descending
inhibition of the CPG, may have a prominent role the mesencephalic locomotor
region (MLR) placed at the level of the brainstem. Inside it is also located the
pontine nucleus peduncle (PPN), a region that has close connections with the basal
ganglia (GB), with the Pars reticulate the substantia nigra (SNpr), with the
cerebellum and the ventral medial column of the gray matter of the spinal cord,
and that seems to be involved in the genesis of disorders of gait and freezing in
patients with Parkinson's disease, as well as from postural disorders.
Adaptive Behavior of the Spinal Cord in the
Transition from Quiet Stance to Walking:
The Use of Widthrawal Reflexes to Support
Gait Initiation

Mariano Serrao

Department of Medical and Surgical Neurosciences and Biotechnologies,


Neurorehabilitation Unit, University of Rome, Latina, Italy
mariano.serrao@uniromal.it

1 Introduction

Investigation of spinal reflexes is an approach commonly used, in both animals


and humans, to explore spinal behaviour during walking. The modulation and
integration of spinal reflexes during walking are crucial to the production of
movement and also part of CPG organization. Among the spinal reflexes, the
nociceptive withdrawal reflex (NWR) is easily evoked in many muscles of the
arms and legs and it is a useful tool for studying spinal cord function during limb
movements in humans (Sandrini et al., 2005, Andersen et al., 2007). Although the
NWR is not involved in voluntary movements, afferents belonging to this reflex
do participate in movement through alternative excitatory and inhibitory spinal
neural pathways.
In this presentation it will be addressed the problem on how to use the electrical
stimulation evoking the NWR in patients with gait initiation disturbances in the
light of what is known about the physiology of the gait initiation. The method of
evoking the NWR may give advantages, compared to direct stimulation of
muscles, to obtain desired biomechanical responses by synchronizing the
activation of many muscles in a “physiological way”.

2 Nociceptive Reflex Modulation during Gait Iniitation

Some evidences on the transition from quit stance to walking have revealed that
NWR is modulated according to the gait initiation phases (Crenna and Frigo,
1991; McIlroy et al., 199; Bent et al., 2001; Serrao et al., 2012). Particularly, the
NWR is enhanced in the hip and knee flexor muscles of the starting leg just before
any movement is initiated. These results suggest that the descending pathways
conveying the commands for the motor programming of gait initiation activate the
spinal circuitries mediating the NWR of the starting leg. This activation, which
may serve to prepare and assist the leg in the first step, takes place just before any

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 161
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_31, © Springer International Publishing Switzerland 2014
162 M. Serrao

movement actually occurs suggesting that the intentional descending commands


interact with the spinal circuitry in accordance with the role that the CNS assigns
to each leg (starting or standing) at the very beginning of gait. From this
perspective, it can be suggested that one role of the descending commands is to
initiate an asymmetrical (left-right) and unbalanced (flexor-extensor) activation of
the spinal cord system.
It has also been observed that the NWR is increased in the knee flexor muscles
soon after the leg is unloaded (Serrao et al., 2012a,b).
Furthermore, irrespective of phase-related modulation, the NWR is modulated
by hip joint motion Thus, after selective and asymmetrical excitation of the spinal
substrate mediating the NWR leg unloading and hip joint motion work in concert
to produce an alternating (right and left) and crossed (flexors and extensors)
activation mainly of the hip and knee joint muscles, predisposing the legs to the
cyclical pattern of steady-state walking.

3 Using Electrical Stimulation to Support Gait Initiation

The knowledge on how the NWR is modulated during gait initiation in humans
may be exploited to plan new rehabilitative strategies and to develop electrical
devices to sustain and facilitate gait initiation in several neurological diseases with
gait initiation disorders (e.g. gait freezing in Parkinson disease, stroke patients,
etc.). Particularly, the electrical stimulation evoking NWR should be released at
different time intervals across gait initiation phases and triggered with specific and
meaningful gait events. The initial stimulation should be delivered during the
symmetrical stance. This may induce an asymmetrical activation of spinal circuitry
mediating NWR, shifts the center of mass toward the unstimulated limb and
facilitate the CNS to attribute, to each limb, a specific role in gait initiation
(swinging vs standing). Electrical stimulation in this phase could be particularly
useful in those patients (e.g. Parkinson with freezing, idiopathic freezing, stroke,
etc.) who have lost the ability of intentionally shifting the center of mass from one
leg to another and thereby preventing the loading-unloading sequence of gait
initiation. A second stimulation should be released when the limb is quickly
unloaded and the hip is flexed. The evocation of the NWR in hip and knee flexors
in this phase is important to promote the initial step. The electrical stimulation in
this phase may be used in those patients who need to be supported in their hip and
knee joints flexion (muscles strength deficit, joint constraint, etc).
An important issue on how to plan and develop a device to rehabilitate an
support gait initiation is how electrical stimulation should be triggered during gait
initiation. One possible solution is to trigger the electrical stimulation with the
loading-unloading level of the limbs by means of pressure sensors applied under
the feet. Customized footwear may be particularly suitable for this purpose.
However, electrical prosthesis constructed for gait initiation support and training
still need to be implemented.
Adaptive Behavior of the Spinal Cord in the Transition from Quiet Stance to Walking 163

References
[1] Andersen, O.K.: Studies of the organization of the human nociceptive withdrawal
reflex. Focus on sensory convergence and stimulation site dependency. Acta
Physiol. 189(suppl. 654), 1–35 (2007)
[2] Crenna, P., Frigo, C.: A motor programme for the initiation of forwardoriented
movements in humans. J. Physiol. 437, 635–653 (1991)
[3] Bent, L.R., Potvin, J.R., Brooke, J.D., McIlroy, W.E.: Medio-lateral balance
adjustments preceding reflexive limb withdrawal are modified by postural demands.
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[4] McIlroy, W.E., Bent, L.R., Potvin, J.R., Brooke, J.D., Maki, B.E.: Preparatory balance
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[5] Sandrini, G., Serrao, M., Rossi, P., Romaniello, A., Cruccu, G., Willer, J.C.: The lower
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[6] Serrao, M., Ranavolo, A., Andersen, O.K., Conte, C., Don, R., Cortese, F., Mari, S.,
Draicchio, F., Padua, L., Sandrini, G., Pierelli, F.: Adaptive behaviour of the spinal
cord in the transition from quiet stance to walking. BMC Neurosci. 16(13), 80 (2012)
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on the lower limb nociceptive withdrawal reflex during symmetrical stance. Clin.
Neurophysiol. 123, 1035–1043 (2012)
Using Painful Sensory Stimulation to Improve
the Hemiparetic Gait

Erika Geraldina Spaich and Ole Kæseler Andersen

Aalborg University, Aalborg, Denmark


espaich@hst.aau.dk

Abstract. The nociceptive withdrawal reflex elicited by painful sensory


stimulation of the sole of the foot has been shown to produce responses that can
support the initiation and development of the swing phase in both healthy and
stroke individuals. Using this stimulation modality might have a great impact on
the rehabilitation of the hemiparetic gait. The principles behind this method and its
use in the clinical setup will be presented.

1 Introduction

Gait deficit is one of the common consequences of stroke; it is commonly


characterized by reduced speed and longer stance phase, reduced hip, knee, and
ankle flexion during swing, and reduced knee extension during early-stance in the
most affected side [1]. Gait oriented training is commonly used after stroke as
proper gait function is vital for the quality of life. It has been shown to improve
gait speed and walking distance [2]. Training includes typically conventional
physiotherapy, lower extremity muscle strengthening, overground walking
combined with stepping and cycling, and treadmill walking [3-5].
The use of functional electrical stimulation of selected lower limb muscles,
properly timed with the gait cycle, has been shown to improve gait performance
[6;7]. Placing the stimulation electrodes, calibrating the stimulation intensity, and
synchronizing the stimulation onset and offset for all muscles of interest are an
integral part of this modality of training, which might result cumbersome in some
clinical settings.
As an alternative, a different stimulation strategy involving the lower limb
nociceptive withdrawal reflex (NWR) could be used. The NWR can be elicited
using painful electrical stimulation of the sole of the foot. It results in the
coordinated activation of multiple bilateral muscle groups leading to adequate
unloading of the stimulated area while maintaining balance and ensuring
continuation of the ongoing motor programs [8;9].
The size of the NWR response has been shown to be modulated by various
factors such as the stimulation site, intensity, frequency, and body posture [8-11]).
During gait, the NWR elicited by a single electrical stimulus at various locations

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 165
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_32, © Springer International Publishing Switzerland 2014
166 E.G. Spaich and O.K. Andersen

in the sole of the foot elicits site-modulated responses [9]. These responses are
also phase-modulated, showing the strongest kinematic flexion responses during
the swing phase [9]. Furthermore, these responses change from consisting
primarily of a large hip flexion accompanied by ankle dorsiflexion immediately
after heel-off to being a large ankle dorisflexion and smaller hip flexion after toe-
off [12], showing the fine phase-modulation of the NWR.
In hemiparetic individuals, the characteristic kinematic response included
dorsiflexion of the ankle joint and flexion of the knee and hip joints when
stimulated during the late stance and swing phases [13]. Using painful sensory
stimulation of the sole of the foot to elicit the NWR could therefore be used to
initiate and facilitate the swing phase of the hemiparetic gait, helping to lift the
most affected leg and clearing the foot.
A more functional gait has been obtained during a single training session when
using both, an open-loop, single channel stimulator and a closed-loop system that
selects the stimulation site and timing [14], suggesting that this modality of
stimulation might benefit gait training.
Furthermore, eliciting the NWR during the subacute gait therapy has shown
improvements of the hemiparetic gait that outlasted the training period [15]. It is
hypothesized that cortical plasticity might have been induced as a consequence of
the intensive training involving functional gait supported by the NWR.

References
[1] Olney, S.J., Richards, C.: Hemiparetic gait following stroke. Part I: Characteristics.
Gait & Posture 4(2), 136–148 (1996)
[2] van de Port, I.G., Wood-Dauphinee, S., Lindeman, E., Kwakkel, G.: Effects of
exercise training programs on walking competency after stroke: a systematic review.
Am. J. Phys. Med. Rehabil. 86(11), 935–951 (2007)
[3] Richards, C.L., Malouin, F., Wood-Dauphinee, S., Williams, J.I., Bouchard, J.P.,
Brunet, D.: Task-specific physical therapy for optimization of gait recovery in acute
stroke patients. Arch. Phys. Med. Rehabil. 74(6), 612–620 (1993)
[4] Laufer, Y., Dickstein, R., Chefez, Y., Marcovitz, E.: The effect of treadmill training
on the ambulation of stroke survivors in the early stages of rehabilitation: a
randomized study. J. Rehabil. Res. Dev. 38(1), 69–78 (2001)
[5] Pohl, M., Werner, C., Holzgraefe, M., Kroczek, G., Mehrholz, J., Wingendorf, I., et
al.: Repetitive locomotor training and physiotherapy improve walking and basic
activities of daily living after stroke: a single-blind, randomized multicentre trial
(DEutsche GAngtrainerStudie, DEGAS). Clin. Rehabil. 21(1), 17–27 (2007)
[6] Bogataj, U., Gros, N., Kljajic, M., Acimovic, R., Malezic, M.: The rehabilitation of
gait in patients with hemiplegia: a comparison between conventional therapy and
multichannel functional electrical stimulation therapy. Phys. Ther. 75(6), 490–502
(1995)
[7] Stanic, U., Acimovic-Janezic, R., Gros, N., Trnkoczy, A., Bajd, T., Kljajic, M.:
Multichannel electrical stimulation for correction of hemiplegic gait. Methodology
and preliminary results. Scand. J. Rehabil. Med. 10(2), 75–92 (1978)
Using Painful Sensory Stimulation to Improve the Hemiparetic Gait 167

[8] Andersen, O.K., Sonnenborg, F.A., Arendt-Nielsen, L.: Modular organization of


human leg withdrawal reflexes elicited by electrical stimulation of the foot sole.
Muscle Nerve 22(11), 1520–1530 (1999)
[9] Spaich, E.G., Arendt-Nielsen, L., Andersen, O.K.: Modulation of lower limb
withdrawal reflexes during gait: a topographical study. J. Neurophysiol. 91(1), 258–
266 (2004)
[10] Andersen, O.K., Sonnenborg, F.A., Matjacic, Z., Arendt-Nielsen, L.: Foot-sole reflex
receptive fields for human withdrawal reflexes in symmetrical standing position. Exp.
Brain Res. 152, 434–443 (2003)
[11] Spaich, E.G., Emborg, J., Collet, T., Arendt-Nielsen, L., Andersen, O.K.: Withdrawal
reflex responses evoked by repetitive painful stimulation delivered on the sole of the
foot during late stance: site, phase, and frequency modulation. Exp. Brain Res. 194,
359–368 (2009)
[12] Emborg, J., Spaich, E.G., Andersen, O.K.: Withdrawal reflexes examined during
human gait by ground reaction forces: site and gait phase dependency. Medical &
Biological Engineering & Computing 47(1), 29–39 (2009)
[13] Spaich, E.G., Hinge, H.H., Arendt-Nielsen, L., Andersen, O.K.: Modulation of the
withdrawal reflex during hemiplegic gait: effect of stimulation site and gait phase.
Clin. Neurophysiol. 117, 2482–2495 (2006)
[14] Emborg, J., Matjacic, Z., Bendtsen, J.D., Spaich, E.G., Cikajlo, I., Goljar, N.,
Andersen, O.K.: Design and test of a novel closed-loop system that exploits the
nociceptive withdrawal reflex for swing-phase support of the hemiparetic gait. IEEE
Transactions on Biomedical Engineering 58(4), 960–970 (2011)
[15] Spaich, E.G., Svaneborg, N., Andersen, O.K.: Improved gait symmetry in
hemiparetic patients following gait rehabilitation supported by activation of the
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Converging Clinical & Engi. Research on NR. BIOSYSROB, vol. 1, pp. 519–523.
Springer, Heidelberg (2013)
Advanced Rehabilitation for Amputees after
Selective Nerve Transfers: EMG-Guided
Training and Testing

Agnes Sturma1, Peter Göbel2, Malvina Herceg3, Nan Gee2, Aidan Roche1,4,
Veronika Fialka-Moser3, and Oskar C. Aszmann1,5,*
1
Christian Doppler Laboratory for Restoration of Extremity Function,
Medical University of Vienna, 1090 Vienna, Austria
2
Otto Bock Helthcare Products GmbH, 1070 Vienna, Austria
3
Department of Physical and Rehabilitation Medicine, Medical University of Vienna,
1090 Vienna, Austria
4
Academic Foundation Program, Newcastle upon Tyne Hospitals NHS Trust,
Freeman Hospital, Newcastle upon Tyne, UK
5
Division of Plastic and Reconstructive Surgery, Department of Surgery,
Medical University of Vienna, 1090 Vienna, Austria
oskar.aszmann@meduniwien.ac.at

Abstract. A special kind of selective nerve transfer, targeted muscle


reinnervation, can provide upper limb amputees with up to 6 intuitive myosignals
to govern their myoelectric prosthesis. Following surgery, a comprehensive
rehabilitation package is required. It should include electromyographic (EMG)
feedback training to facilitate recruitment of newly reinnervated muscles. In order
to select appropriate tasks for training, an EMG testing tool is required that can
provide clinicians with scores directly reflecting the patient’s ability to generate
myoelectric signals. Here, an EMG testing tool implementing the Item Response
Theory for ability classification is presented. Used for testing healthy subjects and
patients, the tool was able to detect an increase of muscular coordination with
training, as well as existing deficits in motor control. These findings suggest that
this tool can assist in rehabilitation planning for patients after selective nerve
transfers.

1 Introduction

While selective transfer of nerves is an effective surgical technique for improving


prosthetic control, overall outcomes also depend on a comprehensive
rehabilitation package. Following surgery, a rehabilitation program focusing on
motor learning is required.[24] A therapy proto-col for amputees with TMR
has previously been presented by Stubblefield in 2009[34]. Additionally,
*
Corresponding author.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 169
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_33, © Springer International Publishing Switzerland 2014
170 A. Sturma et al.

recommendations for upper limb amputees rehabilitation[22] [31] and for


selective nerve transfers patients[24] are available. Furthermore, motor imagery
and EMG biofeedback have previously been shown to be useful to facilitate
recruitment of newly reinnervated mus-cles. [9] [7] [29] [15] [6] Based on this
background knowledge and our own clinical experi-ence with patients with TMR,
a “TechNeuroRehabilitation” process was developed.
EMG biofeedback is widely used for training of muscular recruitment and
relaxation in the field of rehabilitation. [14] [5] [25] For training and testing of
myoelectric signals after TMR surgery, the use of a two-site myotester (e.g. Otto
Bock MyoBoy® [28]) has been described. [17] [34] Devices with multiple
channels are preferable, as they simultaneously record all EMG signals.[30] In this
way isolated contractions of different signal strengths can be trained. In order to
select appropriate training tasks, the ability to generate myoelectric signals must
be known. However, in clinical practice the rating of performance greatly depends
on the indi-vidual scorer. Therefore, an EMG testing tool is needed for
standardised testing and rating of patients. Tools like the Noraxon Telemyo
2400G2 [23] can fulfil the requirement of testing muscular recruitment by
measuring the arithmetic mean between a predesigned profile and the patient’s
own EMG curve. However, to our knowledge no tool available on the market can
provide the clinician with scores directly reflecting the patient’s ability of
generating my-oelectric signals. Such assignment to ability classes can be
provided by the use of Item Re-sponse Theory (IRT), which is a psychometric
instrument for modeling the relationship be-tween latent traits and responses. [32]
Therefore the aim of this study was to develop a test tool based on EMG
biofeedback and IRT and to evaluate it. Here we describe how specific motor
tasks using EMG can be used for patient training, and for quantification of signal
control to adjust further training. Subjects:

2 Materials and Methods

a. Patients
5 healthy, able-bodied persons (2 male, 3 female, age 34.4 ± 9.7) were tested. The
ethics committee of the Medical University of Vienna granted their approval for
the clinical study described [1164/2013] and all participants gave their informed
consent. They performed 3 testing-sessions with 4 movements (wrist flexion, wrist
extension, finger flexion and extension of the little finger) within 2 weeks.
Additionally, 4 non-healthy persons were selected. This included two patients
with peripheral nerve injury (brachial plexus injury) and nerve transfers, one
transradial amputee (otherwise healthy) and one transhumeral amputee after TMR.

b. The TechNeuroRehabilitation Process


After selective nerve transfers, amputees underwent our group’s
“TechNeuroRehabilitation” process. The duration of this varied between patients,
but takes 1.5±0.5 years and consisted of 4 stages:
Advanced Rehabilitation for Amputees after Selective Nerve Transfers 171

Stage 1: Regeneration (0-3 months after surgery)


Approximately 3 to 6 months after surgery, the transferred nerves reached their
targets and the first contractions could be registered either by surface or needle
electrodes. During this time it was important to facilitate the cortical
representation of the non-existing arm and its move-ments, which was later used
in the rehabilitation process. This was done through motor im-agery (imagined
movements) or mirror therapy (where the patient sees the mirror image of the
sound side, where the amputated limb is expected). Another focus in this stage
was pain and oedema control as well as trunk stability, body symmetry and
restoration of range of move-ment of the existing joints. Also, first motor activity
was facilitated using bilateral gross movement patterns.

Stage 2: Signal training (about 3-15 months after surgery)


As soon as the first EMG signals could be recorded the aim of rehabilitation was
then to im-prove neuromuscular control. The patient was asked to perform
movements typical for the transferred nerves with the non-existing limb, e.g. hand
opening for the radial nerve. Different movements were tested to find those that
elicit the most powerful and distinct signals. Then, the activation of the
reinnervated muscles was trained. Since the precise control of the myoe-lectric
signals is of utmost importance for later prosthetic control, this training was
monitored closely. Visual control of motor activity was provided with the use of
EMG-biofeedback and supported the patient during the motor learning phase.

Stage 3: Prosthetic Fitting (about 12-18 months after surgery)


Once the signals were established, the final prosthesis with up to 6 electrodes was
fitted. This was done by an experienced prosthetist. For defining the final
positions of the electrodes the collaboration of surgeons, PMR specialists,
therapists, technicians and prosthetists was essen-tial. After fitting, the prosthetic
control training was performed with and without different ob-jects and
grasp/release tasks. Finally, the patient received the prosthesis for daily use.

Stage 4: Follow-ups (6, 12 and 24 months after final fitting)


While using the prosthesis at home, patients became skilled in manipulation of
everyday ob-jects. Nevertheless, some problems may have occurred as changes in
the stump may have led to the necessity for socket changes. Since the muscle
reinnervation could still continue after final fitting, the optimal electrode positions
could change over time. Thus it was very im-portant to maintain contact with the
patients after final fitting and to regularly assess their prosthetic function, pain and
quality of life.

c. The Surface EMG Test Tool


The surface electromyography (sEMG) test tool used an interactive EMG
biofeedback work-station, with an extra computer screen dedicated to the patient.
172 A. Sturma et al.

Predefined profiles demanding different movements and contraction-strengths


were presented. The aim was to follow them using visual feedback.
At the beginning of testing, the movements (e.g. hand open/close, wrist
flexion/extension, supination/pronation, elbow flexion/extension) were selected.
Then the training profiles were calibrated for all selected movements using
maximum long-term voluntary contraction (MLVC), which is a strong contraction
level that the patient is able to hold for at least five seconds. This was required as
the strength of EMG signals varied between different record-ings. These changes
may have been due to small changes in the electrode positions, the skin
conductance, and also the patient's mood[11].

d. Item Response Theory


In the next step, IRT was applied to relate the raw scores to some reference. IRT is
a psycho-metric instrument that is well-established for testing human ability,
which models the relation-ship between latent traits and item-responses (here the
predesigned profile and the patient’s tracking line)[32]. By using IRT the patient’s
raw scores are compared to a “gold standard”, determined from the scoring of 39
well-trained able-bodied subjects and transformed into the patient’s motor-ability.
Consequently, the patient’s performance could be graded using five ability-
classes:
I) Excellent (no further training is required);
II) Good (some refinements need to be done);
III) Average (not able to control the prosthesis yet, but will most likely learn
with some training);
IV) Poor (a lot of training is required to get a good prosthetic function);
V) Incapable (no muscular control).
The IRT scores were generated for each movement, and a total score was
generated using the arithmetic mean of the movements’ scores. A value between 1
and 1.5 represents an ability class of I, between 1.5 and 2.5 an ability class of II,
between 2.5 and 3.5 an ability class of III and so forth. This provided a brief
overview of the patient’s abilities, and also determined the requirements for
further training in detail.

3 Results

The IRT testing results of the five healthy persons are shown in table 1. A small
increase in muscle coordination was observed across the means for the three
measurements.
Advanced Rehabilitation for Amputees after Selective Nerve Transfers 173

Table 1 IRT Scores for 5 healthy subjects measured 3 times within 2 weeks. Smaller values
mean a better muscular recuruitement, with 1 being the best score. A value between 1 and
1.5 means an abilty class of 1, between 1.5 and 2.5 an ability class of 2, etc.

RMSE
P1 P2 P3 P4 P5 Mean of
mean
M1 2.59 1.42 2.24 1.13 1.96 1.87 0.595
M2 1.17 1.45 2.86 1.00 1.28 1.55 0.751
M3 1.67 1.24 2.65 1.00 1.17 1.55 0.666

The results for the 4 patients are presented in table 2.


Patient 1 (brachial plexus injury, nerve transfer, training expe-rience) Patient 2
(brachial plexus injury, nerve transfer, no training experience at the be-ginning)
Transradial amputee Amputee after targeted muscle reinnervation

Table 2 IRT scores of the 4 patients. As before, 1 indicates the best possible muscular
coordination and 5 the worst.

P1 P2 P3 P4
M1 2.01 4.18 2.25 3.26
M2 - 2.64 - 2.32

Both patients with brachial plexus injury showed a completely functionless


hand, but never-theless were able to generate 2 independent sEMG signals. The
first of these brachial patients had trained the activation of these signals for 9
months, while the second patient had only re-cently started training when testing
was performed. Using the sEMG test tool, the well-trained patient reached a score
of 2.01. In contrast, the untrained patient had a score of 4.18 and he also reported
that he felt muscle fatigue after the 40 minutes of testing. When testing was
repeated after 5 months of training, his ability score had improved to 2.64.
The transradial amputee had some myoelectric training before testing, but was
not fitted with a prosthesis. His overall tracking performance was 2.25.
The transradial amputee and the first patient with brachial plexus injury were
were unavailable for follow-up measurements.
The TMR patient performed at class III (3.26) five months after surgery using 4
different muscles and improved with training to class II (2.32) using 5 different
signals one year after surgery. At this time he was also able to reliable control a
prosthesis.
174 A. Sturma et al.

4 Discussion

Selectively transferring nerves, as in the case of TMR, can provide amputees with
up to 6 in-tuitive signals to govern their prosthesis. After nerve transfer the central
nervous system needs to adapt to the new muscular interface.[1] To support this
process of motor learning, a rehabil-itation program is needed. Surface EMG
biofeedback has been shown to be a useful tool to facilitate this learning process.
[12] [24] Therefor it was incorporated into the development of the
“TechNeuroRehabilitation” program described here, to aid patients after selective
nerve transfers achieve intuitive prosthetic control.
To monitor the rehabilitation process and to select appropriate training, a tool to
measure muscular control and recruitment was needed. Many tests for hand
function are available in the field of upper limb prosthetics [4] [20] [8] [33], but
they can only be used after prosthetic fitting. However, a suitable testing tool
within the rehabilitation process prior to actual pros-thetic fitting does not exist to
our knowledge. Testing can also be achieved by virtual reality systems, which are
currently used in laboratory settings to train and test EMG signals for prosthetic
control. [13] [35] Some of these systems also provide performance scores of
motor control. To our knowledge, these systems are not used clinically for
amputees after TMR and are dependent on patients having prior experience of
learning how to use their EMG signals for control. Therefore, they cannot be used
at the beginning of rehabilitation. Furthermore, the available systems do not show
which muscles and functions need to be trained in a specific way. The same
problem occurs with current EMG testing systems that cannot provide the cli-
nician with an easy score for motor recruitment.
To reach this goal, a test tool demanding specific motor tasks was developed.
Using visual feedback the patient was asked to follow a predesigned profile. Later,
the normalized RMSE between the patient’s tracking line and the profile is
calculated. To compare the NRMSE scores (and therefore the difficulty between
different motor tasks) with a normative popula-tion, IRT was used. Consequently,
the patient’s performance could be graded using five abil-ity-classes, ranging
between “excellent” and “incapable”. This helped the therapist plan the
rehabilitation process.
To evaluate the usability and accuracy, five healthy subjects were tested three
times in a row. An increase of muscular coordination within each measure was
shown for the mean value. This indicates that the sEMG test tool is able to detect
changes in neuromuscular coordination. Findings in patients were similar: Two
patients with similar nerve transfers but different durations of biofeedback training
had a notable discrepancy in their IRT scores. Furthermore the effect of training
could be shown directly on the second patient with brachial plexus injury and on
the amputee after targeted muscle reinnervation.
Nevertheless, the explanatory power of this study is limited due to small sample
size, different diagnosis and different times of measuring. Also, the population
sample of 39 well-trained able-bodied subjects as “gold standard” may not be
Advanced Rehabilitation for Amputees after Selective Nerve Transfers 175

ideal, since they are not the target group for those measurements. With on-going
testing, a database with amputees’ abilities can be created and used as a new
standard.
To conclude, the sEMG test tool was able to successfully measure the ability of
muscular re-cruitment in healthy subjects and patients after selective nerve
transfers. It assists in rehabili-tation planning for patients after selective nerve
transfers. Further studies are needed to evalu-ate reliability and validity compared
to other outcome measures. Also, a broader scope of ap-plication for testing EMG
biofeedback training (e.g. in patients after stroke) can be explored.

Acknowledgment. The scientific work of the Christian Doppler Laboratory for


Bionic Reconstruction is spon-sored by the Christian Doppler Gesellschaft,
Boltzmanngasse 20, 1090 Vienna, Austria.
A.S. thanks Michael Krutzler and Aidan Roche for their support.

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Learning to Change a Reflex to Improve
Locomotion

Aiko K. Thompson

Helen Hayes Hospital, New York State Department of Health, West Haverstraw,
NY 10993 USA
and
Wadsworth Center, New York State Department of Health, Albany, NY 12201 USA
and
The Department of Neurology, Neurological Institute,
Columbia University, New York, NY 10032 USA
and
The Department of Biomedical Sciences, State University of New York,
Albany, NY 12222 USA
thompsona@helenhayeshosp.org

Abstract. After spinal cord injury (SCI), spinal reflex activity often becomes
abnormal, contributing to common movement problems, such as spasticity and
weak voluntary muscle control. Learning to change a reflex through an operant
conditioning protocol may enhance motor function recovery. Indeed, in spastic
people with hyperreflexia due to incomplete SCI, down-conditioning of the soleus
H-reflex improved walking speed, right-left step symmetry, and modulation of
EMG activity in multiple muscles bilaterally. Operant conditioning protocols
could be developed to modify other spinal reflexes or corticospinal connections
and might be combined with other rehabilitation methods to enhance recovery in
people with SCI or other neurological disorders.

1 Introduction

The central nervous system (CNS) changes throughout life and activity-dependent
plasticity occurs continually everywhere in the CNS. Such ubiquity of activity-
dependent plasticity in the CNS has become increasingly recognized over the past
several decades [1, 2]. In particular, understanding that the plasticity associated
with motor skill acquisition is not limited to the brain or the cerebral cortex but
rather extends all the way down to the spinal cord has been advancing the field of
motor control and rehabilitation neuroscience research [1-3]. It is now known that
extensive training or skill acquisition that repeats certain patterns of peripheral
sensory and/or descending inputs to the spinal cord induces plasticity that shapes
the activity of spinal reflex pathways, and may also affect activity elsewhere in the
CNS [2, 3]. Thus, to facilitate motor skill re-learning after CNS damage, it is

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 179
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_34, © Springer International Publishing Switzerland 2014
180 A.K. Thompson

important to understand how plasticity is induced and guided at many different


CNS sites, including spinal cord pathways, and how these changes are combined
together to produce a new skill while maintaining or improving existing skills.
Operant conditioning, in which modification of a behavior is brought about by
the consequence of that behavior, is very effective in inducing learning. Through
operant conditioning, even the simplest behaviors, such as spinal reflex behaviors,
can be changed. Operant conditioning of a spinal reflex, which is comprised of a
spinal reflex, supraspinal influence over that reflex pathway, and the spinal cord
plasticity induced by that supraspinal influence [6], provides an experimental
model for studying motor skill acquisition. By basing reward on reflex size, the
conditioning protocol operantly conditions the brain to generate supraspinal
influence that appropriately affects reflex size. In addition to providing a model
for skill acquisition research, reflex conditioning is now showing its effectiveness
in enhancing neurorehabilitation by inducing and guiding beneficial CNS
plasticity.

2 Learning to Change a Reflex

2.1 Why Do We Want to Change a Reflex?


Spinal reflexes normally function as components of complex skills such as
locomotion [7, 8]. However, spinal reflex activity is often altered after SCI, and
abnormal activity in spinal pathways contributes to motor impairments in multiple
ways [9-12]. Ia excitation is heightened and H-reflex modulation is diminished;
and Ib inhibition, reciprocal inhibition, presynaptic inhibition, and recurrent
inhibition are impaired (reviewed in [13]). Alterations in motoneuron and
interneuron properties also contribute to spastic reflex behaviors [14, 15]. Thus,
reducing abnormalities in the activity of one or more of these spinal pathways may
improve function recovery after SCI.
Below in the initial study, to test the hypothesis that operant conditioning of
spinal reflexes can enhance restoration of motor function after SCI, the soleus H-
reflex was down-conditioned, because excitation of motoneurons by muscle
spindle afferents is enhanced and H-reflex activity is often mal-modulated during
walking and standing in people after SCI [9, 11, 16, 17].

2.2 Operant Conditioning of a Spinal Reflex in People


In humans, reflex operant conditioning was applied first to the biceps brachii
stretch reflex [18] and more recently to the soleus H-reflex [5]. The reflex
conditioning protocol in humans is comparable to that in animals [6, 19], except
for the number of trials; humans perform only 675 trials/wk, only 2-5% as many
as animals.
The standard protocol comprises 6 baseline sessions and 24 (in neurologically
normal subjects) or 30 (in subjects with CNS damage) conditioning sessions at a
Learning to Change a Reflex to Improve Locomotion 181

rate of 3 sessions/wk. In each session, the soleus H-reflex is elicited while the
standing subject maintains a defined stable level of soleus EMG activity. M-wave
size and background EMG are kept constant for all the H-reflex trials within and
between sessions. In each baseline session, 3 blocks of 75 control H-reflex trials
(i.e., 225 H-reflexes) occur. In each conditioning or follow-up session, 20 within-
session control H-reflexes are measured as in the baseline sessions and then 3
blocks of 75 (i.e., 225) conditioned H-reflex trials occur. In these conditioned H-
reflex trials, the subject is encouraged to increase (HRup mode) or decrease
(HRdown mode) H-reflex size and is given visual feedback after each stimulus
that indicates whether the H-reflex was larger (HRup mode) or smaller (HRdown
mode) than a criterion value.
In neurologically normal subjects, over the 24 conditioning sessions, H-reflex
size gradually increased in 6 of 8 HRup subjects and decreased in 8 of 9 HRdown
subjects, resulting in final sizes of 140(±12SEM)% and 69(±6)% of baseline size,
respectively. In these subjects, the final H-reflex change was the sum of within-
session change (i.e., task-dependent adaptation) that appeared within 4-6 sessions
and persisted thereafter (+13% in HRup and -15% in HRdown) and across-session
(i.e., long-term) change that began after 10-12 sessions and increased gradually
thereafter (+27% in HRup and -16% in HRdown). (See [5] for complete
discussion of task-dependent adaptation and long-term change.)

3 Changing a Reflex to Improve Locomotion


This evidence for therapeutic efficacy in rats [20], together with the successful
development of the human H-reflex conditioning protocol [5] and the evidence
that it induced long-term plasticity in the human H-reflex pathway [5, 21],
encouraged an effort to determine whether H-reflex conditioning could improve
locomotion in people. We studied the therapeutic efficacy of down-conditioning
the soleus H-reflex [4] in spastic individuals with chronic incomplete SCI.
Over 30 down-conditioning sessions, the soleus H-reflex decreased in two-
thirds of the subjects (Fig. 1) and remained smaller several months later [4]. In the
subjects in whom H-reflex decreased significantly, locomotion improved; walking
speed increased and right-left symmetry improved (Fig. 2), with better EMG
modulation across the step-cycle in the muscles of both legs. In these subjects, the
H-reflex decrease was also evident during locomotion (i.e., 59% of initial value),
which helped to explain the improved gait. Furthermore, beginning about 5 weeks
into the conditioning sessions, these subjects commented spontaneously that they
were walking faster and farther in their daily lives, and several noted less clonus,
easier stepping, and/or other improvements (Fig. 3). Locomotion did not improve
in the subjects in whom H-reflex down-conditioning was not successful or in
control subjects in whom the H-reflex was simply measured over 30 sessions
without conditioning. These first results in people with SCI, together with the rat
study, suggest that operant conditioning of spinal reflexes can improve gait
recovery after chronic incomplete SCI, and possibly in other disorders as well
(e.g., [22]).
182 A.K. Thompson

Fig. 1 Average (±SE) H-reflexes for baseline and conditioning sessions for down-
conditioning subjects with SCI (A, N=6, [4]) and for normal subjects (B, N=8, [5]) in
whom the H-reflex decreased significantly, and for control subjects with SCI (C, N=4). In
the subjects with SCI (A), over the 30 conditioning sessions the H-reflex decreases to 69%
of the baseline value, the same extent of decrease as in normal subjects (B). This decrease
is specific to down-conditioning, as it is not present in control subjects with SCI (C).

Fig. 2 A: 10-m walking speeds after the 30 conditioning or control sessions (mean±SE % of
baseline speed) for subjects with SCI in whom the H-reflex did or did not decrease
significantly. B: Step-cycle symmetry before (open bars) and after (shaded bars) after the
30 conditioning or control sessions for subjects with SCI in whom the H-reflex did or did
not decrease significantly. Symmetry is measured as the ratio of the time between the
nonconditioned leg’s foot contact (nFC) and the conditioned (or simply “stimulated” in
control subjects) and initially more impaired leg’s foot contact (cFC), to the time between
cFC and nFC. A ratio of 1 indicates a symmetrical gait. Initially, the ratio is >1. After the
30 conditioning or control sessions, the ratio has decreased toward 1 in the subjects in
whom the H-reflex decreased, while it has increased slightly in the subjects in whom the H-
reflex did not decrease. (From [4]).
Learning to Change a Reflex to Improve Locomotion 183

Fig. 3 Spontaneous comments made by subjects over the course of study. “×” indicates
when a subject made the comment for the first time. Every subject in whom the H-reflex
decreased reported walking faster and farther, and that these reports did not occur until
substantial H-reflex decrease had occurred (see Fig. 1) (From [4]).

In data to date, the probability of successful conditioning and the magnitude of


reflex change are comparable in people with or without incomplete SCI [4, 5, 20,
23]. However, these two populations differ markedly in the proportions of task-
dependent adaptation and long-term change in the final conditioned H-reflex [4].
Task-dependent adaptation (i.e., within-session change), which is thought to
reflect immediate change in cortical influence (e.g., on presynaptic inhibition), is
significantly greater in neurologically normal subjects than in subjects with SCI
(-15% vs. -7%). In contrast, long-term H-reflex change (i.e., across-session
change), which is thought to reflect spinal cord plasticity, is significantly greater
in subjects with SCI than in normal subjects (-24% vs. -16%)[4].
This difference between people with and without SCI in the magnitude of long-
term plasticity is reflected in the difference between them in the locomotor effects
of H-reflex conditioning. As described above, appropriate H-reflex conditioning
markedly improved locomotion in people with SCI [4]; while H-reflex
conditioning had no detectable effect on locomotion in people without SCI [24].

4 Operant Conditioning as a New Therapeutic Approach

In addition to the fact that it is non-invasive and non-pharmacological, the key


features of operant conditioning are that it is both specific and flexible. By basing
reward on the output of a specific CNS pathway (e.g., the soleus H-reflex
pathway), it can target plasticity to that pathway; and by selecting the specific
reward contingency (i.e., up- or down-conditioning), it can strengthen or weaken
that pathway as needed. An appropriate operant conditioning protocol could
produce targeted plasticity that addresses the specific motor deficits of each person.
Conditioning protocols might target other proprioceptive or cutaneous reflex
pathways, or even corticospinal connections [25]. It should also be possible to
design conditioning protocols that complement existing therapeutic methods, such
184 A.K. Thompson

as partial body-weight supported treadmill training and constraint-induced


movement therapy, in order to maximize functional recovery. For example, H-
reflex down-conditioning might be performed during the swing phase of the step
cycle, when the H-reflex is very small or absent in normal subjects but abnormally
large in people with spastic hyperreflexia due to chronic SCI [9, 10]. By targeting
the exact time when reflex activity is abnormal, such a protocol might help restore
appropriate phase-dependent reflex modulation during walking [26]. Conditioning
protocols are likely to be particularly useful once significant regeneration becomes
possible. Newly generated spinal cord connections need to be appropriately
shaped, in order to provide useful motor function. Finally, conditioning protocols
might improve treatment of other peripheral or central neuromuscular disorders
(e.g., [22]).
While an operant conditioning protocol can target plasticity to a specific
pathway, the beneficial impact of appropriate conditioning appears to extend far
beyond the effects that can be directly attributed to that plasticity. In people with
SCI, unilateral soleus H-reflex down-conditioning improved the locomotor
behaviors of knee and ankle extensor and flexor muscles in both legs, which
presumably contributed to the improvement in walking speed and symmetry [4].
The plasticity underlying a smaller soleus H-reflex in one leg cannot itself account
for such broad beneficial impact. Together with animal data [20, 27], this impact
implies that H-reflex conditioning triggered additional plasticity in other pathways
important for locomotion, and thereby improved the entire behavior. If
comparable processes are triggered by other appropriately selected operant
conditioning protocols, the therapeutic value of these protocols may be greatly
enhanced.

Acknowledgment. The author’s work was supported in part by the New York
State Spinal Cord Injury Research Trust [C023685]; the National Institutes of
Health [NS069551]; and the Helen Hayes Hospital Foundation.

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[12] Dietz, V., Sinkjaer, T.: Spastic movement disorder: Impaired reflex function and
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Advances in Robotic Gait Training

Herman van der Kooij, Edwin H.F. van Asseldonk, Bram Koopman,
Gijs van Oort, Jos Meuleman, H. Carsten van Voort, and S.M. Behrens

Department of Biomechanical Engineering, University of Twente, PO Box 217, 7500 AE,


Enschede, The Netherlands
h.vanderkooij@utwente.nl

Abstract. In this presentation an overview will be given of robotic gait


trainers. We will focus on devices developed at the University of Twente.

1 Introduction

Robotic gait trainers developed in the past ten years [1] made it possible to
intensively train patients with neurological disorders, like stroke survivors,
paraplegics, and children with cerebral palsy. These patient groups benefit
from intensive training programs that facilitate (faster) recovery. Since
manual therapy is physical demanding and labor intensive, robot gait
trainers relieve therapist from their heavy work and also makes therapy
much less labor intensive, which is beneficial especially in those countries
with a graying population.

2 LOPES I

LOPES I was developed by the University of Twente for stroke survivors


and spinal cord injured patients.
From the beginning three principles guided the decisions taken in the
design and control of the device:
• The patient should be as actively involved in the training as
possible;
• The device should not change the nature of human walking;
• The patient should be free to make task execution errors.

Current findings from animal [2] and human [3], [4] neuro-scientific
studies support these three principles.
Based on these principles the degrees of freedom of the LOPES I were
chosen such that the device allows natural motion and compensatory
strategies of the patient. In particular, whole body motions are

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 187
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_35, © Springer International Publishing Switzerland 2014
188 H. van der Kooij et al.

not constrained, resulting in the patients having to balance


themselves instead of being balanced by the device. For the control these
principles require that LOPES I has to be force- controlled instead of
position-controlled as the first generation of robotic gait trainers. This
allows selectively and partially supporting patients according to their needs.
Force control is realized by the combination of series elastic
actuation and Bowden cables [5]. Since LOPES is force controlled and
does not over-constrain human locomotion, it is possible to selectively
and partial support different functions of human gait, such as foot clearance
[6]. Since joint angles during gait depend on walking speed, we
reconstructed a reference gait generator that is dependent on progression
speed [7]. The therapist can easily adapt this reference gait by
modifying key event parameters. The LOPES I has been evaluated in a
small population of chronic stroke survivors with stiff knee gait, for which
LOPES therapy increased walking speed and knee flexion [8]. LOPES I
training in a small cohort of SCI patients increased their functional outcome
measures [9]. Robotic gait trainers can also be used for diagnostic
purposes. We showed that LOPES I can be used to estimate the impedance of
the knee, the hip, and the impedance between hip and knee, with the use of
system identification techniques [10]. Estimating the impedance of the leg
joints allows to quantify impairments such as stiff-knee gait.

3 LOPES II

From the knowledge and expertise gained with LOPES I, two companies
(MOOG and Demcon) and the University of Twente developed the LOPES II
(Fig. 1). The differences with LOPES I are, that Lopes II:
• Uses admittance control instead of impedance control which
increases the range from no support to full support;
• Has a lower reflected inertia, since a too high reflected inertia
affects the kinematics and metabolic costs of human gait [11];
• Has more passive degrees of freedom so that the device interferes
even less with the natural dynamics of human gait;
• Has a non-exoskeleton structure which minimizes donning on
doffing time, and does not obstruct arm motion;
• Has an improved intuitive interactive graphical user interface,
intended for usage by therapists.

At this moment LOPES II is being optimized and clinically evaluated.


The results will be incorporated in a new version, LOPES III, which is
meant for market introduction.
Advances in Robotic Gait Training 189

Fig. 1 Impression of the LOPES II

Fig. 2 Impression of the Mobile LOPES. A: Bodyweight support(BWS) and patient lift; B)
XYZ Table with adjustable stiffness ; C) Trunk stabilization system; D) Torque controlled
shank and thigh actuation; E) Powered Mobile Base; and F) Touchscreen user interface.
190 H. van der Kooij et al.

4 Mobile LOPES

LOPES I and II, as many other robotic gait trainers can only be used in
combination with a treadmill. This is a disadvantage since many patients
and their medical doctors and physicians prefer over ground walking since
they consider this as more ecological valid.
To overcome this limitation of current robotic gait trainers UT and KACST
developed a prototype of the Mobile LOPES (Fig. 2). The Mobile LOPES is
suited for over ground walking, and supports walking and balance control
of neurologic impaired patients to enhance neural recovery.

References
[1] Colombo, G., Joerg, M., Schreier, R., Dietz, V.: Treadmill training of paraplegic
patients using a robotic orthosis. J. Rehabil. Res. Dev. 37(6), 693–700 (2000)
[2] Van Den Brand, R., Heutschi, J., Barraud, Q., DiGiovanna, J., Bartholdi, K.,
Huerlimann, M., Friedli, L., Vollenweider, I., Moraud, E.M., Duis, S., Dominici, N.,
Micera, S., Musienko, P., Courtine, G.: Restoring Voluntary Control of Locomotion
after Paralyzing Spinal Cord Injury. Science 336(6085), 1182–1185 (2012)
[3] van Asseldonk, E.H.F., Wessels, M., Stienen, A.H.A., van der Helm, F.C.T., van der
Kooij, H.: Influence of haptic guidance in learning a novel visuomotor task. J.
Physiol. Paris 103(3), 276–285 (2009)
[4] Domingo, A., Ferris, D.P.: Effects of physical guidance on short-term learning of
walking on a narrow beam. Gait & Posture 30(4), 464–468 (2009)
[5] Veneman, J., Ekkelenkamp, R., Kruidhof, R., van der Helm, F., van der Kooij, H.: A
Series Elastic- and Bowden-Cable-Based Actuation System for Use as Torque
Actuator in Exoskeleton- Type Robots. The International Journal of Robotics
Research 25(3), 261–281 (2006)
[6] Koopman, B., van Asseldonk, E.H., van der Kooij, H.: Selective control of gait
subtasks in robotic gait training: foot clearance support in stroke survivors with a
powered exoskeleton. J. Neuroengineering Rehabil. (1), 3 (in press, 2013)
[7] Koopman, B., van Asseldonk, E.H.F., van der Kooij, H.: Speed dependent joint
trajectory generation for robotic gait trainer. J. Biomech. (accepted)
[8] van Asseldonk, E.H.F., van der Kooij, H.: Robot-aided gait training with LOPES,” in
Neurorehabilitation Technology. In: Dietz, V., Nef, T., Rymer, W.Z. (eds.)
Neurorehabilitation Technology, vol. 21, pp. 379–396. Springer, London (2012)
[9] Fleerkotte, B.M., Koopman, B., Buurke, J.H., van Asseldonk, E.H.F., van der Kooij,
H., Rietman, H.S.: The effect of impedance-controlled robotic gait training on
walking ability and quality in individuals with chronic incomplete spinal cord injury:
An explorative study. JNER (accepted)
[10] Koopman, B., van Asseldonk, E.H.F., van der Kooij, H.: In vivo measurement of
human knee and hip dynamics using MIMO system identification. presented at the
Proceedings of 32nd Annual Internation. Conference of the IEEE EMBS, Buenos
Aires (2011)
[11] Meuleman, J.H., van Asseldonk, E.H., van der Kooij, H.: The effect of directional
inertias added to pelvis and ankle on gait. J. Neuroeng. Rehabil. 10(1), 40 (2013)
Assessing of Motor Performance
in Stroke Using Body Worn Sensing

Fokke B. van Meulen1 , Jasper Reenalda2 , and Peter H. Veltink1


1
University of Twente, MIRA Institute for Biomedical Engineering
and Technical Medicine, Biomedical Signals and Systems,
Enschede, The Netherlands
{f.b.vanmeulen,p.h.veltink}@utwente.nl
2
Roessingh Research and Development, The University of Twente,
MIRA Institute for Biomedical Engineering and Technical Medicine,
Laboratory of Biomechanical Engineering, Enschede, The Netherlands
j.reenalda@rrd.nl

Abstract. As a part of the EU project INTERACTION, a modular and


unobtrusive body worn sensing system has been developed for the objective
assessment of capacity and performance of body balance and arm movements.
Performance and capacity measures were proposed and clinically tested in
stroke subjects and results were compared with results of frequently used
clinical tests. First results show a discrepancy between subjects’ ability to
use their affected side as evaluated with clinical tests and their actual per-
formance during daily life tasks.

1 Introduction
Stroke often results in impaired body balance and/or arm function. Am-
bulatory qualitatively assessment of body balance and arm function while
performing activities of daily living is essential for optimal guidance of reha-
bilitation therapy. The objective of this study is to evaluate in stroke patients,
body balance and arm capacity and performance while performing activities
of daily living in a simulated ambulatory setting using the INTERACTION
body worn sensing system. Parameters will be related to results of clinical as-
sessments of balance control: Berg balance scale [1] and arm function: upper
limb part of the Fugl-Meyer test [2].

2 Materials and Methods


Seventeen stroke subjects were included in a clinical study, which has been
approved by the local medical ethical committee [3]. Subjects were asked
to perform different activities of daily living in a simulated ambulatory
setting. Using previously developed instrumented shoes (ForceShoesTM -
Xsens, Enschede, The Netherlands) and an ambulatory 3D human kinematic

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 191
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_36,  c Springer International Publishing Switzerland 2014
192 F.B. van Meulen, J. Reenalda, and P.H. Veltink

measurement system (MVN Biomech, Xsens, Enschede, The Netherlands),


capacity and performance measures of body balance control and arm func-
tion, were estimated.
Parameters to qualitatively evaluate ambulation, which are based on
Schepers et al. [4], are: step width, step length, swing/step phase ratio, motion
of the center of pressure (CoP) and the center of mass (CoM). Qualitative
parameters of arm function are: relative distance between hand, sternum and
pelvis; differences in reaching using the affected arm and the non-affected
arm and synergies of shoulder abduction/activation and elbow flexion.

3 Results
Preliminary results of two subjects show differences between the capacity of
reaching movements (maximum reached area of the hand) and the actual
performance of a subject’s affected side. Although a subject had the capacity
to use its affected arm, the arm was hardly used - in quality and quantity -
during the activities of daily living.
Furthermore, differences are found in asymmetry of CoP and estimated
CoM while subjects are standing, performing a 10 meter walk test and walk-
ing while performing other arm tasks. CoP and CoM shifted more towards the
non-affected side while performing more difficult combinations of activities.

4 Discussion
The use of the INTERACTION system enables the measurement of balance
and arm performance parameters during activities of daily living without be-
ing restricted to a laboratory environment. Measured performance parame-
ters vary per individual and per task, but results did not appear to correspond
with the results of the frequently used tests and clinically assessed functional
motor capacity. This supports the need for assessment of the quality and
quantity of motor performance during daily-life activities in stroke survivors.
However, in-home tests need to be performed to evaluate the possibility to
assess motor performance in a real daily life setting.

Acknowledgment. This study is part of the INTERACTION project, which


is partially funded by the European Commission under the 7th Framework Pro-
gramme (FP7-ICT-2011-7-287351).

References
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Assessing of Motor Performance in Stroke Using Body Worn Sensing 193

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Improving Interlimb Coordination Following
Stroke: How Can We Change How People Walk
(and Why Should We)?

Erin V. Vasudevan1,2 and Eileen M. Kirk1,3


1
Moss Rehabilitation Research Institute, Einstein Healthcare Network,
Elkins Park, PA 19027 USA
2
School of Health Technology and Management,
SUNY Stony Brook University, Stony Brook, NY 11794 USA
erin.vasudevan@stonybrook.edu
3
Shriners Hospitals for Children, Honolulu, HI 96826 USA
embkirk@gmail.com

Abstract. A frequent and debilitating consequence of stroke is hemiparesis – a


weakness on one side of the body – which contributes to asymmetric interlimb
coordination during walking. Such asymmetries have been associated with
decreased gait efficiency, which may prevent or limit the return to school, work,
and the community. Here, we discuss several approaches to gait rehabilitation that
have been shown to reduce interlimb coordination asymmetries post-stroke. We
also present counterarguments and discuss whether retraining symmetry post-
stroke is optimal for achieving gains in functional mobility. Overall, while it is
possible to alter interlimb coordination following stroke, it is still not entirely
certain that we should.

1 Introduction
Stroke is a leading cause of adult disability, affecting ambulation, performance of
activities of daily living, communication, and cognition. Walking, in particular, is
fundamental to physical independence and improvement of walking function is the
goal most frequently voiced by stroke survivors [1]. Despite this, a minority of
people (7-22%) are able to regain sufficient function to be considered fully
independent community ambulators following a stroke [2, 3]. There is, therefore, a
significant need to understand how we should retrain gait to maximize functional
mobility gains in this population.
There are a number of different ways gait improvements can be documented [4-
6]. Many rehabilitation outcomes are measured by the performance of specific
tasks. The 10m walk test, for instance, is frequently used to evaluate preferred and
maximal gait speeds over a short (10m) distance. As a clinical measure, this can
be quite powerful, as gait velocity is indicative of overall gait performance and
can differentiate levels of disability: a velocity of 0.8m/s is often considered the

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 195
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_37, © Springer International Publishing Switzerland 2014
196 E.V. Vasudevan and E.M. Kirk

minimum threshold for community ambulation [7, 8]; people who are able to
ambulate in a shopping center have a mean gait speed of 1.14m/s [2]. Such
performance measures, however, provide little insight into how these tasks are
accomplished. Some people with hemiparesis due to stroke may walk faster by
using inefficient compensatory strategies, such as increasing the speed of the
paretic swing phase by hip hiking and circumducting the leg. Others may use more
normative gait coordination, which is likely to be more efficient. Laboratory-based
measurements of walking kinematics, kinetics, and EMG may provide more
insight into the underlying neuromuscular control of walking and more accurately
pinpoint targets for rehabilitation [5, 6]. In this paper, we will focus on how stroke
affects interlimb coordination – specifically, coordination between the two legs –
during walking and how such abnormalities can be corrected.

2 Interlimb Coordination Following Stroke

Interlimb coordination (i.e., gait symmetry) likely characterizes walking deficits


following stroke better than intralimb coordination [9]. Normal gait tends to be
symmetric in kinematics and dynamics. There is, for instance, less than a 6%
difference in vertical force and temporal parameters between the two legs [10, 11].
While the precise characteristics of post-stroke gait vary by the location and
severity of the stroke, among other variables [12], many individuals present with
significant asymmetry in temporal (e.g., single- or double-limb support time) and
spatial (e.g. step length, step width) measures of interlimb coordination [9, 10, 13].
Interlimb coordination deficits most commonly manifest as an extended period of
single-limb support on the nonparetic limb coupled with a longer swing phase on
the paretic limb. Simply put, individuals tend to favor the paretic limb, spending
less time on it in single support and extending the duration of swing phase.
Various mechanisms have been proposed to explain these alterations in
spatiotemporal interlimb coordination [13-16]. For instance, a decrease in
available power to quickly swing the paretic limb through to heel strike may
contribute to longer swing phase duration on the paretic side. Impaired balance
and strength make it difficult to support the body with the paretic limb, leading to
a reduction in single limb support time on this side, relative to the nonparetic side.
Indeed, vertical ground reaction forces are decreased on the paretic limb compared
to the nonparetic limb [15]. Other work has shown that step length asymmetries
are related to diminished propulsive force of the paretic limb, as well as decreased
work and power of the hemiparetic plantar flexors [13, 16]. Altogether, compared
to healthy adults, hemiparesis leading to asymmetric interlimb coordination render
walking more metabolically costly. This is due to a combination of factors,
including the additional mechanical work required by the paretic side to lift the
center of mass and generate the force needed to bring the leg through swing phase
[17-20].
Improving Interlimb Coordination Following Stroke 197

3 Gait Training to Alter Interlimb Coordination

Traditional rehabilitation interventions are limited in their ability to improve gait


symmetry. For example, locomotor training without body weight support, with
body weight support, and with therapist or robotic assistance have been associated
with improvements in postural control, gait speed, and/or endurance, but gait
symmetry improvements are more modest [21-23]. Other interventions designed
with the goal to improve gait symmetry have met with more success. In one, Kahn
and Hornby [24] found that 20 minutes of unilateral step training with the
unimpaired limb on a treadmill improved step length asymmetry during walking
over ground. The authors reported asymmetry as a ratio of unimpaired and
impaired step lengths (this was subtracted from 100, thus 0% = perfect symmetry)
and found that this changed from 49% before training to 36% after a single
session. Stated differently, step length symmetry improved 26% from the initial
asymmetry (i.e. 13% change/49% initial value). The effects of a single session
were retained up to 24 hours; when participants were trained over 10 days, the
alteration to gait symmetry were retained up to two weeks.
Another approach uses rhythmic auditory stimulation to synchronize
hemiparetic stepping patterns into stable temporal relationships – the rhythm is
thought to provide a temporal template onto which movements are mapped [25-
27]. Three weeks of training with rhythmic auditory stimulation significantly
altered swing time symmetry (39% improvement from baseline) compared to a
group who was trained using more conventional physical therapy methods (e.g.
neurodevelopmental therapy/Bobath-based training – 20% improvement) [27].
A third approach makes use of the nervous system’s ability to adapt.
Adaptation is defined as the process of gradually modifying a well-practiced
movement to accommodate a novel, perturbing context or environment [28].
Introducing a perturbation that exaggerates movement errors initially makes the
movement worse; over time, however, errors are reduced to baseline levels as the
nervous system makes adjustments to the feedforward motor plan. These
adjustments persist when the perturbation is removed, resulting in aftereffects that
correct the original errors. Gait adaptation has been investigated using a variety of
paradigms in different neurological populations [24, 29-37]. For the purposes of
this review, we will briefly focus on adaptive processes driven by a split-belt
treadmill, which has two separate belts that can drive each leg at a different speed
(for reviews, see [29, 38, 39]). Spatiotemporal measures of interlimb coordination
(e.g. step length, double support duration) can be made more symmetric in stroke
survivors following 10-15 minutes of split-belt walking when the limb with the
shorter step length is trained at the faster speed [35, 39-41]. Furthermore, a
relatively short training period can cause large changes in coordination: for
example, hemiparetic individuals with an average step length asymmetry of 0.15m
improved this to <0.05m immediately following 15 minutes of split-belt walking –
roughly a 67% improvement in symmetry [35]. Improvements reported over the
course of a four-week split-belt training study were not as large (~32% change in
198 E.V. Vasudevan and E.M. Kirk

step length symmetry from pre- to post-training), but these were retained nearly
100% for upwards of 3 months post-training [40].
Interestingly, while this body of work has shown that gait asymmetries can be
reduced with certain types of training, the link to improvements in functional
mobility is less clear. In their long-term training study, Reisman et al. [40] found
that while split-belt training improved step length symmetry, there was no
concurrent change in preferred walking speed. Although Kahn and Hornby [24]
found improvements in preferred gait speed following unilateral stepping training,
there was no correlation between these gains and improvements in step length
symmetry. In a randomized trial of rhythmic auditory cueing, Thaut et al. [27]
found significant improvements in step length symmetry and gait speed, although
a correlation between the two was not tested. The significance of these conflicting
results will be explored in the following section.

4 Should Interlimb Coordination Be Corrected?

Although improving both velocity and symmetry are common goals in


rehabilitation, studies that have examined the relationship between the two have
often reported conflicting findings. While Roth et al. [42] found no relationship
between temporal symmetry and gait velocity in people with hemiparetic gait,
Brandstater [9] and Patterson et al. [21] found that preferred velocity was
negatively associated with temporal asymmetry. Patterson et al. [21] also reported
that spatial asymmetry was not related to gait velocity, but Balasubramanian et al.
[13] noted a negative correlation between the two (albeit a weak one: r = -0.35).
Balasubramanian et al. [13] and Bowden et al. [16] have recently argued that
asymmetries in propulsive forces generated by each leg are correlated with
hemiparetic severity and step length asymmetry, but there was little support for a
direct relationship between asymmetric propulsive forces and gait speed.
Interestingly, Patterson et al. [43] found that gait velocity continues to improve in
the months and years following a stroke, but gait symmetry (temporal and spatial)
worsens over this same timeline. Brower et al. [44] also reported the surprising
finding that people with stroke are kinematically more symmetric while walking
on a treadmill compared to over the ground, but the metabolic cost was also
increased during the (more symmetric) treadmill walking. Overall, these studies
indicate that the relationship between gait symmetry and gait function remains
unclear.
It is possible that gait symmetry may still be advantageous, even if its
relationship with gait speed (and possibly efficiency) is unclear [5]. For instance,
asymmetric gait may contribute to musculoskeletal problems in the nonparetic leg.
Since temporal asymmetry is correlated with increased vertical ground reaction
forces on the nonparetic leg [15], the resultant increased and repetitive loading of
this limb may lead to pain and joint degeneration [18, 20]. While this relationship
has not been investigated in the stroke population, there have been reports of joint
pain and degeneration in the intact limb of amputees who walk asymmetrically
Improving Interlimb Coordination Following Stroke 199

[45, 46]. Balance may also be related to gait asymmetry, although the nature of
this relationship (causal, correlational) is not clear [5, 47, 48]. Finally, it should be
recognized that improving the appearance of gait is a priority for many stroke
survivors – they want to walk without looking like they are limping [1]. In
summary, there are good arguments both for and against improving gait symmetry
which should be systematically evaluated in order to develop effective
rehabilitation treatments that maximize functional mobility gains post-stroke.

Acknowledgment. E.V. Vasudevan was supported in part by the American Heart


Association (Grant ID: 12SDG12200001).

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Exoskeletons Supporting Postural Balance –
The BALANCE Project

Jan F. Veneman

Tecnalia Research and Innovation, Tecnalia M1, Health Division - Rehabilitation,


Paseo Mikeletegi 1, E-20009 San Sebastian, Spain
and Coordinator of the EU FP7 Project BALANCE
{jan.veneman,balance}@tecnalia.com

Abstract. Lower extremity exoskeleton robots have become an established


technology, especially in the field of gait rehabilitation training. However, none of
the devices available on the market use the exoskeleton itself to support postural
balance. On the contrary, all need additional supports as crutches or overhead
supports, or need the user perform the balance control. The target of the
BALANCE research project is to explore and implement the possibility to use the
exoskeleton itself to support postural balance and prevent falls during walking.
The main challenges and initial progress of this project are described in this
abstract.

1 Introduction

Lower extremity exoskeletons have become an established technology. Nowadays


they can be bought from different companies around the world, such as the
autonomous exoskeletons eLegs from Eksobionics (eksobionics.com), HAL from
Cyberdyne Inc. (www.cyberdyne.jp) and Indego from Parker (indigo.parker.com),
or treadmill based exoskeleton system such as the Lokomat from Hocoma
(www.hocoma.com). The features and pricing of these devices are such that they
are mostly only suitable for providing gait training in clinical rehabilitation.
In the future, applications of leg exoskeletons are foreseen as assistive device in
the all-day living environment or as support for workers or soldiers that perform
strenuous tasks. For such applications a number of issues have to be resolved for
exoskeletons to become a feasible technology. Important issues being: cost, range
of use (battery life, energy use), size/bulkiness, cooperative control, meaning the
ability to function efficiently together with a (partially) functional person, and
finally safety, mainly in the sense of avoiding falls [1, 2].
In all current exoskeletons the devices provide or support the essential
movements of the stance and swing leg that contribute to progression of the body
during walking, but they do not provide or support the adequate behavior of the
legs as is needed to maintain postural stability. This means that such exoskeletons
can only be used safely by healthy users that can take care of maintaining their

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 203
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_38, © Springer International Publishing Switzerland 2014
204 J.F. Veneman

postural balance themselves, or they have to be used in combination with crutches,


walkers, or overhead supports in cases where the user is not able to maintain
postural balance.
The EU FP7 project BALANCE aims at supporting the function of maintaining
postural balance directly through the leg exoskeleton, in such a way that the
exoskeleton cooperates with its user in a natural way. In the project the acronym
BALANCE stands for Balance Augmentation in Locomotion, through Anticipative,
Natural and Cooperative control of Exoskeletons. The project focuses on
understanding the fundamental strategies that humans use for postural control and
implementing similar strategies in the control of the exoskeleton, assuming this will
also support implementation of human-robot cooperative control.

2 Challenges in BALANCE

On the road to realizing active support of postural balance as integrated exoskeleton


function lie many challenges. The main challenges addressed in the BALANCE
project are:
• Improve understanding of how humans realize a robust postural balance
control during functional standing and functional walking.
• Develop controller algorithms that robustly implement human-like postural
stability supporting strategies.
• Realize a sense of balance that allows to assess the postural balance during
functional standing and walking, and allows to trigger proper (re-)actions
• Develop strategies for human-cooperative robot control, as in the typical
situation the user will have remaining or full functionality and needs to
cooperate with the robot
• Create an exoskeleton that has adequate features in order to be able to
demonstrate the postural stability support.
• Develop strategies to evaluate the performance of the exoskeleton on these
tasks, including evaluation scenarios and adequate safety measures.
The term ‘functional walking’ is used to distinguish walking as it takes place in
real life, from ‘walking’, taken as ‘constant-speed straight walking on flat ground’.
Functional walking includes many additional gait tasks, such as gait initiation and
termination, turning, avoiding obstacles, stepping up or down height differences,
and dual tasks, - for example walking while lifting an object.
The focus in addressing these challenges is controlling the postural stability
based on sensing of kinematic and kinetic parameters on human and exoskeleton
and actuating the principal degrees of freedom involved in the leg function. This
implies some limitations, for example that the project will not emphasize the task
of automated understanding environmental conditions, which are also important for
adaptation of postural control strategies.
In the first year of the project, these challenges listed above, have all been
initially addressed in parallel, and the first steps are described in this paper.
Exoskeletons Supporting Postural Balance – The BALANCE Project 205

3 Progress of BALANCE

The most important progress highlights of the first year of the BALANCE project
are described in this section.
A) Based on an analysis of measurements on corrective stepping in humans
(motion profiles of leg joints), and on general requirements to control foot
placement, we derived the basic specifications for the exoskeleton. The chosen
specifications are shown in figure 1.

Fig. 1 Degrees of Freedom of the exoskeleton specified for BALANCE, together with the
technical specifications of the joints

The exoskeleton will have four actuated joints per leg, and four passive joints, to
allow functional walking and to be able to support essential strategies in balance
support, such as adequate foot placement.
B) Experiments to study human reactions to perturbations during walking are
currently being prepared and initiated. For these experiments advanced testing
environments are required, for example tilting, rotating, or fast accelerating
walking surfaces, or additional devices to perturb humans walking on a treadmill
or over ground. The main focus is on ankle- and foot placement strategies, but also
the stiffness adaptation of the leg is being considered.
C) As human modelling environment we have selected to build on the SLIP
(spring-loaded inverted pendulum) modelling approach, starting with a highly
simplified 2D model and from there adding the elements needed to adequately
describe the experimental results (a more complex SLIP model example shown in
figure 2.)
206 J.F. Veneman

Fig. 2 Schematic drawing of an example SLIP model, including trunk segment. VPP is the
‘virtual pivot point’, a virtual point in which the GRF vectors intersect [3].

D) To develop the ‘sense of balance’ we are studying the approaches used in


bipedal robot control and in biomechanics, and translating them for use in
BALANCE. We classified methods in “Instantaneous” and “Retrospective”,
where the first can be used in online control to detect the onset of a fall, and the
second to evaluate performance over a number of strides. Most of the existing
methods only are valid during a specified continuous task, or at least require
information about the actual environment and task carried out. For implementing
these sensing approaches on the exoskeleton we are developing methods to track
the Center of Pressure (CoP) and total body Center of Mass (CoM) of the human
wearing the exoskeleton in real time, as these two virtual points are essential for
describing the postural balance situation.
E) For the interaction control, we are studying the use of head motions to
achieve an intuitive control of turning with the exoskeleton, based on anticipative
head motions that humans normally apply when turning. Also, we are
implementing a rigid body model of human and exoskeleton, which will provide
the environment for the project to develop robust balancing control algorithms.
These algorithms will initially be tested on the legged, hydraulically actuated HyQ
robot (figure 3).
Finally, for evaluation of the postural balancing performance of the exoskeleton
we developed a “motion catalogue” that classifies a number of typical ‘actions’
meaning specifics tasks, carried out in a specific environment or under specific
environmental conditions, with an increasing difficulty. These actions were
collected from:
• Descriptions of real life use cases that were defined for the exoskeleton
(rehabilitation training, assistive device, worker support), which describe
which typical actions can be expected to be performed with an exoskeleton if
used in these specific application.
• Procedures as are defined in the BESTest postural balance clinical
assessment procedure [4].
Exoskeletons Supporting Postural Balance – The BALANCE Project 207

Fig. 3 The quadruped robot HyQ Blue, which will be used for first evaluation of control
algorithms

From this “library” of relevant actions we are selecting a more limited


evaluation scenario that defines a number of tasks and environments, that will be
used for project result evalution. In these tasks the performance of the human
wearing the exoskeleton will be assessed through different metrics, for example
the balance-sensing methods mentioned above under IIID. (figure 4).

Evaluation
actions:

Tasks

Environ-
ment
ments

Metrics
Met
triics

Fig. 4 Structure of the development of an evaluation process for an exoskeleton. The three
horizontal lines describe three inputs to the proposed evaluation structure: a motion
catalogue with specific tasks carried out in specific environments is formulated, based on
functional requirements derived from use cases. Additional items are added to the motion
catalogue adapted from clinical assessment procedures found in the BESTest method. Then
exeskeletong performance in these selected motions will be assessed through suitable
metrics that somehow quantify postural balancing behaviour. For these metrics we adapt
methods defined for implementing the “sense of balance’ in the project.

Acknowledgment. This work is supported by the partially EU funded project BALANCE,


FP7-ICT-2011.2.1 grant no. 601003; www.balance-fp7.eu.
208 J.F. Veneman

References
[1] Dollar, A., Herr, H.: Lower extremity exoskeletons and active orthoses: Challenges
and state-of-the-art. IEEE Transactions on Robotics 24(1), 144–158 (2008)
[2] Herr, H.: Exoskeletons and orthoses: classification, design challenges and future
directions. Journal of NeuroEngineering and Rehabilitation (6) (2009)
[3] Maus, H.-M., Lipfert, S.W., Gross, M., Rummel, J., Seyfarth, A.: Upright human gait
did not provide a major mechanical challenge for our ancestors. Nat. Commun. 1, 70
(2010)
[4] Horak, F.B., Wrisley, D.M., Frank, J.: The balance evaluation systems test (BESTest)
to differentiate balance deficits. Physical Therapy 89(5), 484–498 (2009)
Spinal Reflex Conditioning: Mechanisms
and Implications

Jonathan R. Wolpaw

Wadsworth Center of the New York State Department of Health,


Albany, NY 12201 USA
and
Department of Biomedical Sciences, State University of New York,
Albany, NY 12222
and
Department of Neurology, Neurological Institute,
Columbia University, New York, NY 10032 USA
wolpaw@wadsworth.org

Abstract. Operant conditioning protocols that induce and maintain specific


descending influence over spinal cord reflex pathways can gradually change these
reflexes. These protocols create a complex hierarchy of plasticity in which
plasticity in the brain induces and maintains the plasticity in the spinal cord that
directly underlies reflex change. Thus, they provide a powerful model for studying
the substrates of motor learning. In addition, because spinal cord reflexes
contribute to behaviors such as locomotion, and because abnormalities in these
reflexes often contribute to the motor impairments caused by spinal cord injury
and other disorders, operant conditioning protocols provide a promising new
therapeutic approach to improving recovery. In both animals and humans with
incomplete spinal cord injuries, an appropriately selected operant conditioning
protocol can restore more normal locomotion.

Keywords: spinal cord, H-reflex, plasticity, motor learning, rehabilitation.

1 Introduction
Spinal cord reflexes are produced by CNS pathways that lie within the spinal cord.
While these pathways are wholly spinal, they are influenced by descending
activity from the brain. Via descending tracts, the brain exerts both short-term and
long-term influence over these pathways. In the short-term, the brain adjusts them
according to the requirements of different behaviors (e.g., standing or walking or
running). In the long-term, it gradually shapes spinal reflex pathways in early
development, during skill acquisition throughout life, and in reaction to trauma or
disease. These long-term changes include plasticity in the spinal cord itself as well
as in the brain.
Because the spinal cord is the simplest and most accessible region in the
mammalian CNS, spinal cord reflexes, the brain’s control of them, and the spinal

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 209
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_39, © Springer International Publishing Switzerland 2014
210 J.R. Wolpaw

cord plasticity this control produces are the basis for a unique and valuable
experimental model for the mechanisms and substrates of learning and memory.
By rewarding a subject (i.e., monkey, rat, mouse, or human) for a larger or smaller
reflex, an operant conditioning protocol induces the subject to maintain
descending activity appropriate to the reward criterion (i.e., descending activity
that increases or decreases reflex size). As a laboratory equivalent of the brain’s
long-term shaping of spinal reflexes during life, the long-term maintenance of this
appropriate descending activity induces plasticity in the spinal reflex pathway that
changes reflex size appropriately. In terms of a standard definition of a skill as an
adaptive behavior acquired through practice, the larger or smaller reflex is a
simple motor skill; and the plasticity directly underlying it is in the spinal cord
where it is accessible to detailed study.
A long series of studies with this model has yielded new insights into the
complicated spinal and supraspinal plasticity that underlies acquisition and
maintenance of a simple motor skill. In addition, the model is the basis for a
promising new therapeutic approach to improving impaired motor function after
trauma or disease. These studies have focused on operant conditioning of the
simplest spinal reflex, the spinal stretch reflex (SSR), and its electrical analog, the
H-reflex. These reflexes are produced primarily by a two-neuron monosynaptic
pathway comprised of the primary afferent fiber from the muscle spindle, its
synapse on the spinal motoneuron, and the motoneuron. In the SSR, muscle
stretch excites the afferent; in the H-reflex, electrical stimulation of the nerve
excites it. The following sections briefly review the major results of these studies.
More detailed recent reviews are available (Wolpaw, 2010; Thompson and
Wolpaw, 2014a &b).

2 The Operant Conditioning Protocol and Its Results


Figure 1 illustrates the operant conditioning protocol and its results in rats and
humans. Because the H-reflex is the earliest CNS response to the nerve excitation,
the subject can change H-reflex size only by maintaining appropriate descending
influence over the spinal pathway of the reflex. This continued descending
influence gradually induces activity-dependent plasticity in the spinal cord that
underlies H-reflex change.
The central finding is that the up- or down-conditioning mode changes reflex
size appropriately over days and weeks. The reflex changes in two phases, a small
rapid phase-1 change in the first few hours or days, and a far slower phase-2
change that progresses over weeks (Wolpaw and O’Keefe, 1984; Thompson et al.
2013 for review). Phase 1 is thought to reflect rapid appropriate change in
descending influence over the reflex pathway. This change in descending
influence is operantly conditioned by the reward criterion. In contrast, phase 2 is
thought to reflect gradual spinal cord plasticity induced by the long-term
persistence of the descending influence. The spinal cord plasticity survives for
some days after all descending influence is removed, indicating that the
conditioning modifies the spinal cord itself (Wolpaw and Lee, 1989).
Spinal Reflex Conditioning: Mechanisms and Implications 211

Fig. 1 The H-reflex operant conditioning model and its results in rats (A) and humans (B)

A, Left: Soleus EMG is monitored 24hr/d in a rat with implanted EMG electrodes and a
tibial nerve cuff. The wires travel subcutaneously to a head-mounted connector and
through a flexible cable and a commutator to amplifiers and stimulator. The rat can move
freely about the cage. Whenever the absolute (i.e., rectified) value of soleus EMG activity
stays in a specific range for a randomly varying 2.3-2.7 s period, a nerve cuff stimulus
elicits a threshold M wave (i.e., a direct muscle response) and an H-reflex. The trace shows
one trial. A rat averages 2,000-6,000 trials/day.
A, Middle: For the first 10 days (Day -10 to Day 0), the rat is exposed to the control mode,
in which no reward occurs and the H-reflex is simply measured to define its initial size.
For the next 50 days, it is exposed to the up-conditioning or down-conditioning mode, in
which a food-pellet reward occurs whenever the H-reflex is above (HRup mode) or below
(HRdown mode) a criterion value. Background EMG and M wave stay constant
throughout. Successful conditioning (i.e., change ≥20% in the correct direction) occurs in
75-80% of the rats (the others remain within 20% of initial value). The graphs show
average (±SE) daily H-reflex sizes for 55 successful HRup rats (purple !) and 72 successful
HRdown rats (blue ˝). In both groups, mode-appropriate H-reflex change develops steadily
over the 50 days. If a rat is switched from the up-mode to the down-mode (or vice versa),
the H-reflex change reverses in the same gradual fashion.
A, right: Average post-stimulus EMG (absol value) for a day from an HRup rat (left) and an
HRdown rat (right) in control mode (solid) and at the end of conditioning (dashed). The H-
reflex is larger after up-conditioning and smaller after down-conditioning. Background
EMG (shown here by EMG at time zero) and M waves are not changed.
B, Left: Soleus EMG is monitored in a person with EMG electrodes over the muscle and
tibial nerve-stimulating electrodes in the popliteal fossa. The person stands facing a screen
showing the current level (absolute value) of soleus EMG versus a specified range.
Whenever EMG stays in the range for several sec, stimulation elicits a threshold M wave
and an H-reflex. The trace is one trial (with EMG as actual value).
212 J.R. Wolpaw

B, Middle: A person completes three 225-trial sessions/week. For the first 6 (Day -14 to
Day 0), the person is exposed to the control mode, in which the H-reflex is simply
measured to define its initial size. For the next 24 (Days 0-56), the person is exposed to the
HRup or HRdown mode, in which the screen gives immediate feedback after each trial
indicating whether the H-reflex was above (HRup mode) or below (HRdown mode) a
criterion value. After these 24 conditioning sessions, people return for 4 follow-up sessions
over the next 3 months. Background EMG and M wave are constant throughout. Successful
conditioning occurs in ~80% of the people. The graphs show average (±SEM) daily H-
reflex sizes for 6 successful HRup (purple !) and 8 successful HRdown (blue ˝) people. In
both groups, mode-appropriate H reflex change develops steadily over the 24 conditioning
sessions. In the follow-up sessions, the H-reflex increase in the HRup group is smaller but
still evident, and the H-reflex decrease in the HRdown group persists unchanged.
B, Right: Average post-stimulus EMG for a session from an HRup person (left) and an
HRdown person (right) in control mode (solid) and at the end of conditioning (dashed). The
H-reflex is larger after up-conditioning and smaller after down-conditioning. Background
EMG and M waves do not change. (Stimulus artifacts are evident at 0 ms.) (Modified from
Wolpaw, 2010.)

3 Reflex Conditioning Produces a Hierarchy of Brain


and Spinal Cord Plasticity
A series of investigations have begun to reveal the spinal cord plasticity associated
with conditioning and the role of the brain in producing and maintaining this
plasticity. Intracellular studies in monkeys and rats showed that down-conditioning
changes motoneuron firing threshold and reduces axonal conduction velocity (Carp
and Wolpaw, 1994; Carp et al., 2001a&b). The positive threshold shift, and a small
decrease in the primary afferent EPSP, largely accounts for the smaller H-reflex
(Halter et al., 1995). A modification in motoneuron sodium channels is the
probable etiology of the positive threshold shift and the lower conduction
velocity (Halter et al., 1995; Wang et al., 2013). Electromicroscopic and
immunohistochemical explorations identified changes in several synaptic
populations on the motoneuron (Feng-Chen and Wolpaw, 1996; Wang et al., 2006;
Pillai et al., 2008). Especially prominent is a large increase in the number of
identifiable GABAergic terminals with down-conditioning (Wang et al., 2006).
This is accompanied by a large increase in the number of identifiable GABAergic
interneurons in the ventral horn (Wang et al., 2009). In addition, physiological
studies detected modification in di- or tri-synaptic pathways that contribute to the
H-reflex, specifically in up-conditioning (Wolpaw and Chen, 2001), and also
detected changes on motor unit type (Carp et al., 2001b). Reflex conditioning even
changed the contralateral spinal cord (Wolpaw and Lee, 1989).
In sum, H-reflex conditioning is associated with complex multi-site plasticity in
the spinal cord. Although some of these changes (e.g., the positive threshold shift
with down-conditioning) are likely to account for the H-reflex change (i.e., primary
plasticity (Wolpaw, 1997 & 2010)), others appear to be unrelated (e.g., the change
Spinal Reflex Conditioning: Mechanisms and Implications 213

Fig. 2 A hierarchy of brain and spinal cord plasticity underlies H-reflex conditioning. The
shaded ovals indicate the spinal and supraspinal sites of definite or probable plasticity
associated with operant conditioning of the H-reflex. "MN" is the motoneuron, “CST” is
the main corticospinal tract, "IN" is a spinal interneuron, and “GABA IN” is a GABAergic
spinal interneuron. Dashed pathways imply the possibility of intervening spinal
interneurons. The monosynaptic and probably oligosynaptic H-reflex pathway from groups
Ia, II, and Ib afferents to the motoneuron is shown. Definite (dark gray) or probable (light
gray) sites of plasticity include: the motoneuron membrane (i.e., firing threshold and axonal
conduction velocity); motor unit properties; GABAergic interneurons; GABAergic
terminals and C terminals on the motoneuron; the Ia afferent synaptic connection; terminals
conveying oligosynaptic groups I and II inhibition or excitation to the motoneuron;
sensorimotor cortex; and cerebellum. As described in the text, the data suggest that the
reward contingency acts through the inferior olive to guide and maintain plasticity in the
cerebellum that guides and maintains plasticity in sensorimotor cortex that (via the CST)
guides and maintains plasticity in the spinal cord that is directly responsible for H-reflex
change. (Modified from Wolpaw, 2010.)
214 J.R. Wolpaw

in the contralateral spinal cord ((Wolpaw and Lee, 1989)). These latter changes
probably represent compensatory plasticity that preserves other behaviors affected
by the change in the H-reflex pathway, or reactive (i.e., downstream) plasticity
caused by the changes in ongoing CNS activity caused by primary and
compensatory plasticity (Wolpaw, 1997 & 2010).
A series of tract and areal lesion studies established that H-reflex conditioning
requires the corticospinal tract (CST) and sensorimotor cortex, but does not
require other major descending or ascending spinal cord pathways (Chen et al.,
2002; Chen and Wolpaw, 2002; Chen et al., 2006a; Chen et al., 2006b). The
cerebellum and the inferior olive are needed, at least for down-conditioning (Chen
and Wolpaw, 2005; Wolpaw and Chen, 2006; Chen et al., 2012). Since the
rubrospinal tract is not essential, cerebellar output to cortex seems to be the
cerebellum’s essential contribution (Chen and Wolpaw, 2005; Wolpaw and Chen,
2006). The impacts of specific lesions after down-conditioning has already
occurred show that plasticity in sensorimotor cortex (or in closely related areas) is
needed for the persistence (beyond 5-10 days) of the spinal cord plasticity that
directly underlies H-reflex change (Chen et al., 2006a; Chen et al., 2006b), that the
cerebellum is needed for long-term maintenance (beyond 40 days) of this cortical
plasticity (Chen and Wolpaw, 2005; Wolpaw and Chen, 2006), and that the
cerebellum’s role is likely to depend on cerebellar plasticity that is induced and
preserved by climbing fiber input from the inferior olive (Chen et al., 2012).
Together, these studies indicate that H-reflex conditioning creates a hierarchy of
plasticity (i.e., Figure 2): the reward criterion induces plasticity in the brain that
guides and maintains spinal cord plasticity that directly underlies the H-reflex
change (Wolpaw, 2010). Figure 2 summarizes current understanding of the
hierarchy of brain and spinal cord plasticity that is responsible H-reflex
conditioning.

4 Comparable Plasticity Occurs Throughout Life

The complex spinal plasticity that accompanies H-reflex conditioning is not


merely a laboratory phenomenon. Gradual activity-dependent plasticity, induced
and guided by inputs from the brain and the periphery, shapes spinal function in
development and modifies it throughout subsequent life. In the normal CNS, this
plasticity ensures that spinal cord pathways enable effective motor behaviors
(reviewed in Wolpaw and Tennissen, 2002; Wolpaw, 2010; Thompson and
Wolpaw, 2014a &b).
During the initial years of life, the brain induces spinal cord plasticity that leads
to an adult spinal cord that has normal reflexes, enables standard behaviors such as
locomotion, and can also support specialized behaviors such as dancing. When
perinatal supraspinal damage (e.g., cerebral palsy) distorts this descending input,
infantile reflex patterns may persist into adulthood and impair motor control.
The acquisition of motor skills later in life is associated with spinal reflex
changes similar to those created in the laboratory. These reflexes are affected by
Spinal Reflex Conditioning: Mechanisms and Implications 215

the nature, intensity, and duration of past physical activity and by particular
training regimens. SSRs and H-reflexes differ between athletes and non-athletes,
and among different kinds of athletes. These differences are likely to contribute to
the differing skills of these different groups. Thus, H-reflexes and disynaptic
reciprocal inhibition in the leg are unusually small in highly trained ballet dancers
(Nielsen et al., 1993). These reductions may underlie the capacity for muscle
cocontraction that is important in this form of dance. Reflex changes that occur
with aging are additional evidence of spinal cord plasticity (Koceja et al., 1995).
These changes in reflex size and task-dependent modulation probably reflect both
direct and indirect effects of aging (i.e., direct effects of aging on the reflex
pathway and indirect effects of aging that result from its effects elsewhere in the
CNS or on the peripheral sensory and motor apparatus of movement).

5 Potential Therapeutic Uses of Spinal Reflex Conditioning

Spinal reflex abnormalities contribute to the motor impairments caused by spinal


cord injuries and other neuromuscular disorders. Because the sites and
mechanisms of these abnormalities differ across individuals and disorders, new
methods, such as H-reflex conditioning, that can strengthen or weaken a specific
pathway according to the nature of the impairment could complement other
therapeutic methods (e.g., locomotor training) and augment recovery of function.
Indeed, H-reflex conditioning can improve locomotion in rats with an
incomplete spinal cord injury (Chen et al. 2006a). Mid-thoracic transection of the
right lateral column (which leaves the CST intact) results in a persistent locomotor
asymmetry; the right stance phase is shorter than the left. H-reflex up-
conditioning, which increases the right soleus burst, eliminates this asymmetry.
These animal data suggest that reflex conditioning protocols might improve motor
function in people with partial spinal cord injuries. In the next talk, Dr. Thompson
with describe her exciting new studies that confirm this possibility (Thompson et
al, 2013). Spinal reflex conditioning protocols could be particularly useful when
regeneration becomes practical and precise techniques for retraining the
regenerated spinal cord are needed to restore useful function.

Acknowledgments. Work in the author’s laboratory has been supported by NIH (NS22189
(JRW), NS061823 (XY Chen & JRW), HD36020 (XY Chen), & HD32571 (AW English)).

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Carp, J.S., Chen, X.Y., Sheikh, H., Wolpaw, J.R.: Motor unit properties after operant
conditioning of rat H-reflex. Exp. Brain Res. 140, 382–386 (2001b)
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ablation prevents acquisition and long-term maintenance of soleus H-reflex down-
conditioning in rats. In: Society for Neuroscience 42nd Annual Meeting, Program No.
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Chen, X.Y., Wolpaw, J.R.: Probable corticospinal tract control of spinal cord plasticity in
the rat. J. Neurophysiol. 87, 645–652 (2002)
Chen, X.Y., Wolpaw, J.R.: Ablation of cerebellar nuclei prevents H-reflex down-
conditioning in rats. Learn Mem. 12, 248–254 (2005)
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Neuromechanical Interlimb Interactions
and Rehabilitation of Walking after Stroke

E. Paul Zehr1,2, Trevor S. Barss1,2, Chelsea Kaupp1,2, Taryn Klarner1,2,


Rinaldo A. Mezzarane3, Tsuyoshi Nakajima4, Yao Sun1,2,
and Tomoyoshi Komiyama5
1
Centre for Biomedical Research, Rehabilitation Neuroscience Laboratory,
School of Exercise Science, Physical, and Health Education,
and Division of Medical Sciences at the University of Victoria
Victoria, Canada
pzehr@uvic.ca www.zehr.ca
2
ICORD, Vancouver, BC, Canada
3
University of Brasilia, Brazil
4
Kyorin University, Japan
5
Chiba University, Japan

Abstract. Bipedal humans operate using elements of quadrupedal neuronal limb


control during locomotion. This has significant implications for supporting
transfer of the huge body of quadrupedal animal literature to human rehabilitation.
In particular, this has translational applications for neurological rehabilitation after
stroke where interlimb coordination is compromised. The data supports including
arm activity in addition to leg activity as a component of gait retraining after
stroke. An additional component is to consider strength training of the less
affected limb to improve motor output of the more affected limb when that limb is
too weak to be initially incorporated in functional rehabilitation. The major
concept is to use activity related to the less affected limbs to modulate output of
the more affected limbs after stroke. A key example is to incorporate arm activity
into rehabilitation of leg motion in stepping after stroke.

1 Introduction

Cerebrovascular accident, or stroke, presents a typical hemiparesis producing


more (MA) and less (LA) affected sides. A focus in walking retraining is
addressing major deficits experienced in the MA leg to restore the sublime
interaction of descending inputs, spinal cord mechanisms, and somatosensory
feedback. Related efforts attempt to modify the activity in the MA limb by therapy
and direct training. The perspective in this paper is to highlight complimentary
efforts that access interlimb neural circuits. That is, influencing the MA limb by
using pathways from the LA side, or by using the arms to access the legs.
The thesis here is that interlimb circuits can be recruited into locomotor
networks through targeted training after stroke. The focus here is to highlight the

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 219
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_40, © Springer International Publishing Switzerland 2014
220 E.P. Zehr et al.

persistence after stroke of: 1) locomotor-activated and somatosensory linkages


between the arms and legs; and, 2) improvements in bilateral strength by training
of one limb only.

2 Persistent Somatosensory and Locomotor-Activated


Linkages between the Arms and Legs after Stroke

In quadrupeds, forelimb-hindlimb coordination is mediated by neuronal linkage


between lumbosacral and cervical spinal central pattern generating (CPG)
locomotor control networks [1-3]. It is likely that bipedal human locomotion is
built upon elements of quadrupedal interlimb coordination [3, 4]. Examples include
modulated H-reflex amplitudes in stationary legs during locomotor-related
rhythmic arm cycling [2, 5, 6]. During walking, interlimb reflexes in both the arms
and legs following stimulation of cutaneous nerves in the hand and foot are
modulated in a way suggestive of coupling between segmental spinal networks
regulating human limb motion [7]. Also, reflex modulation in the legs during
combined rhythmic arm and leg movement is sensitive to contributions from the
arms [8] and there is specific tuning of this coupling at the level of the
motoneuronal pool [9]. There is also a strong reciprocal organization such that
rhythmic leg movement modulates cervical spinal cord excitability [10-14].
Although there are modifications in locomotor phasing [15, 16], portions of
interlimb communication between CPG elements for the legs are maintained after
stroke [17, 18]. These reciprocally organized bilateral pathways between the legs
could be functionally relevant during locomotion, based on the observation that
contralateral leg cycling could induce a coordinated pattern in both legs [18]. There
is a preservation of activity in circuitry contributing to rhythmic arm movement
after stroke [19]. Rhythmic modulation of background EMG patterns were found in
both the LA and MA arms after stroke, with a “blunted” pattern compared to
control. Despite the observation that cutaneous reflex (superficial radial (SR) n.)
amplitudes were altered after stroke compared to control participants, reflexes
remained phase-modulated in some muscles of both the MA and the LA arms. This
suggested that reflex patterns are partially retained even in the MA limb during
rhythmic arm cycling after stroke.
During rhythmic arm cycling, changes in lumbosacral reflex excitability (as
measured by H-reflex modulation) were also found in participants with
hyperreflexia after stroke [20]. This effect was generally similar, but somewhat
weaker, than that observed in age-matched controls. Importantly this results
confirms residual access to interlimb pathways linking rhythmic arm and leg
activity after stroke.
Interlimb networks of cutaneous reflexes also remain active during gait after
stroke [21]. Interlimb cutaneous reflex pathways from the LA hand (SR n.) and foot
(superficial peroneal n.) remain viable and modulated during walking after stroke
[21], a result complimentary to observations within the MA leg [22]. Interestingly,
there is a potential enhancement in transmission from LA arm to MA leg as
Neuromechanical Interlimb Interactions and Rehabilitation of Walking after Stroke 221

compared to control participants. This suggests that the somatosensory linkages


remain active (and possibly potentiated) and that the rhythm generating CPG
circuits remain accessible after stroke.
The schematic in Figure 1 illustrates the issue of arm and leg interactions during
rhythmic movement schematically where the relative strength of coupling effects
(thicker lines = stronger coupling) between neuromechanical locomotor controllers
for each limb (drawn as yin/yang images) are shown. There is considerable
evidence that the legs are strongly coupled (thick arrow between legs) and that the
arms are much more weakly coupled (thin arrow between arms) [1, 3, 23]. It is also
known that there is a relation between the arms and legs (see thick descending
vertical grey arrow). The exact details of the nature and strength of arm to leg
coupling between the MA and LA limbs after stroke remain to be fully elucidated.

3 Strengthening Motor Circuits on the More Affected Side


after Stroke with High Intensity Resistance Training of the
Opposite Side
Following stroke, weakness of leg flexor and arm extensor muscles is commonly
combined with excessive antagonist muscle activity presenting as hyper-excitable
reflex pathways [24-27]. This leads to reduced movement at a given joint and
decreased ability to generate purposeful torques and move the arm functionally
[25, 28-30]. There is a particular dysfunction in reciprocal inhibition between
functional antagonists [31].
Short-term, high intensity resistance training on one side of the body causes a
“crossed” strength gain in the untrained limb [32-35]. This phenomenon was
initially described over 125 years ago by Scripture and colleagues (1894) and
named “cross education”. Unilateral plantarflexion [36] or dorsiflexion [37]
resistance training produces bilateral strength gains in neurologically intact
participants. These changes in strength can be associated with changes in muscle
activation and reflex excitability [38].
Resistance training improves muscular strength and functional ability in post-
stroke hemiparesis without deleterious results [38, 39], including functional re-
learning to improve arm movement [40]. Unfortunately, implementation of motor
re-training may be compromised for those in critical need, namely, those with
significant post-stroke hemiparesis. In this group, substantial weakness in the MA
limb may prevent sufficient activation to gain a training effect [41].
The efficacy of cross-education training was assessed in 19 participants with
chronic post-stroke hemiparesis who performed high-intensity maximal isometric
dorsiflexion resistance training (5 sets of 5 maximal 2 s voluntary contractions 3
times/wk for 6 wks) of the LA leg [42]. Voluntary dorsiflexion strength in the LA
leg increased by ~40%. In addition, the untrained, MA leg showed an ~30 %
increase in strength and muscle activation was significantly increased bilaterally.
Incredibly, 4 participants who were unable to generate measurable dorsiflexion
torque in the MA leg before training were able to meaningfully activate the
untrained dorsiflexors after the intervention.
222 E.P. Zehr et al.

Fig. 1 Interlimb locomotor linkages after stroke

This study showed that significant gains in voluntary strength and muscle
activation in the untrained MA leg can be achieved by training the opposite, LA
limb after stroke. This demonstrates the residual plasticity that exists post-stroke
and is a significant step toward post-stroke rehabilitation, specifically in cases of
severe hemiparesis where training the MA limb is not initially possible [43]. The
general overview of this approach is shown in Figure 2 (adapted from 43).

4 Summary

Taken together, the observations cited here support integrating rhythmic arm
movement paradigms and strength training with locomotor rehabilitation after
stroke in humans. Ferris et al. [44] argued that gait rehabilitation therapy should
incorporate simultaneous arm and leg rhythmic activity to harness interlimb neural
coupling after neurotrauma. Combining these approaches with protocols that could
“boost” the ability to recruit targeted motor output on the MA side could be of
benefit in post-stroke locomotor rehabilitation.
Neuromechanical Interlimb Interactions and Rehabilitation of Walking after Stroke 223

Fig. 2 Cross-education of strength after stroke

Acknowledgment. This work was supported by grants from the Heart and Stroke
Foundation of Canada (BC & Yukon).

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Feature and Channel Selection Using
Correlation Based Method for Hand Posture
Classification in Multiple Arm Positions*

Haitham M. Al-Angari, Gunter Kanitz, Sergio Tarantino,


Jacopo Rigosa, and Christian Cipriani

BioRobotics Institute, Scuola Sant’Anna,


56025 Pontedera, (PI) Italy
{h.alangari,g.kanitz,s.tarantino,
j.rigosa,ch.cipriani}@sssup.it

Abstract. In this work we propose a method based on correlation-based feature


selection (CFS) to select features and channels for pattern recognition control of
upper-limb prostheses. This method was applied on features extracted from
myoelectric signals acquired from two able-bodied subjects and one individual
with transradial amputation while contracting the muscles as to perform five
functional hand postures in nine arm positions. The classification accuracy
increased by using CFS for the able-bodied, while no statistical improvements has
been highlighted for the amputee subject. The channels selected by this approach
were mainly placed on the posterior side of the forearm which might reflect
importance role of the extensor muscles over the flexor muscle when performing
these hand postures. Further analysis with bigger dataset will be conducted to
validate these preliminary findings.

1 Introduction

The application of modern pattern recognition techniques to the myoelectric


(EMG) signals used to control multi-degrees of freedom prosthetic limbs is very
promising, as it holds the potential to allow seamless control to the user. To this
aim, several combinations of features of the EMG signal and classification
algorithms have been investigated so far, few of them demonstrating high
classification accuracies in the lab [1-5]. Nevertheless, pattern recognition systems
do not exhibit sufficient robustness in order to be used outside the lab. For this
reason, commercial transradial prostheses still use rudimental control algorithms
(proportional control and finite state machines). The lack of robustness is due to

*
This work was supported by the European Commission under the WAY project (FP7 -
ICT-288551) and by the Italian Ministry of Education University and Research under the
FIRB-2010 MY-HAND Project [RBFR10VCLD].

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 227
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_41, © Springer International Publishing Switzerland 2014
228 H.M. Al-Angari et al.

many factors, including that arm position and varying loads applied to the
prosthetic socket influence the EMG signals in the forearm and hence its
classification [6-9]. The question of which features (and channels) to use for
optimal classification accuracy has not been fully answered. Optimal features can
be selected using filters or wrappers [10]. Filter approaches typically select
features based on their discriminative power. State of the art methods in this
respect include distance, dependency, information, and consistency measures [11].
Wrappers are statistical techniques that use the actual target learning algorithm
(classifier) to estimate the accuracy of features subsets. Filter methods have good
generalization properties, but may be less effective in reducing the dimensionality
of the feature space while boosting the classification rate. On the other hand,
wrappers have the disadvantage of high computational load, susceptibility to
overtraining, and the fact that their results are not often extendable to other types
of classifier. It thus becomes unpractical to apply a wrapper in order to choose
features from a large data set that contains numerous features.
Different feature selection methods have also been used to evaluate
classification accuracy and the related computational load. Zardoshti-Kermani
used Davies-Bouldin index (DBI) and K-nearest neighbor classifier to select
efficient EMG features for classification [12]. Park and Lee evaluated a set of
EMG features by comparing separability measure provided by the Bhattacharyya
distance, and showed that the adaptive cepstrum vector outperformed all other
examined features [13]. Oskoei et al. employed the DBI as a filter objective
function and the support vector machine (SVM) as a wrapper objective function
and developed a genetic algorithm to select the optimal subset among time-
domain, time-scale, and spectral features [11]. Their results showed a slight
improvement of the SVM performance over the DBI filter. However, all this work
was done while the arm was kept in one static position.
This work presents an algorithm that selects the best combination of features
and channels which can accurately classify hand postures (classes) despite
variations in the arm position. The aim was to have a screening filter that selects
only those EMG channels and features that are robust against arm position
variation. To this aim we used a method based on the correlation-base feature
selection (CFS). The CFS algorithm is a filter that performs a heuristic for
evaluating the worth or merit of a subset of features. This heuristic takes into
account the ability of individual features of predicting the class label along with
the level of inter-correlation among them based on the hypothesis that a good
subset contains features highly correlated with the class yet uncorrelated with each
other. CFS has been proposed in different research fields including computer
networking and gene expression studies where large numbers of features are
usually used [14-15].
Feature and Channel Selection Using Correlation Based Method 229

2 Methods

2.1 The CFS Approach


In information theory, the mutual information: I(Y:X) is defined as the measure
of the mutual dependence between the variables Y and X. Given the entropy of Y:
H(Y), and the entropy of Y conditioned to X: H(Y|X), the mutual information of
X and Y is defined as follows:
I(Y;X )= H(Y) - H(Y|X) (1)
By exploring the mutual information between the desired outcome and the
feature set it is possible to estimate the relevance of each feature with respect of a
specific classification problem [16]. In our application, a bounded estimator of the
mutual information is considered:
;
; (2)

In short, the features selection is then evaluated as follows:


1) For each feature Xi, the SU with the Label C is computed: SU(C;Xi).
2) When SU(C;Xi) > δ (where δ is a predefined threshold), the feature Xi is
inserted in the feature set RXC.
3) The pairwise symmetric uncertainty (SXX) among features of set RXC is
estimated as the summation of SU(Xj;Xk) where j≠k.
4) The means µ R and µ S of SU(C;X) and SXX in set RXC are computed.
5) Every feature Xj that respect the condition (µ S/µ R* SU(C;Xj)-SXX(Xj)> 0) is
considered relevant for the final set.

2.2 Experimental Protocol


Three subjects (two able-bodied and one transradial amputee – myoelectric hand
user) volunteered in this study. Each subject was asked to perform five hand
postures in nine different static positions. Able bodied subjects were asked to
perform the movements using their dominant hand, while the amputee was asked
to perform the tasks simultaneously on both limbs for data acquisition and
supervision. The five hand postures were: Relax, Pinch grip (thumb-index), Power
grasp, Lateral grip, and Open hand (Fig. 1). The nine arm positions were: Normal,
Up, Right, Down, Left, Sky, Earth, Front, and Lateral (Fig. 2). The first five
positions (Fig. 2A) were performed with the shoulder adducted while in the last
four (Fig. 2B) the elbow was fully extended towards one of the four directions. In
the Normal position, the elbow was bent for about 90° while the forearm was kept
parallel to the horizontal plane. Instead, positions Up, Right, Down, and Left were
reached by moving the forearm about 45° from the Normal position towards the
proper direction.
230 H.M. Al-Angari et aal.

m right, the following hand postures: relax, pinch grasp, poweer


Fig. 1 From top left to bottom
grasp, lateral grasp and open
n hand

A B

Fig. 2 Arm positions: A) “NNormal” position and 45° variations (right, up, left and downn);
B) Reaching sky, reach lateral, reach front and reach earth. of a figure caption

All subjects were askeed to hold the grasp for 10 seconds while EMG signaals
were acquired at a contracction level that could be sustained that long. Each subjeect
was then given few minu utes to rest between repetitions. Each grasp was repeateed
three times in each positio
on.
The raw surface EMG G data were collected employing the NoraxonTeleMyyo
2400R (Noraxon, Scottsdale, AZ, USA) through a wireless unit (TeleMyo 2400T T).
Raw data were then acqu uired at a sampling frequency of 1.5 kHz, 1st order 10 H Hz
hardware high-pass filterred, 8th order 500 Hz hardware Butterworth low-pass
filters, amplified with a gain of 1000, digitized with 12 bits, and stored for aan
offline analysis in MatL Lab environment. Seven surface differential electrodees
(Ag–AgCl) were used to record
r the myoelectric activity from the forearm musclees.
For the able bodied subjjects the electrodes were placed forming a ring on thhe
forearm, proximal to the elbow. For the amputee, the electrodes (eight channells)
were placed on the ex xtensor and flexor muscles, proximally and distallly
throughout the forearm (F Fig. 3).
Feature and Channel Selection Using Correlation Based Method 231

A B

Fig. 3 Electrode placement for the able-bodied (A) and the amputee subjects (B)

78.0
76.0
74.0
72.0
SVM Acc %

70.0
68.0
66.0
64.0
62.0
60.0
10 (6) 20(12) 30(18) 40 (28) 50(36)
Top Class-correlated features (% of the original set size)

Fig. 4 SVM performance with top 10-50% class-correlated features for an able bodied
subject. The value between brackets represent actual number of feature after removing the
redudant ones.

The EMG signals were processed using a 250 ms overlapping sliding window
(225ms overlap); seven time-domain and frequency-domain features were extracted
from each window. The features were: mean absolute value (MAV), standard
deviation (SD), mean energy (ME), waveform length (WFL), coefficients of the 6th
order auto-regressive model (AR), energy of a 4-level Wavelet Decomposition
Transform (WDC) evaluated at each level of decomposition, and energy difference
of a 4-level WDC (each window was split into two halves and the difference
between the WDC energy of these halves was computed at each level of
decomposition, WDCDIFF). The WFL in each segment was computed as:
232 H.M. Al-Angari et al.

Fig. 5 Contribution from the seven used features in the selected subset using top 30-50%
class-correlated features (results are for same subject of Fig. 4)

Fig. 6 Contribution from the seven cahnnels in the selected subset using top 30-50% class-
correlated features (results are for same subject of Fig. 4)

∑ | | (3)

where xk is the kth EMG sample in that segment and N is the length of the segment.
The AR coefficients were computed as:

∑ 1 (4)

where ai represents the AR coefficients, p is the AR model order, and ek is the


residual white noise. For WDC, the Daubechies 1 wavelet was selected as the
mother wavelet.
Feature and Channel Selection Using Correlation Based Method 233

Each feature was then normalized in order to have a mean equal to zero and a
variance equal to 1 (z-score transformation). All classifications were done using a
SVM classifier with a radial basis function (RBF) kernel and a penalty parameter
C=1. From previous experience, the RBF kernel showed better performance over
the linear and polynomial kernels, while varying the value of C did not cause
significant improvement in the SVM performance. A cross validation by leave-
one repetition out was applied and the average test accuracy was reported. To
analyse inter-subject variation on the features and channels contributions a 1-way
ANOVA test of variance was applied on the top 20-50% features for the three
subjects.

3 Results

The SVM performance of the selected subset using CFS filter for an able-bodied
subject is shown in Fig. 4. The figure shows the SVM accuracy for top Class-
correlated features (10-50% of the original subset). The numbers in brackets
indicate the actual number of features after removing the redundant ones. The
performance with best 10% features was lower as few features were available in the
subset and this was observed in all subjects. Also, for all subjects, the performance
reached a peak between the subsets of the top 20-40% class-correlated features.
When looking at the performance of the seven features in the selected subset for the
same subject of Fig. 4, it was noticed that the WDC together with the MAV, SD
and WFL showed good contribution (Fig. 5).

Fig. 7 SVM performance using the best feature subset (selected by CFS) and the MAV
trained in one arm position and tested in all the other positions for an able-bodied subject
(labels on the x-axis indicate training posions)
234 H.M. Al-Angari et al.

Fig. 8 SVM performance using the best feature subset (selected by CFS) and the MAV
trained in one arm position and tested in all the other positions for the amputee subject
(labels on the x-axis indicate training posions)

Table 1 Percenatge of the contribuion of each feature using top 20-50% class-correlated
feature for all three subjects

Feature SUB1 SUB2 SUB3


MAV 14.3±2.3 11.8±1.3 24.1±6.6*
WDC 22.0±7.7 17.3±3.4 1.5±2.9†
WDCDIFF 8.0±5.3 8.5±5.9 5.2±3.6
WFL 15.7±5.1 20.6±6.5 25.3±8.5
SD 14.3±2.3 12.9±3.2 24.1±6.6*
AR 20.9±7.0 21.8±8.6 17.3±14.5
ME 4.9±2.5 7.3±4.1 2.6±3.5
*, † significantly different (p<0.05, p< 0.01respectively)

Table 2 Percenatge of the contribuion of each channel using top 20-50% class-correlated
feature for able-bodied subjects

Channel SUB1 SUB2


CH1† 11.1±8.2 45.8±9.8
CH2† 41.2±12.1 6.1±2.8
CH3 2.8±2.1 2.6±3.2
CH4* 2.8±2.1 0
CH5 0.7±1.4 4.4±3.8
CH6 25.8±5.5 21.7±1.3
CH7 15.5±5.4 19.4±7.1
*,† significantly different (p<0.05, p< 0.01respectively)
Feature and Channel Selection Using Correlation Based Method 235

Low contribution from WDCDIFF and ME was observed, while the percentage
of the AR increased as the subset size increased. Furthermore, there was a strong
correlation between the selected features and the electrode location (Fig. 6). The
contribution from each feature (mean ± std) and channel for each subject is listed in
Tables 1 and 2 respectively. Lastly, no significant difference was found in the
feature selection between the two able-bodied subjects (SUB1 and SUB2), while on
the amputee subject (SUB3) we noticed a significantly higher information content
for the MAV and the SD (p<0.05) and a significantly lower information content for
WDC (p<0.01). For the channel variations, the analysis was applied only on the
able-bodied since they had the same electrode placement. Channels CH1 and CH2
showed significant different contribution (p<0.01). The contribution from CH4 was
also significantly different (p<0.05) however, this is due to the no contribution for
one subjects compared to the very low contribution from the other. No other
significant differences were found in the other channels. Compared to the SVM
performance from each of the 7 features separately (including all the channels), the
CFS with best subset size performed either similar or better than the MAV which
had the best performance (SUB1 (MAV, CFS): 70%, 76%, SUB2: 79%, 79%,
SUB3: 97%, 96%). Furthermore, the comparison was extended to evaluate the
performance when training in each arm position and testing in all the other
positions showed (Fig. 7, 8). The selected features using the CFS filter gave higher
classification accuracy than the MAV for both of the able-bodied subject and were
a bit lower for the amputee subject.

4 Conclusion

A screening filter that selects proper feature and channel for classifying different
hand posture has been proposed in this work. The selected feature subset always
showed higher performance than each single feature for the able-bodied subjects.
In particular, WDC is often selected for able-bodied subject while is has low
contribution in the amputee case. Furthermore, our results highlight that the most
informative electrodes are the ones placed on the posterior side of the forearm.
This is likely due to a bigger role of extensor muscles compared to the flexor
muscles when performing these hand postures. Datasets from more subjects are
needed to verify these findings. A good application of this approach would be in
the field of high-density EMG research where big number of EMG channels is
used. The CFS filter can be utilized to select only channels that are related to a
certain posture of interest. Such applications can be useful in the case of powered
partial-hand prostheses where precise control site localization is both crucial for
the effective usability of the prosthesis and time consuming during the fitting
process.
236 H.M. Al-Angari et al.

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Detection of Movement Intention from
Movement-Related Cortical Potentials
with Different Paradigms

Susan Aliakbaryhosseinabadi1, Ning Jiang2, Aleksandra Vuckovic3,


Romulus Lontis1, Kim Dremstrup1, Dario Farina2, and Natalie Mrachacz-Kersting1
1
Department of Health Science and Technology, Aalborg University, Aalborg, Denmark
2
Department of Neurorehabilitaion Engineering,
Bernstein Center for Computational Neuroscience (BCCN),
University Medical Center Goettingen, Georg-August University,
Goettingen, Germany
3
Biomedical Engineering Division, University of Glasgow, Glasgow, United Kingdom

Abstract. In this study, we compared the effects of two imagery paradigms


typically used within the field of brain computer interfaces on the detection of
movement intention from scalp electroencephalography (EEG). This issue is
important in the rehabilitation area because of its direct relation with appropriately
timed neurofeedback. Subjects were asked to imagine hand or foot movements
using either a random or a non-random cue. Templates were constructed
individually for each subject. Movement intent was detected according to the
correlation between the movement related cortical potentials (MRCP) of single
trials with the initial part of the template. The large Laplacian filter was used to
increase the signal to noise ratio (SNR). For the random cue, the true positive rate
(TPR) of detection of movement intention was 63.5±5.9% for foot movement and
the corresponding detection latency was 202.8±129.5 ms before movement onset.
For the non-random cue, foot movement intention was detected with TPR of
75.3±5.5% and latency of 291±169.3 ms. These results demonstrate that cue type,
random or non-random, has a significant effect on the performance of MRCP-
based movement intention detection algorithms.

1 Introduction

A Brain Computer Interface (BCI) uses brain signals for interaction with the
environment, replacing the need for muscle actions [1]. Many BCI systems are
based on motor imagination (MI) of different motor tasks, such as left hand, right
hand or foot movements [2-5]. Specific features may be extracted and are then
translated into device control commands.
One of the emerging applications of BCI systems is in the area of neuro-
rehabilitation. Here the aim is to decrease motor disability by using interventions
that induce brain plasticity [6]. Brain plasticity is the brain’s ability to change its

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 237
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_42, © Springer International Publishing Switzerland 2014
238 S. Aliakbaryhosseinabadi et al.

structure or function after natural changes or using artificial techniques [5,7]. The
primary candidate mechanism underlying skill learning and memory acquisition is
long term potentiation (LTP) [8] which is an increase in the efficacy of synaptic
communication. For LTP to occur, the postsynaptic neuron must be activated in a
correlated manner with the pre-synaptic neuron. If the intent of a BCI is to restore
motor function, the relevant brain activation induced by MI must be combined in a
specific temporal sequence with sensory feedback from the periphery. Any design
of a BCI for this purpose must thus have a detection speed and accuracy that
allows the exact onset of the planning and the execution of the movement to be
detected. Only then can sensible peripheral sensory feedback be provided to the
user that is correlated with the specific brain activation.
In previous studies we have shown that the timing between the detection of an
intent and the subsequent activation of the external device must be such that the
detection occurs on average at least 50 ms prior to the intended action being
performed [5] for significant plasticity to be induced. There are a number of signal
modalities that may be extracted from the EEG during either real or imagined
movements, such as event related synchronization and desynchronization
(ERD/ERS), event related potentials (ERP) and movement related cortical
potentials (MRCP) [3]. Of these, we have shown the MRCP to be an ideal
candidate for allowing very early detection prior to the task occurrence. The
MRCP is a low frequency signal that represents motor cortical activation during
imagery or actual movement [9]. In the case the subject is cued to do the
movement, the MRCP is often combined with the contingent negative variation
(CNV). CNV is a slow negative slope, present whenever there are two paired cues,
the first being the focus cue for the subsequent cue. The CNV represents a
response to the first cue [10] with peaks at central brain locations during
preparation and execution of cue-based movements [11, 12]. In paradigms where
preparation and execution of movement are cued by two separate cues, or in self-
paced movements, the MRCP commences 2s to 1s prior to the onset of movement
execution, intention or imagination and it displays various amplitude, slope or
latency characteristics according to the neurological disorder [13].
There are two common paradigms in cue-based tasks. In the first paradigm,
there are three phases: focus, preparation for movement and execution of
movement. If a volunteer is asked to perform several different types of
movements[14], the first ‘focus’ phase presents a general preparation (CNV) and
is not movement specific. Volunteers know which movement to perform only
once they see ‘the preparation’ cue. If there is only one type of movement [5],
then MRCP is also likely to be present in the ‘focus’ phase. In the second
paradigm, there are only two phases: focus and preparation/execution [3]. In this
case, volunteers are typically asked to perform different types of movements, so a
response to ‘the focus’ cue is a general preparation, i.e. CNV. The aim of the
present study was to quantify movement detection using MRCPs in these two cued
paradigms. In both paradigms, a warning stimulus was followed by the cue to
move. The first paradigm consisted of two phases and subjects did not know
which of three different movement types they had to perform until the preparation
Detection of Movement Intention from Movement-Related Cortical Potentials 239

and execution cue, while in paradigm two, which consisted of three phases they
had preparation and execution phase separated and were asked to perform only
one type of movement. We hypothesized that due to the limited information
available at the warning stimulus (focus phase) during paradigm one, the MRCP
detection latency would be significantly affected compared to paradigm two.

2 Method

2.1 Subjects
Eight right-handed subjects (2 females, 6 males, aged 28.25±4.23 years)
participated in the experiment. All subjects were healthy and provided their
written and informed consent. The procedure was approved by the local ethical
committee for the region Nordjylland (N-20130039).

2.2 Experimental Setup


Twenty-eight channels of mono-polar EEG were collected using an active EEG
electrode system (ActiveCap, Brainproducts) and g.USBamp amplifier (gTec,
GmbH). Twenty-eight electrodes were placed on F5,F3, F1, Fz, F2, FC5, FC3,
FC1, FCz, FC2, FC4,C5, C3,C1, Cz, C2, C4, CP5, CP3, CP1, CPz, CP2, CP4, P5,
P3, P1, Pz and P2 according to the standard international 10-20 system. The
ground electrode and reference electrode were placed on Fpz and the right earlobe.
The impedances of all electrodes were below 25 kΩ before data recording. No
EMG signal was recorded.

2.3 Visual Paradigms


Subjects received two types of visual cues, a random cue and a non-random cue.
The random cue was comprised of four sequences. The subjects received a
warning cue (cross sign) on a blank screen at t=0 s. It remained there for 5 seconds
(t=5 s). At=2 s, an arrow as the execution cue appeared on the screen. According
to the random arrow direction, subjects were asked to imagine a special motor
task. The right arrow corresponded to ballistic right wrist extension, left arrow for
ballistic left wrist extension and a downward pointing arrow corresponded to
ballistic dorsiflexion. This arrow disappeared after 1.25s and visual feedback
continued with only the cross sign on the screen until t=5 s (Fig. 1). Between
trials, subjects were provided with random rest intervals of 3-5s. Instructions to
the subjects were to continue the imagination until the cross sign disappeared from
the screen (t=5s). Each type of tasks contained 60 trials recorded in 3 subsets with
20 trials.
240 S. Aliakbaryhosseinabadi et al.

Warning 3-5 s

0 1 2 3 4 5 Time(s)

Fig. 1 Random experimental paradigm

The non-random cue was comprised of five time blocks defined as focus,
preparation, execution, hold and rest time (Fig. 2). The focus period had random
duration of 2-3 s. This was followed by a schematic appearing on the screen in
the form of a ramp. A cursor travelled along the ramp and when it reached the
upward turn, the imagery period started. Subjects had to continue imagery for 2 s
followed by a rest period. Subjects performed a total of four sets of 30 trials. For
each 30 trial period, subjects were asked to imagine only one of the following
movements with the dominant side ballistic dorsiflexion or ballistic wrist
extension.

2s 4-5 s
Hold Phase Rest Phase

2-3 s 2 s Task III. MATH


Focus Preparation

Fig. 2 Non-Random experimental paradigm

2.4 Signal Recording


Subjects were seated in a chair with elbows and forearms in his/her preferred
position. As a training part subjects were asked to perform the limited number of
actual movement, i.e. real ballistic dorsiflexion or wrist extension to become
familiar with movements and make them ready to start the main recording with
imagination. After the training session EEG signals were recorded in the same
manner while the subjects were imagining the movements.

2.5 Signal Analysis


Signals were amplified and digitized with a 256 Hz sampling frequency. In
addition, they were band pass-filtered in the frequency range of 0.05-10 Hz with a
2nd order Butterworth filter. The continuous EEG data were divided into intervals
Detection of Movement Intention from Movement-Related Cortical Potentials 241

of 4 s (from 2 s before to 2 s after visual cue) for both cues. The signal analysis
was divided into two steps: MRCP template extraction and motor imagination
detection. The typical MRCPs have low amplitude so a procedure should be used
to increase the SNR. The large Laplacian filter (LF) was applied to the EEG
recordings and the filtered data were used for all subsequent analyses [11].

2.6 Template Extraction


For each subject, the MRCP template was extracted from the spatially filtered data
for each type of movement of both cues. This template was a reference for test
trials of the corresponding subject.
First, data was divided into two general groups based on 3-fold cross-
validation, training and testing. The templates were extracted from the surrogate
channel in the training set as shown in figure 3. The morphology of these two
templates was not the same because of the cue properties.

(a)

(b)

Fig. 3 Template of training data set for (a) non-random cue and (b) for Random cue
242 S. Aliakbaryhosseinabadi et al.

For movement detection, trials of the test set were correlated with templates.
The threshold for making the decision was selected in a range of relatively
appropriate values of TPR and false positive rate (FPR), as estimated on the
training set. This threshold is obtained from the ROC curve. When the threshold
selected was large (based on the maximum value of the correlation) the number of
true detection decreased, although when it was small (based on mean value of the
correlation) the number of false detections was increased. Thus the threshold was
selected in a range of relatively appropriate values of true-detection and false-
detection.
A movement was detected when three tandem windows (2 s sliding window
with 200 ms shift) passed the selected threshold. Detection accuracy and latencies
were computed for each subject as performance factors.

2.7 Statistics
Paired t-test was used to find if there are significant differences between latencies,
TPR and FPR values of different paradigms. Data consider significant different if
their p values become less than 0.05.

3 Result

Although in this study we have two types of intention for the non-random
paradigm and three kinds of imagination for random cue, only the results of
ballistic dorsiflexion were reported.
When MI was performed using the random cue, the average TPR of foot
intention was 63.5±5.9% and 25.5±7.6% as FPR value with the latency of
202.8±129.5 ms before onset.
On the converse, for MI performed with a non-random cue, the average TPR of
foot intention was 75.3±5.5% and 21.7±7.7% as FPR value with the latency of
291±169.3 ms before onset.
Paired t-test showed significant difference in latency (p=0.008) and TPR
(p=0.01) measurements between the two paradigms. However there was no
significant difference between FPR values (p=0.1).

4 Discussion

The main aim of this study was to compare the detection latency and accuracy of
the MRCP for two cued paradigms. In the rehabilitation setting random cue
paradigm is typically implemented to allow a two-dimensional control of external
devices and to avoid fatigue. Thus it is comprised of the subjects having to
perform more than one movement upon the presentation of the cue to move. Since
the subjects do not have information on which of the movements to perform, the
planning of the movement different from the cases where the subject have prior
Detection of Movement Intention from Movement-Related Cortical Potentials 243

knowledge of the movement to be performed. Classification was in this case based


on detection of CNV which like MRCP has a repeatable shape but has a different
dynamics. This may be the main reason why the detection latency was
significantly later compared to the non-random paradigm where subjects know
which movement to imagine. In spite of the non-random paradigm there is no
difference between different types of movement in the initial negative part of the
signals with the random cue because subjects have no information about the types
of imagination, so, this part is likely a non-specific CNV. Although classification
between various movements is feasible for non-random cues before motor
imagination, for the random paradigm this is likely not possible.

5 Conclusion

This study demonstrates the ability of two paradigms for detection of movement
intention with the latency less than 100 ms. We represent non-random paradigm
has better performance than random cue.

Acknowledgment. This work was supported by the Danish Technical Research Council.

References
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Z.Y., Zhang, H.: Clinical study of neurorehabilitation in stroke using EEG-based
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performance of a Brain–Computer Interface based on object oriented motor imagery.
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movements of the left and the right wrist. Med. Eng. Phys. 7, 964–971 (2012)
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association between cortical potentials evoked by motor imagination and afference
induces cortical plasticity. J. Physiol. 7, 1669–1682 (2012)
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outcomes for neurological rehabilitation. J. Physiol. 3, 637–642 (2007)
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Practice and Their Implications for Neurorehabilitation. Arch. Phys. Med.
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Muscle Synergy Features in Behavior
Adaptation and Recovery

Fady S. Alnajjar1, Vincent Berenz1, Ozaki Ken-ichi2, Kensuke Ohno2,


Hitoshi Yamada3, Izumi Kondo2, and Shingo Shimoda1
1
Intelligent Behavior Control Unit, Brain Science Institute,
RIKEN, Nagoya, 463-0003, Japan
fady@brain.riken.jp
2
National Center for Geriatrics and Gerontology, Aichi, Japan
3
TOYOTA Motor Corporation, Aichi, Japan

Abstract. Muscle synergy is the neuromuscular strategy that allows the central
nervous system (CNS) to deal with muscle redundancy. In muscle synergy, muscles
which are activated in asynchrony, when performing particular movement, are
grouped and controlled by low-dimension motor signal. The relationship between
the neuromuscular strategy for behavioral adaptation to unfamiliar task in healthy
human and recovering motor function after stroke is still unclear. Here we
investigated the behavioral adaptation of six healthy participants who were
introduced to unfamiliar task and we compared their resulting synergies with those
observed from three stroke survivors throughout their recovery process. Our results
revealed that the dimension of the resulting synergies of the healthy participants
when introduced to an unfamiliar task was initially lower than the original; causing
a restriction in the range of the joint motions and resulting in abnormal movements.
The synergy dimension in those participants was gradually adjusted through
behavior training. Interestingly, similar synergy patterns were also observed in
cortical stroke survivors. This similarity in adaptation could be used to enhance the
regular post-stroke therapeutic approaches by providing opportunities of testing
various training protocols in healthy subjects before carrying only the efficient ones
to the post-stroke patients.

1 Introduction
Understanding the complex neuromuscular strategies behind behavioral adaptation
in human is essential to gaining fundamental knowledge of our motor control
system. Many attempts have tried to accomplish the computational mechanism to
explain such as adaptation, including the analyses of motor neuron activities [1][2],
suggesting the biological control architectures [3][4], and proposing learning
mechanisms based on biological systems [5][6]. Along with these efforts, in this
study, we were investigating the behavior adaptation from the viewpoint of how the
CNS deals with muscle redundancy which could be the key factor to provide a
fundamental clue behind our adaptability to the surrounding environments.
The notion of muscle synergy has been used to define the synchronization level
of several muscles as low-dimensional modules controlled by simple control signal.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 245
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_43, © Springer International Publishing Switzerland 2014
246 F.S. Alnajjar et al.

Muscle synergy, therefore, explains the computational mechanism for choosing,


from a wide range of muscle selection, the appropriate combination of muscles to
control efficiently point-to-point movements [7]-[9].
The purpose of the current study was to investigate whether healthy participants
exhibit muscle synergy strategies during their adaptation to an unfamiliar task that
are comparable to those exhibited by stroke survivors during their motor recovery
stage. Answering this question may provide crucial insight in motor adaptation and
recovery that could be used to suggest an effective post-stroke rehabilitation
systems better tailored to the treatment of specific motor deficits.
In this paper, we were comparing the behaviors of post-stroke patients with
those of healthy participants performing unfamiliar task created by a robotic
manipulator with a bilateral controller. We used a non-negative factorization
algorithm (NMF) to compute muscle synergies [10]. Experimental results of both

Participant
Manipulandum’s Ending Starting
knob point point
Robotic A display to
manipulandum show the
workspace (blue)
and the knob
position (white)

(A)

(B) (C)

Fig. 1 (A) Experimental setup for healthy participants (participant posture, manipulandum,
display positions, and workspace). The white circle in the display illustrates the position of
the manupulandum knob. The knob position was displayed to the participant to simplify
tracking in the assigned task. (B) Experiment protocol for the healthy participants. Top
view illustrating the task (horizontal shoulder adduction) and the recorded muscles in the
upper torso and right arm. (C) Experiment protocol for the post-stroke participants. Side
view illustrating the task (shoulder flexion). pectoralis major (PM), deltoid anterior (AD),
infraspinatus (IS), teres major (TM), latissimus dorsi (LD), biceps brachii (BI), and
brachioradialis (BR).
Muscle Synergy Features in Behavior Adaptation and Recovery 247

participants’ group show similar muscle synergy strategies: synergies were


initially operated in a low dimensional space, and gradually adjusted as the
healthy participants adapted to the unfamiliar task and as the post-stroke
participants recovered motor function.

2 Methods
2.1 Experiments on Healthy Participants
2.1.1 Participants
Six healthy adults (age range: 23~37 years), participated in this experiment. All
participants were right-handed and reported no neurological or upper-limb
muscular impairments. This experiment protocol was approved by the RIKEN
ethics committee.

2.1.2 Robotic Manipulators


To design an unfamiliar task, the healthy participants were asked to control the
gripper position of a robotic manipulandum using their right arm. The
manipulandum has a bilateral control system, allowing the participant to feel
the computer-generated virtual space through the forces generated. During the
experiment, a participant was seated on an adjustable chair with the right hand
holding the knob of the manipulandum from the side. A display of the virtual space
was placed in front of the participant to facilitate performance of the assigned tasks,
Fig.1A.

2.1.3 Muscle Activities


Surface Electromyography (sEMG) was recorded from primary muscles acting on
the participant’s right shoulder. Due to the nature of the assigned task (right-hand
horizontal shoulder adduction), the following six muscles were recorded: pectoralis
major (PM), deltoid anterior (AD), infraspinatus (IS), teres major (TM), latissimus
dorsi (LD), and biceps brachii (BI). EMG electrodes were placed in accordance
with the guidelines of Surface Electromyography for the Non-Invasive Assessment
of Muscles (SENIAM)–European Community project [11]. EMG signals were
sampled at 1kHz, high-pass filtered with a cutoff frequency of 30Hz,
root-mean-square rectified, and smoothed using a moving average with a window
of length 10 samples, [9].

2.1.4 Experiment Protocol

The healthy participants were asked to perform three different tasks:


• Standard Task: we asked participants to grasp the knob of the manipulandum
and perform 10 trials of horizontal shoulder adduction from a predefined
starting position, Fig.1B. To ensure that the experiment constraints were similar
across individuals, we instructed the participants to not use their elbow, to
248 F.S. Alnajjar et al.

maintain a constant contraction of the shoulder muscles, and to complete each


trial within 1sec. In this task, the manipulandum was not producing any
significant resistance on the participant’s arm. The starting and ending points of
the movement were denoted by the manipulandum knob position displayed on
the screen in front of the participants. Participants were allowed to practice the
task for 20 trials before actual experiment recording to guarantee that this task
is familiar for all participants.
• Unfamiliar Task: in order to introduce an unfamiliar task to the participants,
we modified the robotic manipulandum responses by randomly applying
approximately 7N of resistance on the participant’s. arm opposite to the
standard task direction. We call this task the unfamiliar task because even
healthy participants could not master the movement (i.e., utilized the proper
muscle synergy, and move the knob in straight trajectory) from a single trial.
• Adaptation to the Unfamiliar Task: we examined the participants’
adaptability to the unfamiliar task through training by free repetition. Thus, we
asked the participants to perform 30 trials of horizontal shoulder adduction (The
7N resistance was applied continuously along all the trials). The participants
were given a rest period of 120sec after the first 15 trials to minimize any
potential for muscle fatigue.

2.2 Experiments on Post-Stroke Participants


2.2.1 Participants
Three stroke survivors (age range: 63~69years) participated in this experiment.
Participants diagnosed with cerebral infarction, unilateral motor impairment with a
stroke impairment assessment set (SIAS) level (SIAS=2~4). This experiments
protocols were approved by the ethics committee of the National Center for
Geriatrics and Gerontology.

2.2.2 Experiment Protocol


Due of the nature of the patients’ impairment and their constrained range of joint
motion, we the patients to do a simple shoulder flexion task (both right and left
arms simultaneously). A set of 5 to 10 trials was conducted for each patient for two
to three sets.
Five sEMG were recorded from muscles acting on the patient’s right and left
shoulders while performing the task: PM, AD, IS, BI, and brachioradialis (BR),
Fig.1C.

2.3 Computation of Muscle Synergy


One of the most important features of using muscle synergy is to reduce the
dimensions of controlling the muscles. When m muscles are controlled, for
instance, m commands are generally required. Assuming EMG data of m
muscles are represented a matrix M, then:
Muscle Synergy Features in Behavior Adaptation and Recovery 249

, (1)

where m and t are the number of muscles and the number of the recorded
sampling data, respectively. The number of commands for controlling m
muscles can be reduced by the use of NMF that factorize M data into matrix of
the muscle synergy W, and neural command C:
, (2)

Where , , , and n is the number of the


needed synergy dimension (SyD) to represent the original data M, with small
enough error E.
Basically, we must choose an appropriate n, according to the behavior, to
estimate the most accurate W and C. We choose n using the following steps:
• Acquire EMG data of m muscles and create time sequential data of the
muscle activations M by filtering the raw EMG data.
• Temporarily define n as nt, and estimate Wnt and Cnt using NMF.
• Compute the estimation error E, and compute the size of E, called variance
accounted for (VAF), such that

(3)

were ||.||F denotes the Frobenius norm. If VAF is smaller than a predefined
threshold, we change nt to (nt + 1) and compute by NMF again. VAF increases as nt
increases. The threshold is decided based on the behavior, but generally on this
study, we use approximately 90% to indicate a good fit to the original data.
• We continue the above computation until VAF becomes larger than the
threshold. We use the value of (nt +i) as the dimension of the neural signal n,
thereby completing our selection of n and estimation of both associated W and
C.
From the above, we define n to be the synergy dimension index (SyD) that plays
a key role in representing level of adaptation to the environment. We illustrate this
feature through our experiments with healthy and post-stroke participants.

3 Results
3.1 Dimensions of Synergy Space
3.1.1 Healthy Participants (Familiar vs. Unfamiliar Task)
Fig.2A shows the dimensionality of the resulting muscle synergies for participants
performing the familiar task. from the figure, all participants needed
two-dimensional muscle synergy to complete successfully the task (the VAF of
250 F.S. Alnajjar et al.

SyD2>90% threshold). We have looked at the functional role of each synergy and
found that: Syn#1 was mainly involved in activating muscles which are primarily
responsible for shoulder adduction. Syn#2, on the other hand, was involved in
manipulating the muscles which assist in internal rotation of the shoulder joint (due
to pages limitation, the figures are not included).
Fig.2C shows the dimensionality of the resulting synergies while performing
the unfamiliar task. When the resistance was randomly applied, all participants
utilized one-dimensional muscle synergy to complete the task (SyD1). The
unorganized muscles activations, represented by the utilized one synergy in this
stage, seem to cause a reduction in the range of shoulder joint-internal rotation
(observed during the experiment).

3.1.2 Post-Stroke Participants (Unaffected vs. Affected Side)

Fig.2B and Fig.2D show the dimensionality of the resulting muscle synergies of the
unaffected and the affected arms of the three patients on the first day of conducting
the experiment, respectively. From the figure, One-dimensional synergy was used
to produce motion in the affected arm, while two-dimensional synergies were used
to produce motion in the unaffected arm. Again, for the two-dimensional synergies
of the unaffected arm, Syn#1 was involved in activating the muscles which are
primarily responsible for shoulder flexion, while Syn#2 was involved in assisting
the internal rotation of the shoulder joint (figures are not included). The
one-dimensional synergy in the affected arm, on the other hand, seem also to be the
major cause of the abnormal synergy movement.

3.2 Adaptation and Recovery


For healthy participants, Fig.3A shows the gradual transformation from
one-dimensional muscle synergy (before adaptation) to two-dimensional synergies
(after adaptation) over the trials 0, 10, 20 and 30.
For post-stroke participants, Fig.3B illustrates the update process of the
one-dimensional synergy case SyD1 of all participants over the first, fifth, and ninth
-week period in which they engaged in a regular rehabilitation course. Although the
synergy remained one-dimensional, there were notable changes in VAF, which
seems to tend toward the formation of two synergies (till the moment we still
following up with the patients to emphasize this part).

4 Discussion
The experimental results in healthy participants revealed that the formation of
muscle synergies was altered when experiencing an unfamiliar task. Compared
with the dimensions of muscle synergy in the familiar task, the dimensionality of
the utilized muscles synergies were reduced when the participants were first
presented to the unfamiliar task. The dimension reduction of the synergy seemed to
Muscle Synergy Features in Behavior Adaptation and Recovery 251

100 100

VAF[%]
90

VAF[%]
90

80 80

70 70
1 2 3 SyD 4 5 6 1 2 3 4 5
SyD

(A) (B)

100 100

VAF[%]
90
VAF[%]

90

80 80

70
70
1 2 3 4 5
1 2 3 SyD 4 5 6 SyD

(C) (D)

Fig. 2 Experimental results: the VAF of all the identified synergies from the recorded EMG
while (A) healthy particiapnts performing the familiar task (mean ± SD of 6 participants).
(B) Post-stroke particiapnts performing by the unaffected arm (mean ± SD of 3
participants). (C) Healthy particiapnts performing the unfamiliar task. (D) Post-stroke
particiapnts performing by the affected arm. The dotted vertical line identifies the estimated
number of utilized synergies that exceeded the threshold (90%; represented by the
horizontal dotted line).

100 100
VAF[%]

95 95
VAF[%]

Trial(1) 90 Week(1)
90 Trial(10) Week(5)
Trial(20)
Trial(30) 85 Week(9)
85
1 2 3 4 5
1 2 3 SyD 4 5 6 SyD

(A) (B)

Fig. 3 (A) For healthy participants: the gradual transformation from one-dimensional
synergy (SyD1) to two-dimensional synergies (SyD2) through training (mean across 6
participants). (B) For post-stroke participants: the gradual changes in the one-dimensional
synergy through the recovery process. Although SyD1 does not transfer to SyD2, it seems to
be moveing towards it (mean across 3 participants).

cause the simultaneous increases in muscle activations in response to the unfamiliar


environmental inputs. This unusual activation state of the muscles implies that all
muscles were placed in a standby status to react to any unpredictable input that may
be caused by the unknown environment.
252 F.S. Alnajjar et al.

The experimental results in post-stroke participants showed the difference


between the synergy dimension utilized by the affected and the unaffected arm.
Again, the dimensionality were reduced in the affected arm that caused unusual
muscle activation, and therefore, abnormal motion. During the recovery process, a
gradual decline in VAF over the recovery period appeared, which could be the
potential toward increases in the dimensionality of synergy.
In this study, the adaptation of the healthy participants and recovery of the
post-stroke participants showed similar features from the viewpoint of muscle
synergy analysis. Regardless of the participants age and/or the assigned tasks,
which we could not make similar due to the limitation that we have in selecting
participants, synergies in both cases varied as a function of how much the control
system is adapted to the environment. Experiencing the unfamiliar task for healthy
participants causes a temporal obstruction in the neural processes of the CNS and
muscles which prevents the CNS from forming an efficient set of muscle synergies.
This can be inferred by the unregulated activities of the muscles and the reduction
of the dimensions of the utilized muscle synergy. Similar scenario occurred in the
post-stroke participants. Through training, however, the dimensions of the utilized
synergies for both the healthy and the post-stroke participants gradually increased,
leading to the emergence of efficient motions.

5 Conclusion

This study suggests that the dimension of muscle synergy could be used as an index
to define the level of motor function adaptation and/or recovery. Our results
showed that the performance of the healthy participants when performing in an
unfamiliar environment and the early stage motions of the post-stroke participants
were initially operated in a low-dimension synergy space. As the healthy
participants adapted to the unfamiliar environment and as the post-stroke
participants recovered motor function, the dimension of the utilized synergy space
gradually increased. These changes in the dimension of synergy can be interpreted
as the result of behavioral adaptation to the environment, given that increases in the
range of joint motion.
Testing various training hypotheses directly in post-stroke patients can be
extremely challenging task due to the age of typical stroke patients and other
related factors. Since our synergy analysis results suggest that motor function
recovery in post-stroke patients is comparable to adaptation to unfamiliar
environments in healthy participants, a natural future step to these findings would
be to investigate the introduction of multiple unfamiliar tasks to healthy
participants, as a way to create a virtual stroke-like scenario on them. This will help
us test various training protocols to determine methods to enhance the adaptation
process. Only the best training protocols that offers speed and proper adaptation,
can be then carried to be tested in stroke survivors. We are currently working in
such as training scenarios.
Muscle Synergy Features in Behavior Adaptation and Recovery 253

Acknowledgment. This work was done under the support of Toyota Motor Co. We are very
grateful for their technical and financial assistance.

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Human Cutaneous Reflexes Evoked with
Simultaneous Multiple Nerve Stimulation
during Rhythmic Locomotor-Like Arm
and Leg Cycling in Stroke Subjects

Ole Kæseler Andersen1, Marc Klimstra2, Evan Thomas2, Pamela M. Loadman2,


Sandra R. Hundza2, and E. Paul Zehr2,3
1
Aalborg University, Aalborg, Denmark
oka@hst.aau.dk
2
Rehabilitation Neuroscience Laboratory,
University of Victoria, Victoria,
British Columbia, Canada
3
Centre for Biomedical Research,
University of Victoria,
Victoria, British Columbia, Canada

Abstract. The neural coupling between arms and legs during rhythmic activity has
previously been investigated in healthy volunteers by cutaneous stimulation
during concurrent arm and leg cycling. In this study, the coupling between arms
and legs was investigated in 15 chronic stroke survivors with hemiplegia.
Cutaneous reflexes were evoked by electrical stimulation of nerves innervating the
foot of the most affected leg. Participants performed rhythmic cycling with the
arms and legs during four trials with different stimulus configurations. Non-
painful stimulations were delivered at the ankle level to the superficial peroneal,
sural, tibial, and by stimulation of all three nerves simultaneously. EMG was
recorded from four ipsilateral muscles (biceps femoris (BF), vastus lateralis (VL),
medial gastrocnemius (MG), and tibialis anterior (TA) in the more affected leg.
Phase-dependency was tested by recording reflexes at four different equally
spaced phases of the locomotor cycle. Large excitatory VL reflexes were seen in
the relaxation phase of the stimulated leg. For BF, an inhibitory reflex was
observed in the power phase while an excitatory reflex was observed in the
relaxation phase of the cycle. In the TA muscle, significantly larger reflexes were
observed when all three nerves were stimulated simultaneously compared to
stimulation of the three nerves individually (ANOVA P<0.05, post-hoc P<0.05).
No differences were found between reflexes evoked by the three nerves in any of
the muscles. No ANOVA interaction between phases and nerves was observed in
any of the ANOVA analysis. Central non-linear summation of afferent non-
nociceptive input occurs within the spinal reflex circuits after stroke. Sensory
integration in reflex pathways could be exploited in gait rehabilitation after stroke
by supporting ankle dorsi-flexion and thereby facilitating the relearning of gait in
the subacute phase.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 255
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_44, © Springer International Publishing Switzerland 2014
256 O.K. Andersen et al.

1 Introduction

The neural coupling between arms and legs during rhythmic activity has
previously been investigated in healthy volunteers by cutaneous stimulation
during concurrent arm and leg cycling [1]. Sensory input from the arms and legs
support functional movements, however the input is modulated by the phase of the
legs in the cyclic movement.
Integration of nociceptive [2] and tactile [3] afferent activity in spinal reflex
pathways has resulted in enhanced reflexes during gait. Moreover, according to
the flexor reflex afferent theory multisensory integration is occurring in the spinal
reflex pathways which include tactile cutaneous afferents [4]. It has not been
investigated to what extent this sensory integration takes place for non-nociceptive
activity originating from closely located skin areas (spatial summation) in humans.
Ergometer cycling involving activity in both arms and legs are speculated to
reflect activity from coupled central pattern generators. Stimulation site
dependency has been observed for nociceptive stimulus intensities during gait in
stroke patients [5].
The aim of the present study was to investigate nonlinear summation in spinal
reflex pathways for non-nociceptive afferent input and further to test phase
modulation in a population of stroke subjects during cycling involving both arms
and legs.

2 Methods

2.1 Participants
Fifteen participants (39 to 83 yrs; 3 female, 12 male) with documented
neurological cerebrovascular accident (CVA) (2 to 23 yrs post injury) localized in
the right (n=8) or left (n=7) cerebral hemisphere participated in the experiments
with informed, written consent. Medical records from all participants were
obtained with consent. Additionally, clinical measurements (Brunnstrom,
Ashworth, Semmes-Weinstein) were performed to determine the level of motor
and sensory deficit. For each participant the more (MA) and less affected (LA)
sides of the body were separately evaluated. This project was conducted under the
sanction of the Human Research Ethics Board at the University of Victoria and
performed according to the Declaration of Helsinki.

2.2 Experimental Protocol


Participants performed simultaneous arm and leg cycling at a comfortable self
selected pace (48±7 rpm; mean±SD) on an instrumented cycle ergometer (Pro II,
SCIFIT Systems, Tulsa OK). The arm and leg cranks of this device are
mechanically coupled such that the arms and legs are 90° out of phase with one
Human Cutaneous Reflexes Evoked with Simultaneous Multiple Nerve Stimulation 257

another in a relationship similar to walking [6]. Prior to cycling, each foot was
secured to the leg cranks using boots that limited excessive ankle
inversion/eversion and would not slide off the pedals. For participants with limited
grasping ability a specially constructed plastic wrist orthosis was used that
allowed attachment of the arm to the cranks. Additionally in order to compensate
for the flexed postures of many participants, a safe and comfortable range of
cyclical motion for each arm and leg was obtained by modifying crank arm length
individually for each limb. Resistance was set to baseline for all participants.

2.3 Nerve Stimulation


Cutaneous reflexes were evoked with trains (5 X 1.0 ms pulses at 300 Hz) of
isolated constant current stimulation delivered pseudorandomly (every 2 to 4
seconds) with a Grass S88 (Grass Instruments, AstroMed Inc.) stimulator
connected in series with an SIU5 isolator and a CCU1 constant current unit. The
electrical stimulation was applied on the participants MA side either separately to
the superficial peroneal (SP), Tibial (Tib) and Sural (Sur) nerves or
simultaneously to all 3 nerves (Sim). Disposable surface electrodes (Thought
Technologies Ltd, Montreal, PQ, CAN) were placed in a bipolar configuration on
the anterior surface of the foot near the crease of the ankle joint (SP), halfway
between the medial malleolus and the Achilles tendon (Tib), and halfway between
the lateral malleolus and the Achilles tendon, (Sur) [6]. Stimulation at these sites
produced radiating paresthesia over the dorsum of the foot (SP) plantar surface
(Tib) and lateral border of the foot (Sur). Participants were instructed to notify the
investigator if the stimulation produced painful or uncomfortable sensation at
which point intensity was returned to non-painful levels. During this procedure the
level of stimulation that was just detectable (perceptual threshold, PT) and that
which produced radiating parasthesia into the appropriate cutaneous field
(radiating threshold, RT) were determined. Stimulation intensity was set to non-
painful levels of approximately 2xRT for each participant. For each nerve
stimulation configuration, participants maintained a static posture (MA leg at 3
o’clock) while 20 stimulations were averaged in order to evaluate stimulation
efficacy. As needed, stimulation conditions (electrode placement and intensity)
were altered slightly to evoke a noticeable cutaneous reflex response in average
EMG traces.
If participants had alteration in sensory perception that made it difficult to
obtain stimulation thresholds, PT and RT were assessed on the unaffected leg and
then these values were used to administer the stimulation to the affected leg in a
similar electrode position to the contralateral (unaffected) side.
During arm and leg cycling cutaneous reflexes were randomly evoked at 4
different equidistantly spaced movement positions (3, 6, 9, 12, see Fig. 1) for a
total of 15 stimulations for each position.
258 O.K. Andersen et al.

2.4 Cycle Timing


The position of the ergometer crank arms in the movement cycle was determined
from an optical encoder that measured the position of the crank arm with respect
to a clock face position.

Fig. 1 Cycle ergonometer: The arm and leg cranks are mechanically coupled so that the
arms and legs are 90° out of phase in a relationship similar to walking.

Thus, the position when the ipsilateral leg crank was straight up was defined as
12 o’clock with positional definitions continuing clockwise on the right side and
counterclockwise on the left side. All references to position in the movement cycle
are thus given with respect to a clock face and partitioned into 12 separate bins [1].

2.5 Electromyography

The skin was cleansed with alcohol and disposable electrodes (Thought
Technologies Ltd, Montreal, PQ, CAN) were applied in a bipolar configuration
(~2 cm interelectrode distance) longitudinal to the predicted path of the muscle
fibres. Muscles studied included the soleus, tibialis anterior, vastus lateralus and
biceps femoris muscles on the most affected side of the body. All EMG recordings
were ipsilateral to the site of nerve stimulation. Ground electrodes for the EMG
were placed over electrically neutral tissue, those being the olecranon and
acromion processes and the patella. EMG signals were preamplified and bandpass
filtered at 100–300 Hz (P511 Grass Instruments, AstroMed, Inc.).
Human Cutaneous Reflexes Evoked with Simultaneous Multiple Nerve Stimulation 259

2.6 Data Acquisition and Analysis


All data were sampled at 1000 Hz with a 12 bit A/D converter connected to a
computer running custom-written (Dr. Tim Carroll, University of New South
Wales, Australia) LabView (National Instruments) virtual instruments. Online,
data were separated into 4 equal phases corresponding to the clock positions on
the affected side with the optical encoder signal. All evoked responses to stimuli
occurring in the same part of the cycle were aligned to stimulus delivery within
that part of the cycle and averaged (n=15) together within a 300 ms window
centred around the delivered stimulus (100 ms prestimulation, 200 ms post-
stimulation). Offline all data (EMG, kinematic) were analyzed using custom
written software (Matlab, MathWorks, Inc).

2.7 EMG Analysis


Reflex EMG traces were produced by subtracting average unstimulated traces
from the stimulated average traces at the same position in the movement cycle.
The stimulation artifact was removed from the reflex traces which were then low-
pass filtered using a 3rd order Butterworth dual pass filter set at 40 Hz.

2.8 Cutaneous Reflexes


For each participant, subtracted reflex EMG traces from each muscle were analyzed
for peak reflex amplitudes in the middle latency period (80–120 ms after stimulus
onset. Only those reflexes which exceeded a 2-SD band were analyzed. The onset
latency was determined as the peak response taken from when the reflex exceeded
this band until it returned back inside the band. Averages of 10 ms duration centered
around these responses were analyzed for phasic reflexes. For each participant,
cutaneous reflexes within a muscle were normalized to the peak value of the control
(unstimulated) EMG for that muscle across the movement cycle.

2.9 Statistical Analysis


Analysis was conducted on averaged values for each participant from each
position in the movement cycle. Significant reflexes were calculated by comparing
the values for control and stimulated positions for each parameter. Repeated
measures two-way analysis of variance was used to determine the main effects.
For post-hoc analysis, the Student Newman–Keuls statistics (SNK) was used. P <
0.05 was regarded as statistically significant.

3 Results

Grand mean reflexes for the four stimulus configurations and four phases of the
gait cycle are depicted in Fig. 2.
260 O.K. Andersen et al.

Fig. 2 Grand mean reflexes evoked by the individual nerves and by concurrent stimulation
of all three nerves. The dashed lines represent baseline EMG activity as a result of
subtracting background EMG activity from traces without stimulation (see methods).

Two-way ANOVA analysis of peak reflex size in the 80-120 ms indicates


phase-dependent modulation in thigh muscles BF (ANOVA P<0.01) and VL
(ANOVA P<0.05). The post-hoc analysis revealed large excitatory reflexes in VL
at 6 o‘clock (recovery phase) compared to three other phases (SNK P<0.05)
independent of which nerve was stimulated. Inhibitory reflexes were observed in
BF at the 12 and 3 o‘clock positions (power phases). Compared to the other
phases, a significant difference was seen compared to the 6 and 9 o’clock phases.
In the TA muscle, the largest reflexes were observed when all three nerves
were stimulated simultaneously compared to stimulation of the three nerves
individually (ANOVA P<0.05, SNK P<0.05). This is particularly evident at the 9
o’clock position which corresponds to mid-swing during walking [8].
No main effects were observed in the MG muscle and no differences were
found between reflexes evoked by the three nerves in any of the muscles. No
ANOVA interaction between phases and nerves was observed in any of the
ANOVA analysis.
No main effects of phase were seen in TA and MG muscles.

4 Discussion

The functional modulation during the recumbent cycling can be interpreted in


terms of similar alternating extensor flexor activity during gait.
Central, non-linear summation of afferent non-nociceptive input occurs within
the spinal reflex circuits after stroke. Summation has previously been
demonstrated for nociceptive input in healthy volunteers during gait [3] and arm
and leg cycling [2] and with the present study sensory integration for non-
nociceptive intensities has been demonstrated also after damage to the nervous
system. This observation has implications for the use of tactile cutaneous
stimulation as a therapeutic modality for gait rehabilitation after stroke.
Human Cutaneous Reflexes Evoked with Simultaneous Multiple Nerve Stimulation 261

5 Conclusion

Central non-linear summation of afferent non-nociceptive input occurs within the


spinal reflex circuits after stroke.

Acknowledgment. The research council for Technology and Production, Denmark funded
OKA and a Grant-in-Aid of Research from the Heart and Stroke Foundation (BC & Yukon)
funded the research in Victoria.

References
[1] Balter, J.E., Zehr, E.P.: Neural coupling between the arms and legs during rhythmic
locomotor-like cycling movement. J. Neurophysiol. 97, 1809–1818 (2007)
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interlimb reflexes evoked by stimulating the hand simultaneously with conditioning
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Towards Establishing Clinical Guidelines for an
Arm Rehabilitation Virtual Reality System

Philippe S. Archambault1, Nahid Gheidari Norouzi1, Dahlia Kairy2,


John M. Solomon3, and Mindy F. Levin1
1
School of Physical and Occupational Therapy, McGill University,
Montreal, H3G 1Y5, Canada
and
Interdisciplinary Research Center
in Rehabilitation (CRIR), Montreal, H2H 2N8, Canada
{philippe.archambault,mindy.levin}@mcgill.ca,
nahid.norouzi@mail.mcgill.ca
2
School of Rehabilitation, University of Montreal, Montreal, H3C 3J7, Canada
and
CRIR
dahlia.kairy@umontreal.ca
3
Department of Physical Therapy, Manipal University, Manipal, 576104, India
john.solomon@manipal.edu

Abstract. Virtual reality (VR) can promote functional rehabilitation of arm


movements through environments allowing the practice of a variety of tasks while
providing feedback. We evaluated an affordable VR system for arm rehabilitation,
developed by Jintronix Inc, based on the Microsoft Kinect and providing three
unilateral and two bilateral activities, each with ten difficulty levels. Our
objectives were to 1) determine which activities and levels of difficulty are
appropriate for rehabilitation of arm movements in stroke patients with different
degrees of motor impairment; and 2) determine the ease of use and subjective
experience of patients using the VR arm rehabilitation system. Stroke patients
participated in three 20-minute practice sessions supervised by a rehabilitation
professional. We determined the highest level of difficulty attained by patients in
each activity with a performance score of at least 50% and mapped these to arm
impairment level according to the Chedoke-McMaster Arm Scale. Over 80% of
the participants provided positive feedback in terms of ease of use and VR
experience. Our data demonstrate the feasibility of using an affordable VR arm
rehabilitation system in a clinical setting and provide clinical guidelines for the
selection of impairment-specific difficulty levels.

1 Introduction

Stroke contributes significantly to the incidence of disabilities of the upper limb


(UL) [1]. Rehabilitation is one of the key interventions for stroke, and there is

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 263
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_45, © Springer International Publishing Switzerland 2014
264 P.S. Archambault et al.

mounting evidence that functional recovery of arm paresis can occur well into the
chronic stage of stroke [2, 3]. Improvements may be due to sensorimotor learning
and adaptive plasticity in the remaining brain tissue [4]. Enriched trainings
environments, such as those afforded by virtual reality (VR) may promote brain
plasticity by incorporating factors related to cognitive abilities [4], the type of
movement [5, 6] and the environmental context [7]. Indeed, each of these factors
can be manipulated in a VR environment [8, 9]. Enhanced learning occurs when
participants practice a variety of related tasks [10, 11] and receive feedback
intermittently, to allow the central nervous system time to integrate sensory
information into purposeful movement [12]. There is limited evidence that motor
improvements gained in VR training environments may transfer to real-world
functional gains [13, 14].
Existing VR systems that promote the use of the UL are often expensive and
restricted to research settings [15]. While there has been an increase in the
availability of consumer-level VR games and systems (Nintendo Wii, Microsoft
Kinect, etc.), such games are not designed for clinical need. For example, while
they may be engaging and readily available, they do not specifically address
rehabilitation of UL movements and do not provide the necessary feedback to
individuals with stroke or to clinicians [16]. In response to this problem, several
research groups and software companies have begun developing and evaluating
VR systems built with consumer-level devices, which are aimed at the
rehabilitation of UL movements [17-20]. Evidence of the effectiveness of VR in
the functional recovery of UE movement is still limited [14] and one reason may
be a lack of clear clinical guidelines, i.e., understanding which activity, at which
difficulty level, can be appropriate for which stroke patient. The long-term
objective of this research is to provide an effective and affordable VR system for
UL rehabilitation in stroke, which could be used in addition to regular therapy. As a
first step, the aim of this study was to provide a flowchart linking UL impairment
level of stroke patients with activities and difficulty levels of a Kinect-based VR
rehabilitation system.

2 Methodology

2.1 Participants
We recruited clinicians and stroke patients from two rehabilitation hospitals in
Canada (Jewish Rehabiliation Hospital [JRH] and Gingras-Lindsay Montreal
Rehablitation Institute [IRGLM]) and one hospital in India (Manipal University
Hospital [MUH]). All participants provided their informed consent, as approved by
local ethics guidelines. Clinicians were physical or occupational therapists, with at
least one year of experience working on a neurological unit. For the stroke
participants, the inclusion/exclusion criteria were: age between 40 and 70 years;
have sustained a stroke at least 3 weeks but not more than 6 months before the study.
Towards Establishing Clinical Guidelines 265

Fig. 1 The Jintronix VR rehabilitation system

2.2 Kinect-Based VR System


The low-cost VR rehabilitation system used in this study was developed by
Jintronix Inc (Montreal, Canada) [20]. It consists of a computer interfaced with a
Kinect camera to track upper body movements (head and trunk, as well as shoulder,
elbow and wrist on both sides). There are in total 3 unilateral and 2 bilateral
activities, in which participants reach for, transport and release objects or move the
arm through a prescribed trajectory (Fig 1). Each activity has 10 difficulty levels,
with increasing requirements on range of motion (object location in the workspace)
movement speed (timer) and precision (size of targets; presence of obstacles). After
completion of each activity, a performance score is provided by the application.
Clinicians in the study received a 30-min training session on the operation of the
VR system and then worked with 2-3 stroke patients during three 20 min individual
VR training sessions, separated by two or three days. Clinicians were asked to
determine the maximal level of performance in each of the five activities for their
patients.

2.3 Data Collection and Analysis


Each stroke participant was assessed using the UL section of the Chedoke-
McMaster Scale (CM) [21], a measure of impairment. We recorded each VR
session’s duration, the activities that were performed together with their difficulty
level and performance score. The system also provided an overall session score,
which is the mean activity performance score weighted by difficulty level. At the
end of the study, stroke participants completed a questionnaire on the perceived
ease of use of the Jintronix VR system [22], as well as the Short Feedback
266 P.S. Archambault et al.

Questionnaire [23], to obtain subjective responses to the VR experience on


presence, enjoyment and realism.
We calculated the highest difficulty level attained over all three sessions, with a
performance score of at least 50%, as a measure of the attainable goal for each
patient. Descriptive statistics (mean, standard deviation, range) were calculated
various outcomes.

Table 1 Characteristics of stroke patients

Age b Stroke onset Computer?


Center Gender CM
(yrs) (mts) (y/n)
50 JRH M 3 8 no
76 JRH F 4 2 no
52 MUH M 5 3 yes
70 MUH M 5 3 no
49 MUH F 5 6 no
70 MUH F 5 1 no
68 JRH M 5 3 no
26 JRH F 5 7 yes
78 IRGLM F 5 2 no
36 JRH M 6 3 no
44 IRGLM M 6 2 yes
54 IRGLM M 6 2 yes
45 IRGLM M 6 1 no
33 IRGLM M 7 1 yes
a
Chedoke-McMaster score

70
60
Session score

50
40
30
20
10
0
1 2 3
Session number

Fig. 2 Progression of overall session score (mean + SD) over the three VR sessions
Towards Establishing Clinical Guidelines 267

10

Difficulty level
CM
6
3-4
4 5

2 6-7

0
Fish Pixel Kitchen CCD Pop clap
frenzy waves clean

Fig. 3 Mean of highest difficulty level achieved with a performance score of at least 50%
for all five activities according to arm impairment level (CM). The first three activities
required unilateral arm movements while the other two were bilateral.

100%
% participants

80% positive
60% neutral
40%
negative
20%
0%

Fig. 4 Proportion of participants who provided positive, neutral or negative answers to the
Ease of Use Questionnaire

100%
% participants

80%
60%
positive
40%
neutral
20%
0% negative

Fig. 5 Proportion of participants who provided positive, neutral or negative answers to the
Short Feedback Questionnaire
268 P.S. Archambault et al.

3 Results

A total of 14 stroke patients with a mean age of 54±16 years completed the three
sessions with the VR arm rehabilitation system (9 males, 5 females), (Table 1). The
mean stroke onset was 3.1±2.2 months (range: 1-8). Stroke severity ranged from 3
to 7 (CM). Five of the participants had previous computer experience.
The actual time spent performing arm movement activities on the VR
rehabilitation system was on average 12.6±4.4 minutes per 20-minute session, the
rest of the time being used to provide instructions or waiting for the next activity to
begin. Over the three sessions, all participants improved their performance and
progressed through difficulty levels on all activities, as measured by the overall
session score (Fig. 2).
The mean level of difficulty attained by stroke participants for each of the
unilateral and bilateral arm movement activities, with a performance score of at
least 50%, is shown in Fig. 3. Participants with lower arm impairment (CM 6-7)
were able to attain higher levels on all activities than participants with more severe
arm impairment (CM 3-5).
Over 80% of the stroke participants expressed positive feelings related to the
ease of use of the arm rehabilitation VR system (Fig. 4). They found it easy to use
and operate, clear and flexible. Most reported they would use it if it were available
at their home or in the clinic. Results of the Short Feedback Questionnaire were
likewise very positive (Fig. 5). Over 80% of participants enjoyed the experience,
felt present in the activities, felt that the level of difficulty was adequate and
experienced no discomfort.

4 Discussion and Conclusion

Results indicate that all 14 stroke participants were able to progress in their
performance over the three practice sessions. Answers to the questionnaires
revealed that over 80% of the participants enjoyed the activities provided by the
VR system and found them easy to use. This data allows us to establish a
preliminary mapping between the arm impairment level, as measured by the CM
Scale, and the difficulty level that patients were able to attain in each of the
activities. This mapping will eventually provide guidelines for prescription of the
UL training using the VR system by clinicians. Clinicians will be able to set precise
goals for their patients as they will have a better idea of what difficulty level can be
expected. Note that initial practice is necessary in order to become familiar with
each activity and to understand the arm movements that are required. Knowing the
relationship between difficulty of an activity and arm impairment will allow
patients to quickly reach their optimal training level, instead of trying each level in
turn, which takes more time.
One limitation of this study is that so far we have only collected data from two
patients with a CM score of less than five. Our aim is to collect additional data
from patients with more severe arm impairment in order to generate complete
Towards Establishing Clinical Guidelines 269

guidelines. Once the dataset is complete, we will perform a regression analysis of


the difficulty level attained by each participant against their CM score and
demographic data (age, gender, previous computer experience, etc.). If this
regression is significant, then we will be able to predict an appropriate difficulty
level for the activities in the Jintronix VR system for stroke patients, depending on
their arm function level. This can be then used as guidelines when treating new
stroke patients with this system. Future work is necessary in order to evaluate the
effects of the VR activities on arm function. Specifically, we aim to compare the
effects of practicing the VR activities to that of a home exercise program, in a
group of chronic stroke patients.

Acknowledgment. This study was funded by Grand Challenges Canada. The authors
would like to thank Jintronix for their collaboration, as well as Alejandro Hernandez and
Tanya Tripathi for their help with data collection.

References
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clinical trial. JAMA 296(17), 2095–2104 (2006)
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(2003)
Modulatory Effect on Spinal and Supraspinal
Responses during Cognitive Attentional
and Distraction Tasks

Federico Gabriel Arguissain, José Alberto Biurrun Manresa,


Carsten Dahl Mørch, and Ole Kæseler Andersen

Center for Sensory-Motor Interaction, Aalborg University, Aalborg, Denmark


{fga,jbiurrun,cdahl,oka}@hst.aau.dk

Abstract. The aim of the present study was to investigate the influence of
modulatory mechanisms on spinal and supraspinal responses triggered by changes
in the cognitive state. Simultaneous nociceptive withdrawal reflex (NWR) and
somatosensory evoked potentials (SEP) in response to electrical stimuli were
acquired during two attentional tasks: attention to the stimuli vs. attention to a
cognitive task (modified Stroop test). Single-trial SEP peaks (N1, N2 and P2) and
NWR root-mean-squared (NWR RMS) were obtained for both experimental
conditions. The present results showed larger N1 (p<0.007), lower P2 (p<0.001)
and larger NWR RMS (p<0.001) during the Stroop task compared to when the
subjects paid attention to the stimulus. This mechanism could be thought as a
protective system that increases the responsiveness of the NWR, in order to react
under the minimum risk of tissue damage when the brain is distracted by
demanding cognitive tasks. The present methodology could be potentially used for
assessment of motor learning.

1 Introduction

There is an increasing amount of evidence sustaining that the spinal cord presents
activity-dependent plasticity in health and disease [1], [2]. Descending and
peripheral inputs can produce changes in the synaptic and neuronal properties of
the components included in the spinal reflex pathways. Thus, spinal reflexes have
been subject of extensive research in the past years and used as a tool for the
evaluation of therapeutic methods to restore motor function [3].
One of the primary measurements to study spinal cord function is the
nociceptive withdrawal reflex (NWR) [4]. The NWR is a spinal polysynaptic
reflex to noxious stimuli that evokes a defensive motor response by integrating
sensory input, ongoing motor commands and descending modulatory signals [5].
This reflex has been shown to be strongly modulated during the gait cycle [6], and
several findings suggest that it can be influenced by the brain [5]. The fact that the
NWR can be modulated by both afferent and descending inputs makes it an
interesting tool for assessing motor learning [7]. Nevertheless, its polysynaptic

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 271
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_46, © Springer International Publishing Switzerland 2014
272 F.G. Arguissain et al.

nature also makes it challenging to identify the source(s) of modulation. For that
purpose, research tools that might allow evaluating the state of supraspinal centers
are of interest.
In humans, one possible way to study concurrent spinal and supraspinal
processes is by simultaneously recording the NWR and scalp somatosensory
evoked potentials (SEPs) in response to noxious stimuli. SEPs are transient brain
responses in the ongoing electroencephalogram (EEG), elicited by a sensory
stimulus. SEPS are largely known to be influenced by cognitive and emotional
factors [8], [9], and evidence supports the idea that SEPs reflect the processes
underlying detection and orientation of attention toward the eliciting stimulus
[10].
The aim of the present study was to investigate the influence of modulatory
mechanisms on simultaneous spinal and supraspinal responses triggered by
changes in the cognitive state. To that end, NWR and SEP signals in response to
electrical stimuli were acquired during attention tasks. Single-trial analysis of
these responses was performed in order to determine differences related to two
experimental conditions: attention to the stimuli vs. attention to a cognitive task
(Stroop test [11]).

2 Methods

2.1 Subjects
Thirteen healthy volunteers (six women and seven men, age range 19-40 yrs) with
no previous neurological diseases participated in the experiment. Prior to
participating, all volunteers were informed about the protocol and provided written
informed consent. The study was approved by the local ethics committee
(N20110027).

2.2 Electrical Stimulation


In order to evoke the NWR and SEPs, electrical stimulation was applied through
two surface electrodes in the right foot. One electrode was placed on the arc of the
sole of the foot, while the other electrode pad was placed at the foot dorsum. The
stimulus consisted of a brief constant current burst (25 ms) of 5 square-wave
pulses, delivered by a computer-controlled electrical stimulator. The subjects felt
the bursts as single stimuli.
After a full explanation of the procedure, NWR threshold (RTh) was obtained
using a staircase method. The stimulus intensity was defined as 1.5 x RTh and kept
through the entire experiment.
Modulatory Effect on Spinal and Supraspinal Responses 273

2.3 Electrophysiological Recordings


The NWR was measured by surface electromyography (EMG) of the tibialis
anterior muscle (front of the leg). Two electrodes were placed in the muscle belly
to record its activation.
Continuous EEG signals were recorded using a 32-electrode cap based on the
International 10-20 system. SEP responses are the transient responses in the EEG
which are time-locked to the stimulus. All signals (EEG and NWR) were sampled
at 4 kHz and stored for offline processing. Only the channel at the vertex of the
head (Cz) is reported here.

2.4 Cognitive Tasks


Two cognitive tasks were performed by the participants during the stimulation
blocks: Stroop and Attention. Distraction from stimulation was performed by a
modified version of the Stroop test. Four randomized color names were displayed
iteratively on a 15.6” screen every 2±0.5 s in front of the participant. The text
color matched the written word 50% of the times and 50% it did not. Participants
were asked to concentrate only on the color of the displayed word. Electrical
stimulation was applied every 4-6 words, giving an inter-stimulus interval of 8-12
seconds approximately. Stimuli were applied prior the presentation of the
subsequent word with 1-1.5 s of difference. In 5% of the trials subjects had to
answer by clicking on a keyboard the first letter of the text color being shown.
During these trials the word “answer” was shown right after the color name
disappear in order to notify the participant to respond. In the attention to stimulus
condition, subjects were asked to focus on the stimulated foot and to count the
stimuli that they perceived. Subjects were asked randomly during the stimulation
block to report the count. Electrical stimulation was applied every 8-12 s.
The experiment consisted of one single session divided into six blocks, with
three blocks for each experimental condition.

2.5 Data Analysis


Continuous EMG signals were filtered (bandpass, 5-500 Hz, notch 50 Hz),
rectified and further cut into epochs of 700 ms (-200, 500 ms). Single-trial root-
mean-squared (RMS) values were calculated in the 60-180 ms post-stimulus
interval. This time window was selected due to the velocity of the nerve fibers
involved in the reflex [5].
Continuous EEG data were filtered (band-pass 0.5-100 Hz, notch 50 Hz) and
further cut into epochs of 700 ms (-200, 500 ms). Single-trial SEP peaks were
obtained using an algorithm based on the derivative of the signal and classification
using fuzzy logic, based on [12]. First, the mean SEP signals were visually
inspected and the three characteristic SEP peaks were measured as previously
described in literature [13]: a first negative peak (N1) at approximately 90 ms,
274 F.G. Arguissain et al.

followed by second negative deflection (N2) around 140 ms and a wave, with a
maximum at 250 ms (P2). After manual examination, three fuzzy zones were
assigned to each peak. Each fuzzy zone was determined by a central latency with
two boundaries. The center of each fuzzy zone and its limits were given by the
grand mean latency ± 2 standard deviations of the manually determined peaks.
Afterwards, automatic single-trial detection was performed by finding all the
peaks where the first derivative of the single- trial SEP signal was zero. Each
found peak was weighted with the product of their amplitude with a weight given
by the fuzzy zone that included it.

2.6 Statistical Analysis


Mixed-model analysis of variance (mixed-model ANOVA) was used to analyze
the effect of “condition” on the SEP peaks and the NWR responses. P-values
<0.05 were considered as significant.

3 Results

The boundaries for the fuzzy zones and consequently the single-trial peak detection
were: 94.2 ±2×9.2 ms for N1, 143.4 ±2×22.3 ms for N2 and 263.5±2×36.7 ms for
P2. Fig. 1 shows the single-trial SEP detection for a representative subject in the
“attention” condition, were the variability of the single-trial responses can be
observed compared to the average response.
There was a significant main effect of the condition on the amplitude of the SEP
at the Cz channel, with larger N1 peaks (more negative) (p<0.007) and smaller P2
peaks (less positive) (p<0.001) during the Stroop test compared to when subjects
were focused on the stimulation (Fig. 2).
There was a significant main effect of the condition on the amplitude of the
NWR, with higher amplitude values during the Stroop test (p<0.001) (Fig. 3).

4 Discussion

In this study, the P2 wave was decreased when subjects were performing the
Stroop, which goes in line with previous findings that have shown a smaller P2
under attentional demanding tasks [8], [14], [15]. The P2 peak has been
consistently associated with engagement of attention to the stimulus [10].
Therefore, the Stroop test seems to effectively distract the subject from the stimulus
and this effect is clearly reflected in the observed reduction of the P2 of the SEPs.
The N1 was significantly larger during the Stroop task compared to the attention
condition. There are indications that the N1component can also be modulated by
attention, but it presents lower sensitivity than the observed effects on the N2-P2
complex [16].
Modulatory Effect on Spinall and Supraspinal Responses 2775

Fig. 1 Average SEP signal an nd single-trial peak detection from a representative subject. Thhe
colored dots indicate the sing
gle-trial values for N1, N2 and P2 peaks.

Fig. 2 Effect of experimen ntal factor “condition” (attention vs. Stroop task) on the SE
EP
peaks at Cz channel. Asterisk
ks indicate significant differences (p<0.05).
276 F.G. Arguissain et aal.

Fig. 3 Effect of experimenttal factor “condition” (attention vs. Stroop task) on the NW
WR
RMS. Asterisk indicate signiificant differences (p<0.05)

The present results sh how that when subjects were focused in the Stroop, thhe
reflex responses were high her than when they pay attention to the stimulus.
It is possible that thee lack of inhibition observed in the NWR during thhe
distraction task in the preesent study is the result of descending modulatory contrrol
over the excitability of dorsal horn neurons involved in the reflex arc. Thhis
mechanism might serv ve as an enhancement of nocifensive excitability
advantageous for survivaal in situations where the attention is focused in another
task.
The methodology pressented here allows probing the interaction between thhe
spinal cord and the braiin during somatosensory processing. The possibility oof
modulating both spinal anda supraspinal responses possesses a great potential foor
the assessment of motor leearning.

Acknowledgment. The auth


hors thank Giandomenico Iannetti for his collaboration in thhis
study.

References
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Modulatory Effect on Spinal and Supraspinal Responses 277

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Equivalent Bilateral Early Latency Cutaneous
Reflex Amplitudes during Graded Contractions
in Right Handers

Trevor S. Barss, Taryn Klarner, and E. Paul Zehr

University of Victoria, Rehabilitation Neuroscience Laboratory,


The Centre for Biomedical Research,
and
The International Collaboration on Repair Discoveries,
British Columbia, Canada
{tsbarss,tklarner,pzehr}@uvic.ca
www.rehabneurolab.ca

Abstract. Functional asymmetries exist in right handers due to


asymmetries at multiple levels of the nervous system. Spinally-mediated
contributions have been assessed using the Hoffmann reflex but have
provided varying results. The purpose of this paper was to explore possible
spinally-mediated contributions from cutaneous receptors to the asymmetry in
strength seen in right handed individuals. Asymmetries were assessed by
maximal voluntary contraction force during wrist flexion, extension, and
handgrip. Peak muscle activation (EMGmax) was measured in the flexor
(FCR) and extensor (ECR) carpi radialis and normalized to the maximal
evoked motor responses (M-Max) elicited via median (MED) or radial
nerve stimulation applied proximal to the elbow joint. Cutaneous reflexes
were evoked by trains of stimulation (5x1ms @ 300Hz) delivered to the
superficial radial (SR) or MED at the wrist during graded ipsilateral wrist
extension contractions of 5, 10, 25, and 50% EMGmax. Results indicate that
asymmetries exist for both strength and maximal muscle activation
normalized to M-Max. Early latency (50 – 70 ms) cutaneous reflex
amplitudes are larger on the dominant (right) side. However, when
normalized to background EMG these differences disappear. Thus, when
considering the same relative input, cutaneous afferent pathways have
similar bilateral effects during ongoing muscle activity.

1 Introduction
Functional asymmetries in the human upper limb (generally described as
“handedness”) have been extensively explored due to our reliance on
manipulating objects in our environment. For most tasks, one hand plays a
manipulative role while the other hand usually plays a stabilizing role [1].

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 279
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_47, © Springer International Publishing Switzerland 2014
280 T.S. Barss, T. Klarner, and E.P. Zehr

In right handers, an asymmetry of strength for a grip task has been


consistently shown [2]. These asymmetries exist due to asymmetries at
multiple levels of the nervous system. Specific cortical areas including both
motor [3,4] and somatosensory areas [5,6] have been implicated as
contributing to this effect. As well, a general enhancement of motor unit
discharge synchronization has been observed in the dominant right wrist
extensors of right handed individuals [7]. Spinally mediated contributions
have been assessed using the Hoffmann (H-) reflex but have provided mixed
results and the data does not clearly distinguish between spinal and
supraspinal influences [8,9]. Tactile feedback plays a critical role in maximal
force production [10] and agonist- antagonist co-activation [11] which could
potentially contribute to the functional asymmetries present in the majority
of right handers. Therefore, the purpose of this paper was to explore
possible spinally mediated contributions from the cutaneous receptors in the
skin to the asymmetry in strength seen in right handers.

2 Methods

2.1 Participants
A sample of 25 participants (8 men and 16 women), aged 18-42
completed this study. All participants were strongly right handed (+16.4 ±
3.2 on the Waterloo Handedness Questionnaire, scale range from -20 to
+20). Participants provided informed written consent to a protocol
approved by the University of Victoria Human Research Ethics Committee
and performed according to the Declaration of Helsinki.

2.2 Experimental Design


The study used a within-subject cross-sectional design with all participants
completing the measurements in a single session. Maximal voluntary
isometric contractions (MVCs) of wrist extension, wrist flexion, and grip
strength were assessed. During these contractions, maximal surface
electromyographic muscle activation (EMGmax) was assessed in the
extensor carpi radialis (ECR) and flexor carpi radialis (FCR). Maximally
evoked motor responses were recorded in the ECR and FCR by supramaximal
stimulation of the median and radial nerves, respectively. As well, early
latency (50 – 70 ms) cutaneous reflexes were evoked with trains of
stimulation (5 x 1.0 ms pulses @300 Hz) to the superficial radial (SR) and
median (MED) nerves during graded ipsilateral contractions. All measures
were assessed bilaterally during separate trials.
Equivalent Bilateral Early Latency Cutaneous Reflex Amplitudes 281

2.3 Procedures
2.3.1 Strength and Electromyography
Participants were seated in a custom-fitted chair designed to minimize wrist,
elbow, and shoulder movement with elbow and shoulder angles maintained
throughout the experimental protocol. Maximal voluntary isometric wrist
flexion and extension force was assessed using a Gamma Sensor 6-axis force
transducer (ATI Industrial Automation, Model FT06598, Apex, USA).
Handgrip force (kg) was assessed by a grip strength dynamometer (Takei
Scientific Instruments Co., Ltd, Japan). Participants completed 3 MVCs
which were held for 3 seconds and separated by 1 minute of rest.

Maximal Voluntary Contractions

90
80
*
70
60
50
40
*
30
20
10
0
Handgrip (kg) Extension (Nm) Flexion (Nm)

Fig. 1 Isometric strength in the dominant (black) and non-dominant (white) forearms
including wrist extension and flexion. * Dominant significantly greater than non-dominant
(p<0.05). Values are mean ±SE.

During the MVCs, EMG was recorded using surface electrodes applied
in bipolar configuration over the ECR and FCR. EMG signals were
amplified (GRASS P511, AstroMed) and band pass filtered from 100 to 300
Hz. The output was sent to the A/D interface (National Instruments, Austin,
TX), and sampled at 1000 Hz. The mean absolute value (MAV) of a 0.5
second window centred around peak force was calculated to determine the
maximal muscle activity (EMGmax). The skin surface was shaved and
cleaned adequately before placing the electrodes. Resting muscle signals
were checked for noise and where appropriate, the skin was cleaned and the
electrodes were repositioned. The contraction with the highest peak force
was used for comparison of both force and EMG.

2.3.2 Maximal Evoked Motor Responses and Cutaneous Reflexes


During the maximal evoked motor responses (Mmax) bipolar stimulation
(1 ms pulses) was delivered randomly every 2 – 4 s using a Grass S88
stimulator connected to a SIU5 isolation unit and a CCU1 constant current
unit (AstroMed Grass, Inc.). Stimulating electrodes were placed over the
median nerve (for FCR) or radial nerve (for ECR). Peak-to-peak amplitudes of
282 T.S. Barss, T. Klarner, and E.P. Zehr

Mmax were calculated offline from the unrectified sweeps of EMG with
custom-written software (Matlab, Nantick).
Finally, early latency cutaneous reflex amplitudes were evaluated in the
FCR and ECR by providing trains of stimulation to the median (MED) and
superficial radial (SR) nerves at the wrist of both the dominant and non-
dominant wrist during separate trials. The stimulation intensity used to elicit
cutaneous reflexes was 3 times the radiating threshold. While the stimulation
intensity remained unchanged the participants performed 4 separate trials of
graded ipsilateral wrist extensor contractions at 5, 10, 25, and 50% of
EMGmax. Participants were provided with visual feedback throughout each
trial in order to maintain contraction level.

2.4 Statistical Analyses


Paired samples t-tests directly compared the force output and EMGmax
(normalized to M-Max) in the dominant right forearm against the non-
dominant left forearm. Differences in subtracted reflex amplitude of the
evoked cutaneous reflexes were assessed via a 2 (Limb: Dominant Vs Non-
dominant) x 4 (Contraction intensity: 5, 10, 25, 50%) repeated measures
ANOVA. Significant interactions were followed by paired samples t-tests.
Significance was accepted at p ≤ 0.05. All values are expressed as
mean±SD.

3 Results

The results of the paired samples t-tests, which are presented in Figure 1,
indicate the force output of the dominant right limb is significantly higher
than the non- dominant limb for both handgrip (Dom: 37.6±13.4 kg vs. Non-
Dom: 35.8±11.7 kg; p = 0.017) and wrist extension (Dom: 74.5±31.6 Nm
vs. Non-Dom: 66.3±24.8 Nm; p=0.002). While a similar trend exists for
wrist flexion there was no significant difference in force output between the
dominant and non-dominant limb (Dom: 81.2±32.4 Nm vs. Non-
Dom:75.6±29.9 Nm; p=0.084).
During the MVCs the results of the paired samples t- tests, which are
presented in Figure 2, indicate significantly higher muscle activation
normalized to M-max in the dominant right ECR during wrist extension
(Dom: 8.6±3.3 vs. Non-Dom: 7.3±4.1; p=0.019) as well as in the dominant
right FCR during wrist flexion (Dom: 7.4±3.3 vs. Non- Dom: 5.9±2.9;
p=0.030). Similar muscle activation in both the FCR (Dom: 4.0±2.2 vs. Non-
Dom: 4.6±2.3; p=0.125) and ECR (Dom: 7.6±4.0 vs. Non-Dom: 7.3±3.3;
p= 0.675 occurred during handgrip contractions.
Equivalent Bilateral Early Latency Cutaneous Reflex Amplitudes 283

Fig. 2 Muscle activation in both the ECR and FCR normalized to Mmax. * Dominant
significantly greater than non-dominant (p<0.05). Values are mean.± SE.

Cutaneous reflexes were measured during graded ipsilateral contractions


of the ECR and are presented in Figure 3. The omnibus ANOVA for early
latency subtracted reflex amplitude in the ECR with SR nerve stimulation
revealed a significant limb x contraction intensity interaction (F[3,72] =
4.469, p=0.006). Post hoc paired t-tests revealed a significant difference
between the right and left subtracted reflex amplitudes at each of the
contraction intensities (p<0.05). However, when these values were
normalized to background EMG activity to account for differences in
284 T.S. Barss, T. Klarner, and E.P. Zehr

Fig. 3 A. Early latency subtracted reflex amplitude in the ECR for stimulation at the SR
nerve. B. Early latency subtracted reflex amplitude normalized to background muscle
activity in the ECR for stimulation at the SR nerve. *Dominant significantly different than
non-dominant (p<0.05). Values are mean ±SE.

descending drive, no significant interactions or main effects occurred between


limbs or contraction intensities (p>0.05). There was no difference in either
reflex latency (Dom: 60.8±0.5 ms vs. Non-Dom: 61.6±1.6 ms) or
stimulation intensity (Dom: 4.1±1.0 mv vs. Non-Dom: 4.0±1.1 mv) for MED
nerve stimulation. Also, there was no difference in latency (Dom: 55.0±0.8
ms vs. Non-Dom 54.7±1.2 ms) or stimulation intensity (Dom: 4.5±0.8 mV vs.
Non-Dom: 4.4±0.8 mV).

4 Discussion

The purpose of this paper was to explore if an asymmetry in spinally


mediated contributions from the cutaneous receptors in the skin existed in
strength tasks of right handed individuals. The results of this study indicate
that when descending input is accounted for cutaneous afferents from the skin
appear to have a similar influence bilaterally during ongoing muscle activity.
Previous studies have shown asymmetries in the motor and somatosensory
cortex. However, there have been limited attempts to address whether there
are asymmetries in spinal motor or sensory pathways.
Equivalent Bilateral Early Latency Cutaneous Reflex Amplitudes 285

Initial attempts to assess spinal level asymmetries were made by assessing


H reflex recovery curves [8]. In right handers it was found that the H-reflex
recovery curve from the right leg was significantly lower than that from the
left leg. However, it is not possible to determine leg dominance directly from
hand preference of participants. As well, the time intervals in the recovery
curve ranged from 40 – 1000 ms and could have influences from multiple
levels of the nervous system. A follow up study by a different group
assessed the same variable but with time intervals ranging only from 40 –
100 ms. They found no difference in the recovery ability of the H-reflex
between the dominant and non-dominant side [9]. A recent study assessed
motor neuron synchronization as a means of investigating synaptic
connectivity in the dominant and non-dominant ECR. It was found that the
percentage of synchronized motor unit pairs was significantly higher in the
dominant arm with synchronization peaks being significantly larger and
broader than the non-dominant arm. It was concluded that an enhancement
of the efficiency of the motor neurons common inputs as well as presynaptic
synchronization of motor neuron inputs [7].

Fig. 4 Early latency subtracted reflex amplitude in the FCR for stimulation at the MED
nerve. B. Early latency subtracted reflex amplitude normalized to background muscle
activity in the FCR for stimulation at the MED nerve. Values are mean ±SE.
286 T.S. Barss, T. Klarner, and E.P. Zehr

In the current investigation the cutaneous reflex analysis was limited to


early latency responses to reduce the possible influences from long loop
supraspinal influences. Our results indicate that in the ECR, at a given
percentage of EMGmax, the early latency reflex amplitude is larger on the
dominant right side in right handed people. As well, there is a linear
relationship between the percentage of contraction and the subtracted reflex
amplitude (Fig. 3). With no difference in the stimulation intensity delivered
and this linear relationship very clear it was necessary to normalize the
subtracted reflex amplitude. When the reflex amplitude was normalized the
background EMG activity during each contraction the asymmetries were no
longer present. Although not highlighted throughout the manuscript the
cutaneous reflex amplitudes were also normalized to M-Max and showed
the same results as normalizing to background EMG activity.
Asymmetries were clearly present for the right handed participants within
this study. The dominant right hand was significantly stronger for both
handgrip and wrist extension which is a confirmation of a number of
previously published studies [2,12,13]. Maximal muscle activation was
significantly higher on the dominant side in the agonist muscle during wrist
flexion and extension. With these EMG measures being normalized to
Mmax, any asymmetries in EMG activity are most likely due to influences
upstream from the motor neuron. Initial findings indicate that early latency
cutaneous sensory information is not relaying information to the motor
neuron differently between the dominant and non- dominant limbs. This
indicates that the cause of the functional asymmetry may lie in an unexplored
spinal pathway or remain housed in the motor and sensory areas of the cortex.

5 Conclusion

In right handers, asymmetries exist for both strength and maximal muscle
activation normalized to Mmax. Absolute early latency reflex amplitudes are
larger on the dominant right side. However, when normalized to Mmax or
background EMG these differences are no longer present which indicates
that with the same relative input, cutaneous afferent pathways have similar
influence during ongoing muscle activity between the dominant right and
non-dominant left limb. Understanding the underlying mechanisms of these
functional asymmetries may allow future researchers to utilize these
pathways when trying to restore symmetry after neurological injuries that
present with asymmetries such as stroke [14].

Acknowledgment. The main support for this research was provided by a Grant-in-
aid of Research (EPZ) and doctoral fellowships (TSB & TK) from the Heart and
Stroke Foundation of Canada (BC & Yukon). Additional funding was provided by
the Natural Sciences and Engineering Research Council of Canada (EPZ & TSB).
Equivalent Bilateral Early Latency Cutaneous Reflex Amplitudes 287

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[2] Bohannon, R.W.: Grip strength: a summary of studies comparing dominant and
nondominant limb measurements. Percept. Mot. Skills 96(3 Pt. 1), 728–730 (2003)
[3] Hammond, G.: Correlates of human handedness in primary motor cortex: a review
and hypothesis. Neurosci. Biobehav. Rev. 26(3), 285–292 (2002)
[4] Amunts, K., Jäncke, L., Mohlberg, H., Steinmetz, H., Zilles, K.: Interhemispheric
asymmetry of the human motor cortex related to handedness and gender.
Neuropsychologia 38(3), 304–312 (2000)
[5] Jung, P., Baumgärtner, U., Bauermann, T., Magerl, W., Gawehn, J., Stoeter, P.,
Treede, R.-D.: Asymmetry in the human primary somatosensory cortex and
handedness. Neuroimage 19(3), 913–923 (2003)
[6] Soros, P., Knecht, S., Imai, T., Gurtler, S., Lutkenhoner, B., Eingelstein, E.B.,
Henningsen, H.: Cortical asymmetries of the human somatosensory hand
representation in right- and left-handers. Peter So. 271, 89–92 (1999)
[7] Schmied, A., Vedel, J.P., Pagni, S.: Human spinal lateralization assessed from
motoneurone synchronization: dependence on handedness and motor unit type. J.
Physiol. 480(Pt. 2), 369–387 (1994)
[8] Tan, U.: Left-right differences in the hoffmann reflex recovery curve associated with
handedness in normal subjects 3, 75–78 (1985)
[9] Nativ, A., Frank, J., Allard, F.: The effect of handedness on spinal and supra-spinal
reflex excitability. Electroencephalogr. Clin. Neurophysiol. 72(2), 157–164 (1989)
[10] Shim, J.K., Karol, S., Kim, Y.-S., Seo, N.J., Kim, Y.H., Kim, Y., Yoon, B.C.: Tactile
feedback plays a critical role in maximum finger force production. J. Biomech. 45(3),
415–420 (2012)
[11] Kim, Y., Shim, J.K., Hong, Y.-K., Lee, S.-H., Yoon, B.C.: Cutaneous sensory
feedback plays a critical role in agonist- antagonist co-activation. Exp. Brain
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[12] Petersen, P., Petrick, M., Connor, H., Conklin, D.: Hand Dominance 43(7), 444–447
(1989)
[13] Ozcan, A., Tulum, Z., Pinar, L., Başkurt, F.: Comparison of pressure pain threshold,
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878 (2004)
[14] Farthing, J.P., Paul Zehr, E.: Restoring Symmetry: Clinical Applications of Cross-
Education. Exerc. Sport Sci. Rev. (February 2014)
The Use of Ecological Sounds in Facilitation
of Tool Use in Apraxia

Marta M.N. Bieńkiewicz, Philipp Gulde,


Andrea Schlegel, and Joachim Hermsdörfer

Technische Universität München, Lehrstuhl für Bewegungswissenschaft,


Georg-Brauchle Ring 60/62, 80992 München, Germany
marta.bienkiewicz@tum.de, p.gulde@gmx.de

Abstract. The CogWatch project (www.cogwatch.eu) aims to create an intelligent


assistance system to improve activities of daily living (ADL) in stroke survivors,
who suffer from impaired ability to use everyday tools (apraxia). This study
explores the use of cues, based on ecological sound linked to the action goal, in
prospective facilitation of tool use in those patients. We hypothesize those patients
with apraxia benefit from supplementary sensory information relevant to the task,
which reinforces the selection of the appropriate motor plan ahead of time. The
aim is to support the development of assistive device that could provide guidance
for the patients during ADL.

Keywords: Apraxia, CVA rehabilitation, ecological sounds.

1 Introduction

Ecoacoustics define environmental sound as an audible product of physical event,


caused by interaction of the materials (i.e. changes in the aerodynamics of
surroundings) [1]. Recent research suggests that motor networks associated with
mirror neurons respond to the action-related sounds [2], [3]. Use of environmental
sounds was previous demonstrated to improve mobility in movement disorders i.e.
Parkinson’s disease [4]. Cerebrovascular accident (CVA) patients with apraxia
suffer from the inability to use tools or perform hand gestures, caused by brain
tissue loss in the left or right hemisphere [5]. Patients are prone to sequence,
conceptual and spatiotemporal errors during ADL that can lead to potential health
and safety issues (e.g., grasping the knife by the sharp edge) [6]. The core of this
symptom lies in the compromised ability to access the appropriate motor program
relevant to the task goal [7]. Patients demonstrate difficulties during the execution
of single and multiple tool use and during the pantomime of the same movement
[5]. So far strategy training approach was found as the most promising approach to
rehabilitation of apraxia and action disorganization disorder [11]. There is lack of
evidence whether sensory cueing can facilitate tool us in those patients in an
immediate fashion if presented prospectively to a patient. The aim of the presented

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 289
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_48, © Springer International Publishing Switzerland 2014
290 M.M.N. Bieńkiewicz et al.

study is to investigate the potential of event-based sounds, compared to picture


sequences and auditory instruction, in improving motor performance in CVA
patients manifesting apraxia.

2 Methods

2.1 Subjects
Until now six CVA patients (with left brain damage) were tested. Patients were
recruited from the Neuropsychology Clinic at the Hospital Bogenhausen in
Munich. Ethical approval was obtained by a local ethics committee.

2.2 Experimental Design


The experimental design involved pantomime and actual tool use in three tasks:
hammering, sawing, and toothbrushing. The practice trial comprised of pouring a
glass of water (to explain differences between different cueing conditions, two
execution modes and familiarize participants with the experimental setup). The
experimental design consisted of four different cueing modes (prior to task
execution): no cues, auditory instruction (step by step commands for each of the
subactions f.e. ‘Pick up the saw’), pictorial instruction (step by step 3rd person
perspective display), and ecological sounds (10s recording of action goal). Each
mode of execution: actual use and pantomime involved two consecutive trials.
Presentation of the experimental conditions was fully randomized using Latin-
squares design.

2.3 Apparatus
The display was controlled via customized software programmed in C#. The
movement data is collected with the use of 5 Qualisys Oqus cameras and analogue
board interface. The sound stimuli were recorded with low-noise condenser Rode
N1 microphone and Yamaha Audiogram 3. Derivate data from motion capture
recordings was analyzed using custom developed MATLAB program.

3 Progress
In the study 6 patients with LBD were tested so far (out of planned 10 patients)
along with age- and sex matched controls. The analysis of this study is in progress.
Preliminary results show potential in facilitation of the tool use with the use of
ecological sound both in the execution and pantomime mode (see Figure 1). In
addition we added clinical scoring of the motor performance based on the video
recording of patients [8].
The Use of Ecological Sounds in Facilitation of Tool Use in Apraxia 291

HAMMERING MOVEMENT

SAWING MOVEMENT

Fig. 1 Summary of patients’ data (n=6) during performance of three tasks in execution and
pantomime mode. The bar plot depicts the frequency of the movement across different
modes of cueing.
292 M.M.N. Bieńkiewicz et al.

TOOTHBRUSHING MOVEMENT

Fig. 1 (continued)

Table 1 Clinical video scoring of performance across two trials

Auditory No Cue Pictures Sound


Mode of
execution M SD M SD M SD M SD

Execution 1.8 0.5 1.6 0.6 1.7 0.5 1.7 0.6

Pantomime 1.2 0.7 1.4 0.7 1.3 0.7 1.4 0.7

M 1.5 1.5 1.5 1.6


Note. M – average, SD – standard deviation

Table 1 illustrates the clinical assessment across two trials for each condition.
The scores were assigned by two independent researchers and averaged. Score 0
illustrates inadequate performance that does not resemble the appropriate handling
of the object or pantomime. Score 1 denotes performance that resembles the
characteristic of the actual tool use, but might be inadequate in terms of plane of
motion, speed or orientation of the tool (or hand posture in pantomime mode).
Score 2 was assigned to accurate performance across the conceptual and
spatiotemporal dimensions. The data collection is ongoing and comparisons with
age-matched controls are pending. Preliminary results show promising
improvement in patients in terms of movement frequency when primed with
sound (see Figure 2).
The Use of Ecological Sounds in Facilitation of Tool Use in Apraxia 293

PATIENT PATIENT HEALTHY CONTROL

Fig. 2 Normalized phase planes (velocity over position/ time) for the apraxic patient
performing a pantomime of hammering in comparison to age-, and sex-matched control
subject. Left panel shows the performance following pictorial instruction. Middle panel
illustrates performance primed with display of ecological sound. Patient suffered CVA in
August 2012; 12 months prior to data collection. Deviation from the circular form
characterizes poor motor control [12].

4 Future Directions

Detailed analysis will be focused on error occurrence [9] classification kinematic


variables noted in the literature as motor features of apraxia [10] such as
movement time, peak velocity, acceleration profile, jerks, path length and ratio of
each path axis and polar variation.

5 Conclusions

The results of this study feed in the development of the CogWatch system. The
aim is to find the most efficient cueing method that would improve the
performance of ADL in stroke survivors. Preliminary results suggest that
environmental sounds might be a promising approach in facilitation of tool use in
apraxia. The work on this line of CogWatch project is in progress and requires
detailed analysis to identify how different sensory information preceding the task
performance impacts patients performance. In addition, the secondary aim is to
identify differences between selected CVA patients that show apraxic behavior
and healthy elderly performance in terms of kinematics and movement
organization.

Acknowledgments. This work was funded by the EU-STREP Project CogWatch (FP7-
ICT- 288912). Authors would like thank to the Klinikum Bogenhausen Munich patients and
staff members for participation in the research and student assistants: Johannes Pflüger,
Anna Voitl and Saskia Steinl for the help with running the experimental sessions.
294 M.M.N. Bieńkiewicz et al.

References
[1] Gaver, W.: How do we hear in the world? Explorations in ecological acoustics.
Ecological Psychology 5(4), 285–313 (1993)
[2] Kohler, E., Keysers, C., Umilta, M., Fogassi, L., Gallese, V., Rizzolatti, G.: Hearing
sounds, understanding actions: action representation in mirror neurons. Science 297,
846–848 (2002)
[3] Ticini, L., Schutz-Bosbach, S., Weiss, C., Casile, A., Waszak, F.: When sounds
become actions: higher-order representation of newly learned action sounds in the
human motor system. Journal of Cognitive Neuroscience 24(2), 464–474 (2013)
[4] Young, W.R., Rodger, M.W.M., Craig, C.M.: Using ecological event-based acoustic
guides to cue gait in Parkinson’s disease patients (abstract). Movement
Disorders 27(suppl. 1), 119 (2012)
[5] Goldenberg, G., Hermsdörfer, J., Glindemann, R., Rorden, C., Karnath, H.:
Pantomime of tool use depends on integrity of left inferior frontal cortex. Cerebral
Cortex 17, 2769–2776 (2007)
[6] Petreska, B., Adriani, M., Blanke, O., Billard, A.: Apraxia: a review. In: von Hofsten,
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Elsevier, Amsterdam (2007)
[7] Hermsdörfer, J., Hentze, S., Goldenberg, G.: Spatial and kinematic features of apraxic
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[8] Goldenberg, G.: Defective imitation of gestures in patients with damage in the left or
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[11] Bienkiewicz, M.M.N., Brandi, M.-L., Goldenberg, G., Hughes, C.M.L., Hermsdörfer,
J.: The tool in the brain: apraxia in ADL. Behavioral and neurological correlates of
apraxia in daily living. Front. Psychol. 5 (2014),
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fpsyg.2014.00353/abstract (accessed April 24, 2014)
[12] Bootsma, R., Fernandez, L., Mottet, D.: Behind Fitts’ law: kinematic patterns in goal-
directed movements. International Journal of Human-Computer Studies 61(6), 811–
821 (2004)
Longitudinal Estimation of Intramuscular
Tibialis Anterior Coherence during Subacute
Spinal Cord Injury: Relationship with
Neurophysiological, Clinical and Functional
Measures*

Elisabeth Bravo-Esteban1,2, Julian Taylor1, Manuel Aleixandre2,


Cristina Simón-Martínez1, Diego Torricelli2, José Luis Pons2,
and Julio Gómez-Soriano1,3
1
Sensorimotor Function Group, Hospital Nacional de Parapléjicos, Toledo, Spain
2
Spanish National Research Council (CSIC), Madrid, Spain
3
Nursing and Physiotherapy School, Castilla La Mancha University, Toledo, Spain

Abstract. Tibialis Anterior (TA) electromyographic coherence estimation is


assumed to reflect common supraspinal descending input spinal motoneurons,
related to corticospinal tract activity. This study documented residual voluntary
motor recovery at 2 week intervals during subacute spinal cord injury (SCI) with
intramuscular TA EMG coherence estimation within the 10-60Hz bandwidth,
assessed during controlled maximal isometric and isokinetic dorsiflexion. Several
clinical and functional lower limb measures (muscular testing, dorsiflexion
maximal voluntary torque and gait function measured with the WISCI II) and
neurophysiological measures (TA motor evoked potentials, MEPs) were also
recorded. Total and TA muscle strength, voluntary torque generation and gait
function improved during subacute SCI, in addition to 40-60Hz, but not 15-30Hz
intramuscular TA coherence. TA MEPs failed to reflect significant recovery of
function. The SCI spasticity syndrome non-specifically reduced 15-30Hz TA
coherence and was detected as high TA coherence values during fast isokinetic
movement in all frequency bands. To conclude, longitudinal assessment of
adaptive and maladaptive motor plasticity during subacute SCI can be detected
with TA EMG coherence estimation during controlled movement, providing
orientative diagnostic information during neurorehabilitation.

Keywords: residual voluntary motor function recovery, muscle coherence, motor


evoked potentials, AIS, modified Ashworth scale, Penn scale, SCATS, subacute
spinal cord injury.

*
This project is funded by the Spanish Ministry of Science and Innovation CONSOLIDER-
INGENIO, project HYPER (Hybrid NeuroProsthetic and NeuroRobotic Devices for
Functional Compensation and Rehabilitation of Motor Disorders, CSD2009-00067).

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 295
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_49, © Springer International Publishing Switzerland 2014
296 E. Bravo-Esteban et al.

1 Introduction

Spinal cord injury (SCI) has a devastating impact on quality of life due to several
degrees of sensorimotor dysfunction [1]. In 52% of SCI cases, subjects are
diagnosed with an incomplete injury [2]. Furthermore the limited recovery of
residual voluntary motor activity present during the subacute phase of
neurorehabilitation may be mediated by mechanisms of neuroplasticity [3].
Neuroplasticity following SCI may include concomitant changes of corticospinal,
extrapyramidal and propriospinal tract function [4]. Unidentified spinal
mechanisms may also mediate motor function recovery during subacute SCI [5].
In parallel, maladaptive motor function may also develop during subacute SCI,
such as spasticity [3]. Furthermore the development of specific motor disorder
symptoms associated with the spasticity syndrome [6-8] may impede the limited
recovery of voluntary motor function and gait mediated by adaptive plasticity of
descending and spinal motor systems [6-8].
Systematic and longitudinal recording of clinical and neurophysiological
variables suggest that mechanisms of neuroplasticity are activated during subacute
SCI [9], although only a few longitudinal studies have been published [10-11]. The
identification of new, comprehensive and sensitive SCI outcome measures should
be targeted to parallel assessment muscle strength, corticospinal tract and gait
function. Muscle coherence activity estimation, a frequency measure of the
similarity of two EMG signals [12], may contribute to this goal. Previous studies
have demonstrated a relationship between EMG coherence estimation with
corticospinal tract function [12-13], voluntary muscle strength and gait function
[14-15]. In addition, muscle coherence has recently been associated with the
development of specific symptoms of the SCI spasticity syndrome [14-15].
The aim of this study was to document residual voluntary motor recovery during
subacute incomplete SCI employing clinical, functional, neurophysiological and
TA muscle coherence estimation to better identify early evidence of adaptive and
maladaptive motor plasticity during neurorehabilitation.

2 Methods
The study was performed following approval by the Local Toledo Hospital Clinical
Ethical Committee (#152) and all recruited subjects were required to sign a consent
form. The longitudinal study was designed to include 4 testing sessions performed
at 2 week intervals. Twenty two subjects with subacute (between 1-8 months after
injury) [8] motor incomplete SCI (American Spinal injury Association (AIS) C or
D), with an injury level between the 2nd cervical to the 12th thoracic vertebrae, were
recruited. Fifteen healthy subjects formed the control group. In subjects with SCI
the recruitment criteria included a Tibialis Anterior (TA) muscle score greater than
2. Patients were diagnosed with the spasticity syndrome and allocated to this
experimental group after study completion if a modified Ashworth score >1 and/or
Penn score ≥1 was diagnosed in 3 out of 4 testing sessions. The exclusion criteria
included musculoskeletal or peripheral nervous system disorders.
Longitudinal Estimation of Intramuscular Tibialis Anterior Coherence 297

2.1 SCI Outcome Measures


Subjects were seated in an isokinetic dynamometer (KinCom, Chattanooga Group
Inc.). The trunk and pelvis were stabilized using straps. The hip, knee and ankle
joints were flexed at 90º. The criteria included a total and TA muscle score greater
than 2, with the subject capable of generating moderate lower limb muscle
contraction levels, which avoided methodological problems associated with the
coherence estimation of non-rectified electromyoggraphic (EMG) signals [16].
The TA muscle was recorded to estimate EMG coherence using double differential
surface electrodes, with a preamplifier gain of 10V/V and an open bandwidth
(Delsys Inc. Signal Conditioning Electrodes 3.1). The electrodes were placed on
two specific locations on the TA muscle belly, and separated by a minimum of 10
cm to avoid electrical cross-talk [17].
TA EMG signals were recorded during two different types of controlled muscle
activation: i) two maximal isometric dorsiflexion (MID) muscle contractions
maintained for 5s, and measured with the dynamometer, ii) ten repetitions of
isokinetic activation at 60º/s and 120º/s, with the ankle joint displaced from 30º
plantarflexion to 0º dorsiflexion.
Clinical and functional tests included: i) gait function measured with the WISCI
II, ii) muscle hypertonia detected during knee and ankle joint during passive flexion
and extension with the modified Ashworth scale in the iii) spasm frequency
quantified with the Penn scale and iv) maximal voluntary torque (MVT) recorded
during maximal isometric dorsiflexion with the dynamometer.
TA motor evoked potentials (MEPs) were also assessed by analysing single
motor evoked potentials following transcraneal magnetic stimulation (TMS)
applied over the primary motor cortex with a Magstim 200 stimulator (Magstim
Rapid 2, Magstim Company Ltd). The double-coned coil was oriented on the skull
to produce an induced current in the posterior-to-anterior direction. Optimal
localization for TMS was determined by varying the position of the coil from the
vertex with gradually increasing intensities, until a MEP in the contralateral TA
muscle was recorded evoked at the lowest stimulation intensity. The subject was
seated with the TA activated at 20% of dorsiflexion MVT. TA MEP threshold was
defined as the stimulus intensity at which five MEPs of 100mV peak-to-peak
amplitude were recorded following ten consecutive stimulus [18].

2.2 EMG Coherence Estimation and Statistical Analysis


EMG signals were recorded with a 10KHz sampling frequency (MicroPlus 1401,
Cambridge Electronic Design) and were subsequently down sampled to 2KHz
using a low pass filter of 700Hz to avoid aliasing (Matlab 7.11). Muscle coherence
activity was calculated with the Signal Processing Toolbox of Matlab 7.11 by
estimating the power spectral densities with Welch’s method [19]. Due to the
methodological requirements of estimating intramuscular TA coherence during
several controlled movement tasks, a minimum EMG signal length of at least 3.5
298 E. Bravo-Esteban et al.

seconds was defined for all movement tasks. The signal was divided into 8 data
segments using 50% overlapping segments performed with a Hamming window
[20]. To obtain the coherence in each frequency band (10-16, 15-30, 24-40 and 40-
60Hz), all the coherence data points within each specific band for each each
movement were averaged to obtain a grand average coherence value for the
specific frequency band for the experimental group. The velocity-dependence of
intramuscular TA coherence was estimated by calculating the ratio of its value
during isokinetic TA muscle movement at 120º/s and at 60º/s.
Statistical analysis was performed with two commercial software packages
(SPSS, version 17.0 and SigmaStat, version 3.1, Systat software, Inc).
Nonparametric analysis was applied to the data following confirmation of the non-
gaussian distribution of the data (Kolmogórov-Smirnoy test). The Mann-Whitney
test was used to compare intramuscular TA coherence values between the control
and SCI groups and also between subjects with and without the spasticity
syndrome. The Friedman test was performed for longitudinal analysis with the
Bonferroni post-test used to identify specific differences among the four sessions.
Statistical significance was defined as p<0.05, with the data presented as median
values with the 25th and 75th percentiles.

3 Results

3.1 40-60Hz TA Coherence Activity, but Not Motor Evoked


Potentials, Increases during Motor Function Recovery
during Subacute SCI
The median time after SCI for session 1 was 12 (7-15) weeks compared to session
4 which was performed at 25 (19-27) weeks. A significant increase in 40-60Hz
intramuscular TA EMG coherence activity was observed during this time window
(Fig. 1A; p=0.03), but not within the 15-30Hz band (Fig. 1B). Longitudinal
recording of TA MEPs following TMS failed to reveal a significant increase in
activity during the follow-up in subjects with SCI (p>0.13).
Clinical and functional measures also revealed recovery of the total muscle score
from session 1 to 4 for TA (3, 3-4 to 4, 4-5) and for the Quadriceps and Hamstrings
muscles (p<0.05) after SCI. Equally dorsiflexion MVT increased from session 3
(114, 89-136 Nm) to session 4 (139, 102-173 Nm, p<0.05). Finally gait function
measured with the WISCI II scale also showed an improvement from session 1 (4,
0-7) to 4 (13, 12-16, p<0.05). Together these clinical and functional measures
indicated a general improvement in voluntary motor function during the follow-up.

3.2 Spasticity Impedes Dorsiflexion MVT Recovery and


Decreases 15-30Hz TA Coherence during Late Subacute SCI
Following SCI those subjects without the spasticity syndrome (n=9) demonstrated
recovery of dorsiflexion MVT from session 1 (87, 65-121 Nm) to session 4 (137,
Longitudinal Estimation of Intramuscular Tibialis Anterior Coherence 299

103-166 Nm, p<0.01). In contrast, no recovery of dorsiflexion MVT was identified


in the SCI spasticity syndrome group compared from session 1 (113, 97-137 Nm)
to session 4 (140, 99-175 Nm, p=0.18).
Finally analysis of those subjects with the SCI spasticity syndrome (n=13)
revealed a general decrease in 15-30Hz TA coherence (p=0.04), but no difference
with the group without the spasticity disorder was observed.

3.3 High Intramuscular TA Coherence Activity Measured at


Fast Isokinetic Movements is Characteristic of the SCI
Spasticity Syndrome

Fig. 1 A. 40-60Hz and B. 15-30Hz TA intramuscular coherence estimated during maximal


isometric dorsiflexion during the four repeated testing sessions in the subacute SCI group.
Dotted line at 0.12 corresponds to the healthy coherence value.
300 E. Bravo-Esteban et al.

During session 4 high TA coherence activity during fast isokinetic activation


was detected in all frequencies bands within the 10-60Hz range in the SCI
spasticity syndrome when compared to the group without this motor disorder.
Calculation of the ratio of TA coherence activity for isokinetic activation at
120/60º/s also demonstrated highTA coherence activity for the SCI spasticity
syndrome group. In contrast no difference was observed for TA coherence and the
battery of clinical and functional measures (muscle testing, WISCI II and TA
MEPs) between the groups with and without the spasticity syndrome during the
initial stage of subacute SCI. Finally a negative correlation was identified between
the grade of lower limb hypertonia (measured as a total modified Ashworth scale
score) and the 40-60Hz TA coherence activity during isokinetics activation at
120º/s (rho=-0.63; p=0.02) as well as the isokinetic 120/60º/s ratio during knee
flexion (rho= -0.70; p= 0.01).

4 Discussion

This study demonstrates recovery of residual voluntary motor function in


individuals with incomplete SCI during subacute rehabilitation based on clinical
and functional measures including total and TA muscle testing, dorsiflexion MVT
and walking index. In parallel an increase in 40-60Hz intramuscular TA coherence
was detected. Mechanisms of adaptive plasticity have been postulated to mediate
the limited recovery of residual voluntary motor function following SCI [4], which
may explain greater neuroplasticity within the subacute phase after injury [21].
Coherence activity within the 40-60Hz band has been associated with non-
pyramidal descending tract function, possibly related to residual activity within
either reticulospinal and/or propriospinal tracts following SCI [22-23]. However
this is the first time that a longitudinal study has identified an increase in 40-60Hz
intramuscular TA coherence during subacute SCI compared to the initial session,
which served as the main control value in this study. No significant recovery of
TA-MEPs was revealed during the follow-up, suggesting that neurophysiological
follow-up of corticospinal tract function using either TMS or 15-30Hz TA
intramuscular coherence is particularly challenging during subacute SCI
rehabilitation.
The pathophysiology of the SCI spasticity syndrome is complex and most
probably involves concomitant changes in pyramidal, extrapyramidal and spinal
motor control mechanisms [23-24]. The presence of the SCI spasticity syndrome
impeded recovery of dorsiflexion MVT and was associated with a general decrease
in 15-30Hz TA intramuscular coherence. These data suggest that the SCI spasticity
syndrome impacts negatively on voluntary motor function, possibly on
corticospinal activity estimated indirectly with intramuscular TA coherence [15].
Previously the severity of evoked spasms and muscle hypertonia in subjects with
SCI revealed a negative correlation with the higher frequency 40-60Hz TA
coherence band [15]. In the present study high TA coherence values estimated
during fast isokinetic movements in subjects with the SCI spasticity syndrome also
Longitudinal Estimation of Intramuscular Tibialis Anterior Coherence 301

suggests that the velocity-dependent component of this motor disorder may also be
detected characterised via the neurophysiological assessment of spinal,
corticospinal and reticulospinal activity following SCI [22-23].

5 Conclusion

Intramuscular TA coherence estimated within the 40-60Hz range during maximal


isometric dorsiflexion increased during subacute SCI, in parallel with clinical and
functional measures of lower limb function, compared to TA-MEP´s or 15-30Hz
coherence activity. These longitudinal data suggest that the application of simple
controlled motor tasks combined with EMG measures have the diagnostic
potential to better assess residual voluntary motor neuroplasticity. However
neurophysiological assessment and the functional implication of 40-60Hz TA
coherence activity as an indirect measure of the subcortical extrapyramidal system
in mediating functional recovery during subacute SCI is required.

Acknowledgments. This project was funded by the Spanish Ministry of Science and
Innovation Consolider-Ingenio Hyper (Hybrid NeuroProsthetic and NeuroRobotic Devices
for Functional Compensation and Rehabilitation of Motor Disorders (CSD2009-00067),
Fundación Mutua Madrileña (2010), Fiscam (PI2010/030) and Pfizer (Liira) project.

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Online Intramuscular EMG
Decomposition with Varying
Number of Active Motor Units

Eric Le Carpentier1 , Yannick Aoustin2 ,


Jonathan Monsifrot2 , and Dario Farina3
1
LUNAM Université, Ecole Centrale de Nantes
and
IRCCyN (UMR CNRS 6597), 1, rue de la Noë, 44321 Nantes, France
{Eric.Le-Carpentier,Yannick.Aoustin,
Jonathan.Monsifrot}@irccyn.ec-nantes.fr
2
LUNAM Université, Université de Nantes
and
IRCCyN (UMR CNRS 6597),
1, rue de la Noë, 44321 Nantes, France
3
Department of Neurorehabilitation Engineering, Bernstein Center for
Computational Neuroscience, University Medical Center Göttingen
Georg-August University, Von-Siebold-Str. 4, 37075 Göttingen, Germany
dario.farina@bccn.uni-goettingen.de

Abstract. This paper deals with the online decomposition of intramuscu-


lar electromyographic (iEMG) signals. A Markov model is proposed, which
takes into account a varying number of firing motor neurons. A Bayes filter
detects online the firing motor units by using a dictionary of approximated
motor unit action potentials waveforms, and estimates precisely the action
potential shapes and the respective firing rates. The method was tested on
both simulated and experimental signals.

1 Introduction
The idea to control active prosthetic devices for amputees through surface
electromyographic (EMG) signals was proposed by N. Wiener in [1]. Cur-
rently it is an active field of research, see [2]. Akazawa et al [3] estimated the
force level and mechanical impedance of limb motion through EMG signals.
A multiple neural network is proposed by Tsukamoto et al [4] to determine
the movement intended by an amputee from surface electromyographic sig-
nals. However, most previous works were devoted to control only a particular
joint depending on the torque estimated from EMG signals, see [5], [3]. There
is an extreme variability in the collected signal between users and within the
user himself, and, the long training of the decoding system, see [6]. The ob-
tained movements of the prosthetic are not fluent, and precise manipulation

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 303
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_50,  c Springer International Publishing Switzerland 2014
304 E. Le Carpentier et al.

and power grasping of heavy object is not currently possible [7]. These tasks
are achieved by a combination of a large number of degrees of freedom. Cur-
rent commercial prosthetic hands are unable to provide enough grasping or
manipulation functionality. However, recent works promote the use of intra-
muscular EMG (iEMG) signals [8] to reach this objective.
We believe that the information on the activity of individual motor neurons
will help to improve the control of prosthetic hands, although this approach is
more challenging than classic methods that use the EMG as a compound sig-
nal. Electromyographic (EMG) signals represent the activity of muscle fibers,
as driven by the population of spinal motor neurons (MN) innervating the
muscle. Thus, despite being measured peripherally, EMG signals reflect neu-
ral activity since they contain information on the activation drive sent from
the spinal cord to the muscles (neural drive to the muscles). The identifica-
tion of individual MN spikes from the EMG signal is called EMG decompo-
sition [9]. To allow physiological investigations of motor unit (MU) behavior
during muscle contractions, decomposition methods for (iEMG), have been
developed, see [10], [11], [12], or [13]. Through theses investigations applied
off-line, including the interaction of an expert operator to optimize the accu-
racy of the result, the neural strategies for movement control are decoded. In
[14] a decomposition method, which could be potentially implemented online,
is proposed. It is based on a new sequential algorithm for the EMG decom-
position that allows full decomposition in a sequential way. This method
processes a single-channel iEMG signal sequentially. The iEMG signals are
modeled as a sum of independent convolved spike trains. The recording of
a whole sequence of spike trains is not necessary to compute the estimates
of the parameters of the model. The sparsity and the regularity of the spike
trains is taken into account by a stochastic model for the time between two
spikes of the same train, based on a discrete Weibull distribution [15]. Then,
an online estimation method for the parameters of the Weibull distribution
and of the motor unit action potentials (MUAP) shapes is implemented.
This paper extends the original contribution [14], in which the number of
firing motor neurons was supposed to be fixed and known.

2 Methods

2.1 Basic Hypotheses


An iEMG signal is an electrical signature of muscle activity, i.e. activity of
muscle fibers. As remarked in [16, 17], the property of the linearity of the
sum of electrical signals justifies modeling the observed signal Y as a sum of
filtered spike trains embedded in a noise W ; for all discrete time indexes n:


nm [n]
Y [n] = (hi ∗ Ui )[n] + W [n] (1)
i=1
Online Intramuscular EMG Decomposition 305

For each source, a time-invariant linear filtering effect is considered. It appears


as a convolution between the input spike train Ui and an impulse response
hi :
• the spike trains Ui are sparse 0-1 processes which firing rates are linked to
the muscle activity;
• the shapes of the impulse responses hi represent the MUAP and are as-
sumed time-invariant.
In a probabilistic framework, the spike train sequences and the noise sequence
are stochastic processes. They are supposed mutually independent. The noise
is assumed independent along time, zero-mean, gaussian, with constant vari-
ance v. The spike trains Ui are not available. The impulse responses hi are
assumed of finite length with known maximum length ir . The noise variance
v is unknown. A dictionary of rough shapes of all possible wavelets hi is nec-
essary, but the nm [n] motor neurons for which discrete time n belongs to a
firing epoch are unknown.
From this convolution model, we aim to derive an hidden Markov model
(HMM), whose state will be representative of the process: active motor neu-
rons, MUAP shapes, firing rates. Then, Bayesian filtering will estimate online
the model state.

2.2 Hidden Markov Model


For each input source Ui , in a firing epoch, interspike intervals Δi [k] - discrete
time length between spikes, k ∈ Z being the spike index - are supposed to
be independent and identically distributed (i.i.d.) random variables, with a
parameterized probability mass function (PMF) defined by Pr(Δi [k] = t|Θi ),
for all positive natural numbers t ≥ 1, where Θi is an unknown parameter
vector (which will be considered as random in the Bayesian framework below).
For each source, we introduce the sawtooth sequence Ti [n], which corre-
sponds to the time interval since the last spike. The value Ti [n] is incremented
at each time index, unless the MN fires; it is then set to zero:

0 if the MN fires at time n + 1
Ti [n + 1] = (2)
Ti [n] + 1 otherwise

By means of the Kronecker delta, the spike trains write:

Ui [n] = δ (Ti [n])

Let us use the exponent n to denote a time span till time n (e.g. Tin =
(Ti [j])1≤j≤n ). Then, under the assumption that the sequence of interspike
intervals is i.i.d., it is shown in [14] that the sequence Ti [n] is Markovian; for
all possible time spans t (positive integer valued) since the last spike:
306 E. Le Carpentier et al.

Pr(Ti [n + 1] = t|Tin , Θi ) = Pr(Ti [n + 1] = t|Ti [n], Θi ) (3)

As shown in [14], choosing a discrete Weibull distribution for the interspike


interval (with 2 parameters: a location one, and a concentration one), this
transition probability and the firing rate (that is 1/E{Δi [k]|Θi }) are easy to
calculate.
The state of the hidden Markov model contains the set of the indexes of
active motor neurons picked in the dictionary of all possible MNs (sources),
with their associated sojourn times and Weibull parameters, that is, for all
n ≥ 1:
• A[n], the set of the nm [n] active sources;
• T[n] = [Ti [n]]i∈A[n] , concatenation of the nm [n] sojourn times (column vec-
tor with value in Nnm [n] );
• Θ[n], concatenation of the nm [n] parameters Θi of the Weibull distribu-
tions (column vector with value in R2nm [n] ;
• H[n], concatenation of the coefficients of the MUAP (column vector with
value in Nir nm [n] );
Note that the size of the state is time-varying. The set A[n] is the set of idle
motor neurons indexes in the dictionary.
The transition law from time n to time n + 1 is built as a birth and death
process, with the help of 2 tuning parameters ti and λ:
• if some sojourn times reach a maximum time ti , the corresponding motor
neuron indexes are dropped from A[n + 1];
• otherwise, an inactive motor unit is picked at random in the dictionary and
added in A[n + 1] with probability λ (that is to say, there is no activation
with probability 1 − λ).
The Weibull parameters and the MUAP shapes are assumed constant, the
sojourn time evolves thanks to transition (2), if the corresponding motor
neuron is kept in the transition above.
The observation equation, which is equivalent to the representation (1),
becomes:  
Y [n] = ϕT1 [n] . . . ϕTnm [n] H + W [n] (4)
 
ψ T[n]
where ϕt is a row vector of size ir that all components are 0, except, if
t < ir , the component in position t + 1 that has value 1.

2.3 Bayes Filtering


The purpose of a Bayes filter is to propagate along time the posterior proba-
bility law of the state sequence of a HMM. Using calculations similar to those
found in [14], we can derive recursions:
Online Intramuscular EMG Decomposition 307

• on posterior probability density functions of continuous-valued variable


H[n], given A[n] and T[n]; note that this is nothing but a rigorous imple-
mentation of the well known Kalman filter;
• on posterior probability density functions of continuous-valued variable
Θ[n], given A[n] and T[n], by means of a reasonable approximation;
• on posterior probability of all possible values of discrete-valued variables
(A[n], T[n]).
At each step n, the paths (A[n], T[n]) are extended thanks to the birth and
death process described above. Obviously, it is impossible to process all pos-
sible values of (A[n], T[n]), since their number increases exponentially as time
index n grows. Only the npath most probable sequences will be kept, the num-
ber npath being a parameter of the method similar to the number of particles
in a particle filter [18].
For all MNs in the dictionary, the MUAP shape in the dictionary is cor-
rected using the Minimum Mean Square Error (MMSE) estimate obtained
as a weighted mean value among the npath state estimators linked to a path
containing this motor neuron index (the weight being the posterior probabil-
ity of the path). The same principle is used to obtain the current estimation
of the Weibull parameters.
Note that a forgetting factor is implemented to track slow variations in
MUAP shapes and Weibull parameters, so that the filter becomes adaptive.
This forgetting factor can be interpreted as an equivalent window length (see
[19, 14]).

2.4 Simulated Signals and Experimental Signal


Simulated signals were generated with the Markov model. A 10 kHz sampling
frequency was assumed for the simulated signals to ease comparison with the
experimental signal.
The filters shapes were obtained from experimental iEMG signals to make
the simulation more realistic. The signal to noise ratio (SNR) was set to 11 dB.
Motor neurons were sequentially activated, then deactivated. Although this
simulation does not reflect a precise physiological mechanism, it allows to test,
over a single trial, the tracking capability of the algorithm over time-varying
parameters, as well as its capability of locking the values of parameters con-
stant over time.
The experimental iEMG signals were recorded from the extensor digitorum
muscle of a healthy subject (age 24 years), with a pair of wire electrodes made
of Teflon coated stainless steel (A-M Systems, Carlsborg, WA, USA; diameter
50μm) inserted into the muscle belly with a 25 G needle, with insertion at
approximately 45 degrees with respect to the skin plane. High selectivity of
the intramuscular recording system was obtained by cutting the wires to ex-
pose only the cross-section (recording surface). The needle was then removed
with the fine wires left into the muscle for the recording. The muscle selected
308 E. Le Carpentier et al.

−3
x 10
Source 1 −3
x 10
Source 2 −3
x 10
Source 3
3 3 3
Discarge rate

actual actual actual


exp exp exp
2 est 2 est 2 est

1 1 1

0 0 0
0 2 4 6 8 0 2 4 6 8 0 2 4 6 8
Time
−3
x 10
Source 4 −3
x 10
Source 5
3 actual 3
Discarge rate

exp actual
exp
2 est 2 est

1 1

0 0
0 2 4 6 8 0 2 4 6 8
Time Time

Fig. 1 Simulations: actual signal and reconstructed one, actual trains and esti-
mated ones, actual firing rates and estimated ones

corresponds to a source of EMG activity often used for the control of pros-
theses by transradial amputees. The iEMG signals were amplified bipolarly
(Counterpoint EMG, DANTEC Medical Skovlunde, Denmark), band-pass fil-
tered (500 Hz-5 kHz), and sampled at 10 kHz. During the experiment, the
subject had access to a visual feedback of the exerted force. He performed few
changes in the contraction force during the experiment. A manual processing
produced 5 different shapes to feed the initial dictionary.
Algorithm was applied to both the simulated signals and the experimental
one, with adaptivity corresponding to a one-second equivalent window length.
The number of selected paths npath was set to 64.
Online Intramuscular EMG Decomposition 309

−4
x 10
MUAP 1 −4
x 10
MUAP 2 −4
x 10
MUAP 3
Discarge rate

estimation estimation estimation


15 15 15

10 10 10

5 5 5

0 0 0
0 2 4 6 8 0 2 4 6 8 0 2 4 6 8
Time (s)
−4
x 10
MUAP 4 −4
x 10
MUAP 5
Discarge rate

estimation estimation
15 15

10 10

5 5

0 0
0 2 4 6 8 0 2 4 6 8
Time (s) Time (s)

Fig. 2 iEMG: actual signal and reconstructed one, estimated trains, estimated
firing rates

3 Results
Results on simulated data (figure 1) did not reveal any missed spikes, and
discharge rates were correctly estimated. Activations and deactivations were
correctly detected, although a delay can be observed at deactivation, which
could be minimized by means of a smaller ti parameter. Note that the differ-
ence between simulated signal and noise-free reconstruction almost perfectly
rebuilds the original additive white noise.
Results on iEMG data (figure 2) were not compared to those of an ex-
pert, but, despite a few glitches, one can see that the automatically detected
switches in the number of active motor neurons (between 0 and 5) provide
a low mean square error between actual signal and noise-free reconstruction.
The figure shows the regularity of the MUAP trains; this regularity is favored
by the stochastic model that drives the interspike intervals.
310 E. Le Carpentier et al.

4 Perspectives
This paper proposes a new decomposition algorithm of iEMG signals which
tackles both the problems of time-varying discharge rates and time-varying
activation of motor neurons. He has an online architecture which makes it
usable in applications which need on-the-fly estimation, such as prosthesis
control. Nevertheless, practical implementation remains to be done: the algo-
rithm has a parallel architecture (npath scenarios are played together) which
could be implemented using parallel computating, e.g. GPGPU (General-
Purpose computing on Graphics Processing Units). For prosthesis control,
the mapping between iEMG decomposition and actual forces and movements
remains to be done. Automatic adjustment of the equivalent window length
has to be investigated: this length can be high for precise and meticulous
tasks, but should be low for fast and nervous movements.

References
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for force control of mechanical hands. In: IEEE Int. Conf. on Robotics and
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MIT Press, Massachusetts (1983)
Inter-session Reliability of Robot-Measured
Parameters for the Evaluation of Upper Limb
Recovery

Ivana Cusmano1, Roberto Colombo1,2, Irma Sterpi1, Alessandra Mazzone2,


Carmen Delconte2, and Fabrizio Pisano2
1
“Salvatore Maugeri” Foundation, IRCCS,
Service of Bioengineering,
27100 Pavia
roberto.colombo@fsm.it,
{ivana.cusmano,irma.sterpi}@fms.it
2
“Salvatore Maugeri” Foundation, IRCCS,
Service of Bioengineering, 28010 Veruno, Italy
alessandra.mazzone@fsm.it,
{carmen.delconte,fabrizio.pisano}@fsm.it

Abstract. Rehabilitation robots have built-in technology and sensors that allow
accurate measurement of movement kinematics and kinetics, which can be used to
derive measures related to upper limb performance and highlight changes in motor
behavior due to rehabilitation. This study aimed to assess the test-retest reliability
of some robot-measured parameters by analyzing their inter-session (day-by-day)
variability. The study was carried out using the MEMOS device, in a group of 14
patients after stroke who practiced two different motor tasks consisting of point-
to-point reaching movements in the shape of two geometrical figures specifically
selected for the assessment of global and directional (8 directions of the
workspace) test-retest reliability. The reliability of 4 parameters measuring
movement velocity, accuracy, efficiency and smoothness was assessed by the
Intra-class Correlation Coefficient, Standard Error of Measurements and
Coefficient of Variation. Patients enrolled in the study had high reproducibility
values. Directional analysis showed that in some parameters the reliability was
generally high but not homogeneous in all directions. In addition, some directions
showed systematic error. This study demonstrates that robot-measured parameters
are reliable and can be considered ideal candidates for use in combination with
clinical scales assessing functional impairment to evaluate motor improvement
during robot-assisted neurorehabilitation.

1 Introduction

Specific aspects of motor behavior in stroke survivors and the effect of therapeutic
interventions are generally measured by therapists with clinical assessment tools.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 313
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_51, © Springer International Publishing Switzerland 2014
314 I. Cusmano et al.

Although existing clinical measures are widely accepted, standardized, and


validated, they are subjective, non-linear and have a low resolution because of the
use of ordinal scales. Rehabilitation robots have built-in technology and sensors
that allow accurate measurement of movement kinematics and kinetics which can
be used to derive measures related to upper limb movements. In contrast to ordinal
scales, robotic measures provide continuous data that can be treated with
parametric statistics. However, given that this evaluation method has only recently
been introduced, few data on their reliability are available at present [1]. Here we
present the results of a preliminary study assessing the test-retest reliability of
kinematic robot-measured parameters that were previously applied to assess the
time course of recovery of stroke patients [2].

2 Methods

2.1 Subjects
The reliability of the robot measured parameters was assessed in a group of 14
patients after stroke (8 females and 6 males; aged 59±15 years). The study was
performed at the Salvatore Maugeri Foundation, IRCCS Rehabilitation Institute of
Veruno (Veruno, NO, Italy). Nine patients were in sub-acute phase, i.e. ≤6 months
elapsed since their unilateral cerebrovascular accident (CVA), and 5 at chronic
stage, i.e. > 6 months since CVA. Inclusion criteria were the presence of a single
unilateral CVA and the presence of at least 10° of motion in the treated joints
(shoulder and elbow). Exclusion criteria were the presence of severe elbow
contractures, severe visual deficits, neglect syndrome, apraxia and pain.

2.2 Robotic Device and Experimental Protocol


The robot-measured parameters were evaluated by the two degrees of freedom
elbow-shoulder manipulator MEMOS, a robot prototype partly developed at our
Institute [3]. Subjects grasped the end-effector of the manipulandum consisting of
a sensorized handle that was moved through a 40x80 cm area in the horizontal
plane (the device workspace). The limb was supported at the elbow by a low
friction pad that slid along the surface of the robot table. The robot controller
enabled ‘shared’ controlled movements in which the device assisted the subject to
complete the part of the task he/she was not able to do autonomously. Subjects
were comfortably seated at the robot desk with the trunk fastened to the back of
the chair by a special jacket and were instructed to limit compensation phenomena
by trunk movements. They were facing a video screen that provided visual
feedback of the assigned motor task. Subjects had to make a sequence of point-to-
point reaching movements in the shape of a geometrical figure in the horizontal
plane, and were instructed to move the handle from the starting point to the target.
Inter-session Reliability of Robot-Measured Parameters 315

2.3 Protocol for Reliability Assessment


We decided to evaluate the test-retest reliability of robot-measured parameters in
assessing inter-session variability (i.e. day-by-day variability). Each experimental
session consisted of 4 sub-sessions of exercise lasting 5 minutes each followed by
a 3-min. resting period. Patients underwent robot-assisted rehabilitation twice a
day, 5 days a week for at least three weeks. Inter-session reliability was assessed
by considering the first session of the last two days of training. All patients started
practice with a square path (SP) and if they showed significant motor
improvement the physiotherapist could decide to change the task to the more
complex diamond-shaped path (DP), exploring 8 different movement directions
(0°, 45°, 90°, 135°, 180°, 225°, 270°, 315°). In this case, according to our previous
findings that demonstrated no significant difference in motor gains of sub-tasks
within the practiced workspace, the global reliability was assessed by considering
the SP (i.e. the sub-task) included in the DP task [4]. Inter-session reliability was
assessed globally considering the parameters’ mean values obtained with the SP
task and directionally using data of the DP task.

2.4 Robot-Measured Parameters


During experiments the robot devices recorded the position of the end-effector at
100 Hz sampling rate and computed the following performance parameters [2],[5]:
• Mean Velocity (MV): the mean value of the velocity of the end-effector.
• Movement Accuracy: this was assessed by measuring the mean absolute value
of the distance (MD=mean distance) of each point of the actual path travelled
by the subject from the theoretical path.
• Normalized Path Length (nPL): obtained by computing the path length of the
trajectory travelled by the subject to reach the target and normalized to the
theoretical path. This parameter is a measure of the error of movement
efficiency.
• Movement Smoothness: this was estimated by the spectral arc length (SAL), to
assess small oscillations in the trajectory speed profile that correspond to higher
frequencies than the underlying movement [6].

2.5 Statistical Analysis


The calculation of reliability was carried out using the results of repeated–
measures ANOVA. In particular, it was assessed using the computational formula
(2-way fixed model equation C,1) of the intra-class correlation coefficient (ICC),
reported by McGraw and Wong [7], [8]:

1
1
316 I. Cusmano et al.

where MSE is the error mean square, MSS is the subject’s mean square and k=2. In
addition we estimated the standard error of measurements (SEM) that provides an
absolute index of reliability and quantifies the precision of individual measures on
a test. SEM was estimated by:

where MSE is again the error mean square term from the ANOVA results. It is
expressed in the metric units of the measured parameter and includes both random
and systematic components of the measurement error. Then, in order to allow
comparison of performance parameters having different measurement units, we
computed the coefficient of variation (CV) of SEM [9]. It was calculated as the
ratio between SEM and the overall mean for each parameter and expressed as a
percentage. Calculations were performed using a Matlab® custom software
(2009b, The Math Works, Natick, MS, USA) and StatView statistical package
(SAS Inst., Cary, NC, USA).

3 Results

Figure 1 reports an example of the trajectories obtained in a patient who practiced


both the SP and the DP tasks. Figure 1a refers to the last training session with the
SP before the difficulty level change. Figure 1b refers to the last session of
training.

Fig. 1 Example of trajectories obtained in a patient

Table 1 reports the mean values and standard deviations and the inter-session
reliability results of stroke patients during the SP task. The ICC was very high for
MD and nPL. The SEM was low and MD showed the worst performance with a
CV score of about 12%.
Figures 2 and 3 report the inter-session reliability analysis of 12 out of 14
patients (directional reliability) who completed the DP task. The nPL showed a
systematic error in the 225° direction. Again the MD was the parameter with the
worst CV in all directions.
Inter-session Reliability of Robot-Measured Parameters 317

Table 1 Inter-session reliability of robot-measured parameters in stoke patients

Inter-session CV
Parameters ICC SEM
Mean ± SD (%)
MV (mm/s) 73.89 ± 12.74 0.85 6.60 4.87
MD (mm) 7.90 ± 3.93 0.94 12.65 1.00
nPL (a.u.) 1.14 ± 0.13 0.92 3.39 0.04
SAL (a.u.) -2.24 ± 0.29 0.75 6.37 0.14
a.u. = arbitrary units.

Fig. 2 ICC values of the inter-session directional reliability analysis obtained in stroke
patients

Fig. 3 CV values of the inter-session directional reliability analysis obtained in our group of
stroke patients

4 Discussion

In this study we analyzed the test-retest reliability of robot-measured parameters in


a group of stroke patients who underwent robot-assisted neurorehabilitation of the
upper limb. The findings show that all the parameters are characterized by a good
318 I. Cusmano et al.

global reliability with high ICC (> 0.75 for SAL and >0.85 for the remaining
parameters) and low SEM and CV values (<13% for SAL and about 6% or lower
for the other parameters). The introduction in the reliability assessment protocol of
a more complex motor task such as the DP task showed that different directions of
the training workspace are characterized by different variability of the motor
pattern. The ICC showed the worst performance (<0.75) at 90° direction for SAL
and MV and at 135° direction for MD and nPL. The CV of MD was higher than
20% in the 135°, 270°, 315° directions. The remaining directions exhibited less
variability thus indicating a more stereotyped behavior comparable to that observed
for the other parameters. Our research group showed, in line with other authors,
that the recovery after stroke displays a non-linear logarithmic pattern in which the
largest improvements are observed early after rehabilitation onset and subsequently
gradually level off both in sub-acute and in chronic patients [10],[11]. Thus, inter-
session reliability was evaluated at the end of training where the parameter’s
variability due to learning should reach a minimum value. Limitations of this study
regard mainly the assessment protocol of patients, in that we used the parameters
measured during training to assess reliability, and not specific test-retest sessions.
On the other hand, these parameters are usually used to assess motor improvement
during training and to evaluate the time course of recovery; for this reason we
decided to use the same protocol both for training and for the reliability assessment.

5 Conclusion

The robot-measured parameters that we considered in this test-retest reliability


study exhibited very good inter-session reliability performances. MV, nPL and
SAL showed a very low SEM and CV and should be considered ideal candidates
for use in combination with clinical scales assessing impairment and functional
performance to evaluate the motor improvement of patients undergoing robot-
assisted neurorehabilitation. However, our results should be considered
preliminary and a future study including healthy subjects and with a larger sample
size is required to confirm the good reliability of these parameters.

Acknowledgment. This research was partly funded by the EU-COST Action TD1006, and
by the “5 per mille”-2009 project funded by the Italian Ministry of Health.

References
[1] Coderre, A.M., Zeid, A.A., Dukelow, S.P., Demmer, M.J., Moore, K.D., Demers,
M.J., Bretzke, H., Herter, T.M., Glasgow, J.I., Norman, K.E., Bagg, S.D., Scott, S.H.:
Assessment of Upper-Limb Sensorimotor Function of Subacute Stroke Patients Using
Visually Guided Reaching. Neurorehabil. Neural Repair 24(6), 528–541 (2010)
Inter-session Reliability of Robot-Measured Parameters 319

[2] Colombo, R., Pisano, F., Micera, S., Mazzone, A., Delconte, C., Carrozza, M.C.,
Dario, P., Minuco, G.: Assessing Mechanisms of Recovery During Robot-Aided
Neurorehabilitation of the Upper Limb. Neurorehabil. Neural Repair 22(1), 50–63
(2008)
[3] Colombo, R., Pisano, F., Micera, S., Mazzone, A., Delconte, C., Carrozza, M.C.,
Dario, P., Minuco, G.: Robotic techniques for upper limb evaluation and
rehabilitation of stroke patients. IEEE Trans. Neural Syst. Rehabil. Eng. 13(3), 311–
324 (2005)
[4] Panarese, A., Colombo, R., Sterpi, I., Pisano, F., Micera, S.: Tracking Motor
Improvement at the Subtask Level During Robot-Aided Neurorehabilitation of Stroke
Patients. Neurorehabil. Neural Repair 26(7), 822–833 (2012)
[5] Balasubramanian, S., Colombo, R., Sterpi, I., Sanguineti, V., Burdet, E.: Robotic
Assessment of Upper Limb Motor Function After Stroke. Am. J. Phys. Med.
Rehabil. 91, S255–S269 (2012)
[6] Balasubramanian, S., Melendez-Calderon, A., Burdet, E.: A Robust and Sensitive
Metric for Quantifying Movement Smoothness. IEEE Trans. Biomed. Eng. 59(8),
2126–2136 (2012)
[7] McGraw, K.O., Wong, S.P.: Forming inferences about some intraclass correlation
coefficients. Psychol. Methods 1(1), 30–46 (1996)
[8] Weir, J.P.: Quantifying test-retest reliability using the intraclass correlation
coefficient and the SEM. J. Strength Cond. Res. Natl. Strength Cond. Assoc. 19(1),
231–240 (2005)
[9] Brodie, F.G., Atkins, E.R., Robinson, T.G., Panerai, R.B.: Reliability of dynamic
cerebral autoregulation measurement using spontaneous fluctuations in blood
pressure. Clin. Sci. 116(6), 513 (2009)
[10] Colombo, R., Sterpi, I., Mazzone, A., Delconte, C., Minuco, G., Pisano, F.:
Measuring Changes of Movement Dynamics During Robot-Aided
Neurorehabilitation of Stroke Patients. IEEE Trans. Neural Syst. Rehabil. Eng. 18(1),
75–85 (2010)
[11] Kwakkel, G., Kollen, B., Twisk, J.: Impact of Time on Improvement of Outcome
After. Stroke 37(9), 2348–2353 (2006)
Reducing the False Positives Rate
in a BCI System to Detect
Error-Related EEG Potentials

Álvaro Costa, Enrique Hortal, Andrés Úbeda,


Eduardo Iáñez, and José Marı́a Azorı́n

Biomedical Neuroengineering Group, Miguel Hernández University,


Av. de la Universidad S/N, 03202 Elche, Spain
acosta@umh.es

Abstract. The goal of this paper is to detect error-related EEG poten-


tial (ErrP) to perform lower limb rehabilitation tasks. The detection of this
potential can be used as a support mechanism to avoid error during this reha-
bilitation. For that purpose, a graphical interface has been used to simulate
the error in the movement of a cursor that generate the appearance of ErrP
on a user. The EEG signals were recorded using 16 electrodes and analyzed
by two classifiers. Results from both classifiers were then combined in order
to improve the performance of the system. Preliminary results suggest that
it is possible to detect Errp with a low false positive rate.

1 Introduction
Brain-Computer interfaces (BCI) allow obtaining control commands from
the EEG signals recorded from the brain [1]. Traditionally, these interfaces
have been used to assist people with disabilities, for example,to control a
wheelchair or a care management interface [2, 3, 4]. Brain-computer interfaces
are also used in motor rehabilitation tasks related to lower limb [5, 6]. The
use of invasive brain interfaces in humans involves certain ethical and medical
limitations [7]. For this reason, the research areas that involve non-invasive
neural interfaces in humans are much more extended [8, 9]. Error-related
EEG potentials are amplitude peaks produced in fronto-central areas of the
cortex. They are characterized by a deflexion peak 250 ms after the error
stimulation is produced and a positive peak 70 ms afterwards (320 ms after
the error stimulation). Fig. 1 shows the typical appearance of an Errp.
This paper is a preliminary research for the Biomot Project (Smart Wear-
able Robots with Bioinspired Sensory-Motor Skills, Grant Agreement num-
ber IFP7-ICT- 2013-10-611695). The main goal of this project is to use EEG
signals to control a wearable robot (WR) to perform lower limb rehabilita-
tion tasks. One of the challenges of this project is the detection of obstacles
during gait. Unexpected obstacles should generate the appearance of ErrP.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 321
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_52,  c Springer International Publishing Switzerland 2014
322 Á. Costa et al.

Fig. 1 Error-related EEG potential appearance on Cz electrode. The negative


deflexion appears 250 ms after the error stimulation and the positive peak 70 ms
afterwards.

Non-invasive brain interfaces have been studied in relation to the analysis and
detection of ErrP signals [10, 11, 12]. However, the results obtained show a
high number of false positives. Each false positive represents that an obstacle
has been detected but it does not actually exist. Therefore, the appearance
of false positives produces negative effects on obstacles detection. For this
reason, the main goal of this research is to reduce the false positive rate.
This reduction is also going to be associated with a reduction on the success
rate. As we are going to work with a system with significant error sensitiv-
ity, the reduction of false positives brings a significant improvement in its
performance.

2 Material and Methods

2.1 Register and Processing


The brain-machine interface implemented for ErrP detection consists of a
non-invasive system. The signals are acquired using the commercial amplifier
g.USBamp of the g.Tec company with the g.GAMMAcap which has active
electrodes to reduce signal/noise ratio. The acquisition of EEG signals is
done using 16 electrodes of the device placed over the scalp with the following
distribution: FC5, FC1, FC2, FC6, C3, Cz, C4, CP5, CP1, CP2, CP6, P3, Pz,
Reducing the False Positives Rate in a BCI System 323

Fig. 2 Graph A: The dashed line represents the time spaces where Error-related
EEG potentials appear. Continuous function shows the vector of classification.
Graphs B and C: Final classification values. A ErrP is detected only if the clas-
sifier detects ErrP signals a specific number of times. On graph B 5 consecutive
detections are required and on graph C 3 consecutive detections are required.

P4 , PO3 and PO4, according to the International System 10/10. A sample


frequency of 1200 Hz has been used. A bandpass filter from 0.5 to 100 Hz
has been applied. Also, a Notch filter in 50 Hz to remove the noise from
electrical network is used. The time signal is divided into 600 ms windows
with a 500 ms overlap between windows. On each window a three-nearest
neighbors Laplacian filter is applied.

2.2 ErrP Detection


To detect Errp potentials it is necessary to work on the time domain. Ev-
ery signal window is associated with a class. There are two possible classes:
normal signals and ErrP signals. The model to classify each window is ob-
tained by applying two classifiers and combining them in order to reduce the
false positive rate. The first one is a quadratic discriminant analysis classifier
(QDA) and the second one is a K nearest neighbors classifier with K = 1,
with a correlation distance metric which uses random as rule. Each classifier
creates a different model. These two models are applied to the new incom-
ing signal windows providing two vectors of classification. Each classifier has
been modified to be restrictive with the detection of error-related EEG po-
tentials. They provide a small amount of correct detections but in exchange
the number of false positives is lower. Due to the characteristics of each clas-
sifier, they have a small intersection in their respective classification results.
For this reason, the union of both classification results is used to provide the
final result.
As it was mentioned in section 2.2, each window is 600 ms long overlapped
500 ms which makes 100 ms between window classifications. The ErrP signal
324 Á. Costa et al.

lasts 100-120 ms, therefore it appears in several windows consecutively. A


real ErrP signal is detected many times consecutively as it is shown in Fig. 2
(graph A). The algorithm that receives the classification vector detects a ErrP
only if the classifier detects it a consecutively number of times. This value
has been specified for each classifier. If this number is too small, most of the
ErrP signals are detected but the number of false positives increase. In Fig. 2,
the classification vector provided by the Knn classifier is shown as well as the
final classification for different values of the number of consecutively detected
ErrP signals. In graph B, 5 out of 6 ErrP signals are correctly detected and
0 false negatives appear. In graph C, 6 out of 6 ErrP are detected and 3 false
positives appear.

2.3 Experimental Procedure


This procedure has been tested in 4 healthy users (numbered 1 to 4 in Table
1) with ages between 23 and 28 all of them righthanded. They have performed
a total of 10 runs each. A run consists of 15 repetitions of a red cursor moving
from the left side of a screen to a target on the right side. Twelve movements
to the right are needed for the cursor to reach the target but the program
that controls this movement has a 20% chance of moving the cursor in the
opposite direction (with a maximum of 3 errors per repetition). When the
cursor moves from right to left an ErrP should appear in the signal. During
this movement the cursor color changes to blue in order to increase the error
stimulation. The graphical interface designed is shown in Fig. 3.

Fig. 3 Graphical interface. For 3 seconds the cursor remains stopped (the user
can blink and gesticulate during this period), on the next 10-12 seconds the cursor
moves one step right each 0.5 seconds with a 20% chance of moving left (3 no
consecutive times maximum) until the target is reached. This process is repeated
15 times completing a whole session.
Reducing the False Positives Rate in a BCI System 325

Table 1 Classification results for 4 users. Showing the total number of windows
analyzed, correctly detected and the false positives.

General data Success False positive

Total n No-error Error Error widows Success No- error windows False positive
User of windows windows windows detected rate detected rate

1 1503 1343 160 63 39.38% 24 1.79%

2 1500 1343 157 114 72.61% 10 0.74%

3 1500 1344 156 39 25.00% 10 0.74%

4 1502 1345 157 72 45,86% 23 1.53%

3 Results
Table 1 shows the results obtained. For each user, the success rate and the
false positive rate has been obtained. Because of the nature of the experiment,
the results are shown also in absolute value. As it can be seen, results have
a big variation between users. Independently of this variation, the number
of false positives (16.75 false positives - 1.20% false positive rate on average)
is lower than the correct classified ErrP windows (72 correct detections -
45.71% success rate). After applying this detection, the number of errors
detected is bigger than the number of errors introduced. On binary systems
(such a wearable robot for rehabilitation that only considers 2 different states:
appearance or not appearance of an obstacle) that means an improvement of
their performance because errors can be automatically corrected.
The variation of the results does not necessary mean that the system works
better or worse depending on the user brainwaves. That can be the conse-
quence of a subjective factor. Each subject experiences a different degree of
error sensation using the interface described. In a real environment, when
something unexpected happens and significantly affects the user interaction
with the system (obstacle appearance), the error stimulation is expected to
be higher. The system can work better on the same user working on a envi-
ronment where the sense of error is higher.
An example of the results obtained are shown in Fig 4. The top graph
shows the real number of errors and the bottom graph shows the classified
signal after the two classifiers are combined.
326 Á. Costa et al.

Fig. 4 Classification results. The top graph represents the moments where an error
occurs. The bottom graph shows the detections made by both classifiers: Dashed
lines are QDA classifications and continuous lines are Knn classifications

4 Conclusion
This research shows that ErrP signals can be detected with a low false pos-
itive rate. Depending on the user, the success rate can also be low, but it
is definitely higher than the false positive rate which was the goal of this
research. The next step is to apply this system in a real environment where
ErrP appearance corresponds to obstacles appearance. On the one hand the
sense of error experienced by the users under these circumstances should be
higher. On the other hand, registering EEG signals during gait leads to arti-
facts appearance. In future works several lines of research should be opened.
Methods for detecting and removing artifacts like [13] and other classification
methods like neural networks will be tested. The design of different interfaces
is also proposed in order to see how error stimulation changes depending on
the user and the interface.

Acknowledgment. This research has been funded by the Commission of the Eu-
ropean Union under the BioMot project - Smart Wearable Robots with Bioinspired
Sensory-Motor Skills (Grant Agreement number IFP7-ICT- 2013-10-611695), by the
Spanish Ministry of Economy and Competitiveness as part of the project DPI2011-
27022-C02-01, and by Conselleria d’Educació, Cultura i Esport of Generalitat Va-
lenciana of Spain through grant VALi+d ACIF/2012/135.
Reducing the False Positives Rate in a BCI System 327

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A Tool to Address Movement Quality
Outcomes of Post-stroke Patients

Vincent Crocher1 , Justin Fong1 , Marlena Klaic2 ,


Denny Oetomo1 , and Ying Tan1
1
University of Melbourne, Parkville, VIC 3010, Australia
{vcrocher,doetomo,yingt}@unimelb.edu.au,
justinf@student.unimelb.edu.au.com
2
Melbourne Health, Parkville, VIC 3050, Australia
Marlena.Klaic@mh.org.au

Abstract. A new neuro-rehabilitation system is proposed to address the


movement quality of post-stroke patients. The system is designed to be used
concurrently with existing upper-extremity virtual rehabilitation devices, and
to aide correction of compensatory trunk and shoulder movements. A 3D
sensor is utilised to estimate the movement of the shoulder, and an auditory
cue is given to the patient when the system estimates that a compensatory
movement has been made. The results of preliminary trials of this system on
a single patient are presented.

1 Introduction
Compensatory movements are often observed in post-stroke patients, in which
limited mobility of certain body parts is augmented with unnatural movement
of another. A classic example of this is seen in reaching movements of the
upper extremities, during which post-stroke patients often lean with their
torso to reduce the distance they are required to reach, even if this action
may normally be comfortably completed without leaning. This is considered
a poor quality movement.
Concurrently, many new robotic and virtual rehabilitation (VR) systems
dedicated to recovering movement through neuro-rehabilitation have been
developed over the past decades [1, 2, 3]. These devices are seen to be of
particular interest due to their potential to reduce the work load on clini-
cians; their potential to be used to employ new rehabilitation strategies; and
their contribution to a patient’s motivation levels within a therapy session.
Some of these systems are now used in clinics such as the Able-Reach from
Im-Able.nz, the ReJoyce from Rehabtronics, the ArmeoSpring from Hocoma
or the InMotion ARM from Interactive Motion Technologies. However, they
often do not address the problem of movement quality. Only some exoskele-
tons, such as the passive ArmeoSpring or the active ArmeoPower, are capable
of interacting with the whole limb at the joint level. However, even with these

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 329
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_53, © Springer International Publishing Switzerland 2014
330 V. Crocher et al.

devices, the interactive games do not usually take into account the way the
movement is achieved and instead present only high level goals. Often, these
goals are related only to the hand trajectory of the patient, and thus this is
the only feedback presented to the patient. Information about the limb move-
ment, such as trunk, shoulder or elbow is neglected. This can lead to poor
movement quality due to the reinforcement or development of undesirable
compensatory movement patterns commonly seen in post-stroke patients.
In contrast to this, in a systematic review of the studies where extrinsic
feedback is provided to post-stroke patients in a rehabilitation process [4],
the authors, state that “there is evidence to conclude that extrinsic feedback
is useful for implicit motor learning in stroke survivors”. More precisely they
differentiate between feedback related to a task completion and thus provided
at the end of the task, called KR (for Knowledge of Result) feedback, and
feedback based on the way the movement is performed — i.e. the movement
quality — and that can thus be provided real-time, during the movement
itself. According to their review, the latter type of feedback, Knowledge of
Performance (KP), is the most commonly used and appears to be the most
suitable and efficient in a rehabilitation process. Moreover, there are indica-
tions that the treatment of pathological synergies and compensatory strate-
gies in post-stroke patients is also important [5, 6, 7]. Following these two
ideas, in [8] the author has shown that during a classical rehabilitation ther-
apy when patients are asked to reach and manipulate different objects, the
use of an external audio feedback related to the trunk displacements, such as
‘lean against the back of the chair’, was more beneficial than a restriction of
the trunk movements using a harness.
In this paper we introduce a low-cost system to facilitate rehabilitation,
focusing on reducing trunk and shoulder compensatory movements — it aims
to provide feedback to the patient in order to improve the quality of his or
her movements. The system is based on a 3D sensor (Kinect from Microsoft,
Redmond, USA) and is intended to be used in conjunction with classical
robotics or virtual rehabilitation devices. The system and the feedback com-
putations are described in section 2 and a first preliminary study is presented
in section 3.

2 System Description
2.1 Overview
The system aims to provide feedback based on the tracking of the shoulder
movements, which are observed at the acromion. These movements are mostly
due to the trunk movements and to acromioclavicular and sternocalvicular
joint rotations — it is assumed that the glenohumeral joint rotations have
no effect on the acromion position. In order to track these movements, the
system uses a Kinect sensor and an image processing algorithm able to detect
A Tool to Address Movement Quality Outcomes of Post-stroke Patients 331

the 3d positions of two coloured plastic markers. The use of a Kinect sensor
and simple plastic markers ensures a very low-cost and simple system which
constitutes one of the main advantages of VR systems.
The subject is thus equipped with one or two markers, secured on his/her
shoulder(s) while he or she is undergoing rehabilitation therapy. C++ Soft-
ware is used to capture a colour image (rgb) and a depth image (depth)from
the Kinect. This data is then processed in real time to identify the positions
and speeds of the markers in 3D space. The software finally computes a feed-
back input value (i) according to this position or speed and translates it into
a vocal cue through a speaker placed behind the subject.
A general schematic of the system is given in Fig. 1, and Fig. 2 shows a
subject using the system.

Fig. 1 System overview

2.2 Feedback Computations


The system provides feedback during the movement itself, related to the
quality of movement, inferred through the quantity of shoulder movements.
The feedback is intermittent, active only when a given threshold is exceeded,
and is provided as a vocal cue.
332 V. Crocher et al.

Fig. 2 Subject using the system. The feedback is computed and provided by the
laptop, whereas a separate VR game is run on the desktop computer.

To address different types of pathologies, two different ways of comput-


ing the feedback — i.e. the input value i — are proposed. In the first mode,
denoted speed based feedback, the input value is the current speed of the shoul-
der whereas in a second mode, postural feedback, the input value is computed
relative to the patient static trunk posture.

2.2.1 Speed Based Feedback Computation


In the first mode, the input value i corresponds to a filtered measure of the
instantaneous speed of the marker, computed as:

i(t) = Ẋ(t)

(x(t)−x(t-5))2 +(y(t)−y(t-5))2 +(z(t)−z(t-5))2 (1)
 5×Δt
⎡ ⎤
x(t)
where X(t) = ⎣ y(t) ⎦ is the position of the marker on the impaired shoul-
z(t)
der and Δt the time step of the system. The time step is approximatively
60 ms which corresponds to a frequency of 17 Hz, sufficient to capture slow
human movements occurring at approximately 1 Hz. In order to filter the po-
sitioning noise, the speed is computed over five time steps, which correspond
to approximately 300 ms, as described in equation 1.
A Tool to Address Movement Quality Outcomes of Post-stroke Patients 333

2.2.2 Postural Feedback Computation


In the second mode, an input value is calculated proportional to the difference
between the current posture and an optimal reference posture.
Specifically, unit vectors are constructed from the position of the first
shoulder to the second shoulder. The first vector, Sref , is calculated when
the subject is in the optimal reference posture, during an initial calibration
stage. During the operation of the system, the second vector, S is calculated
at each time instant in real time. The input value is then calculated as the
sum of the angle between these two vectors in the (XY ) plane (γ), and the
(XZ) plane ψ). Fig. 3 shows the construction of the vector, and the angles
in each plane.

Fig. 3 Subject using the system in the postural feedback mode with the Sref and
S vectors, the two angles γ and ψ and the global frame. Back and top views

The angles γ and ψ can be seen as approximations of the rotations around


the central point of the C7 vertebra, in the coronal plane and transverse plane
respectively.

2.3 Feedback Provision


For both modes, the feedback is an auditory cue in the form of a voice pro-
nouncing the word “Shoulder”. This feedback explicitly reminds the subject
to correct his/her shoulder movements. The audio medium has been chosen in
order to be complimentary to the classical visual feedback provided by clas-
sical virtual rehabilitation games. Indeed, the proposed system aims to be
complementary to existing devices which mainly focus on hand movements.
334 V. Crocher et al.

The feedback is provided depending on the input value (i), calculated at


each time instant, and a threshold value (iT hreshold ). The feedback (f ) is
provided each time the input value exceeds the threshold value.
The threshold value (iT hreshold ) can be either manually or automatically
set. When set manually, a therapist observes the motion of the patient, and
sets the threshold at the value at which he or she believes requires correction.
Alternatively, an automatic adaptation of the threshold value (iT hreshold ) can
be used instead of manual tuning. With this automatic tuning, the threshold
is computed such that no feedback is provided (f = 0) 97% of the time, sug-
gesting that 97% of the time, the subject’s movement is considered normal
and does not require correction. The 97% value was determined experimen-
tally through an identification based on the threshold values chosen by a
therapist. The use of this adaptive method also provides a degree of per-
sonalised rehabilitation — the patient is consistently challenged at their own
level without the need for constant supervision and monitoring by a therapist.

3 Experiments
3.1 Method
In order to validate the usability of the proposed system in a rehabilita-
tion context, preliminary trials have been conducted at the Royal Melbourne
Hospital. The system has been tested over nine sessions — three sessions a
week — with one chronic stroke patient involved in a virtual rehabilitation
protocol.
The patient used the Able-Reach (from Im-Able.nz, Lower Hutt, New
Zealand) system together with the proposed shoulder tracking system. The
Able-Reach offers different games dedicated to upper-limb rehabilitation that
the patient controls using a mouse like device, which supports the entire fore-
arm, over a table (see Fig. 4).
Each one-hour session consisted of several playing “blocks” of duration 5
to 8 minutes — depending on the game. A 5 minute rest was offered to the
patient between each block and the program (game choice, difficulty level,
duration) was constantly adapted by the therapist to the patients current
motor capacity, motivation and needs.
Four different games were trialled: (a) Apples, (b) Targets, (c) Mosquitoes
and (d) Butterflies. These games can be classified into two categories accord-
ing to the task to be performed. The first two ((a) and (b)) require slow and
controlled movements with precise starting points and targets. In contrast,
the second two ((c) and (d)) consist of tasks requiring quicker and continuous
movements with no precise targets or desired direction of movements.
In addition to the Able-Reach, the patient was equipped with the shoul-
der tracking system with speed based feedback. The shoulder of his impaired
limb was thus equipped with a coloured marker and the position and speed
A Tool to Address Movement Quality Outcomes of Post-stroke Patients 335

Fig. 4 A subject using the Able-Reach and wearing a shoulder marker

calculated in real-time. The auditory feedback was activated each time the
patient moved the shoulder with a speed higher than the threshold. During
the first three sessions the threshold value was tuned by the therapist for each
game and for the last four sessions, the threshold was automatically tuned
by the system in order to be activated only 3% of the time (see Section 2.3).
In order to observe the immediate effect of the feedback on the patient be-
haviour, the feedback provision was turned off randomly during one block in
several sessions.
During each session the shoulder movements, the feedback input value —
i.e. the shoulder speed —, the feedback threshold and the Able-Reach game
data were recorded.

3.2 Results and Discussion


In order to observe the evolution of the patient’s shoulder speed over the
different sessions, the speed values have been averaged for each session.

3.2.1 Game Types


Since the games proposed by the Able-Reach system are of two different
types, this computation has been done separately in each session according
to the game played in the different session blocks. Fig. 5 presents the average
336 V. Crocher et al.

Fig. 5 Mean shoulder speed for each session for the two different game types and
for each session. Note that games (a) and (b) and games (c) and (d) were not played
int the first and last sessions respectively.

speed of the patient’s shoulder movements for the different sessions while he
was playing either the games (a) and (b) or (c) and (d).
In every session, a difference in the speed was observed between the two
game types. This suggests that the patient was using more compensatory
shoulder movements in games (c) and (d), which is coherent with the re-
quested task: quicker and less controlled movements. The clear difference
in the shoulder movements observed by the proposed system also confirm
the sufficient sensibility of the proposed system to track such compensatory
strategies.

3.2.2 Shoulder Movements Evolution


According to results presented on Fig. 5, no clear evolution or global trends
can be observed over the different sessions on the averaged speed value, mean-
ing that the patient does not seem to reduce his amount of shoulder move-
ments over the therapy. Nevertheless, observing the differences in Fig. 6 in
between the blocks when the feedback was activated and when the it was not
activated shows that an immediate effect of the feedback exists after several
sessions and that the patient can properly respond to the feedback, when
provided, after some training.

3.2.3 Hand Trajectories


Analysing the cursor trajectories — directly related to the patient’s hand
trajectories — recorded by the Able-Reach system in the games (a) and (b)
allow us to display the evolution of the trajectories’ smoothness. These have
been computed as the Spectral Arc Length (SAL) smoothness value, and
the mean speed of the cursor during these movements as shown in Fig. 7.
A Tool to Address Movement Quality Outcomes of Post-stroke Patients 337

Fig. 6 Differences of the mean shoulder speed with and without feedback activated
for the two different game types.

Fig. 7 Spectral Arc Length smoothness coefficient (higher means smoother) of the
trajectories and mean cursor speed, for games (a) and (b) during each session.

The SAL value is introduced in [9] and is a measure of smoothness based on


the Fast Fourier Transform (FFT) coefficients of the speed profile.
From these values, no particular evolution or correlation between smooth-
ness and shoulder speed can be observed at this point. The patient’s potential
progress is thus not observable through these variables — smoothness and
mean speed — at this stage. More sessions are needed to confirm or infirm
this assumption.
338 V. Crocher et al.

4 Conclusion
In this paper a new system aimed at addressing movement quality is proposed
to complement existing rehabilitation systems. The system provides auditory
feedback based on the inference of compensatory movements through the
shoulder. Preliminary experiments with one subject demonstrate the usability
of the system in a clinical context, as the patient appears to respond to the
auditory feedback. However, these trials do not yet provide an indication of
the effectiveness of the system to limit compensatory movement and improve
patients’ quality of movement. Nevertheless, this can certainly be explained
by the absence of formal training to teach the patient how to correct his/her
movement when the feedback is provided. In order to further investigate the
potential efficiency of such kind of systems, further experiments with more
subjects and a proper training session will be conducted in the future.
Since VR systems are becoming more prominent in clinical settings, and
may soon arrive in patients’ homes to be operated without a therapist super-
vision, it is obvious it will be important to:
• ensure that these devices can be used correctly by the patients on their
own, with correct movements;
• ensure that these devices do not only reinforce patients compensatory
strategies and pathological movement synergies but really provide a ”true”
recovery.
Systems such as the one proposed can be used to address these points.

Acknowledgement. This work was supported by the Australian Research Council


Discovery Project DP130100849.

References
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Characterization of a Dual PID-ILC
FES Controller for FES-Robot
Control of Swing Phase of Walking

Antonio J. del-Ama1 , Ángel Gil-Agudo1 ,


José Luis Pons2 , and Juan C. Moreno2
1
Biomechanics and Technical Aids Unit, National Hospital for Spinal Cord
Injury (SESCAM), Toledo, Spain
ajdela@sescam.jccm.es
2
Bioengineering Group, National Council for Scientific Research, Madrid, Spain

Abstract. Accurate control of neuroprosthesis (NP) to restore walking abil-


ity in spinal cord injured people is still challenging due to the non-linear char-
acteristics of neuromuscular tissue. The presence of an external exoskeleton
in hybrid configuration (hybrid exoskeleton) that provides joint support and
monitoring capabilities, can be exploited for control of the NP. In this work
we present the characterization experiments of a dual NP controller, com-
prised by a proportional-integral-derivative (PID) and an iterative learning
algorithm of a hybrid exoskeleton. It is found that non-causal learning allows
to overcome the electromechanical delay of knee flexor muscles. Besides, the
PID controller decreases stimulation performance.

1 Introduction
Accurate control of neuroprosthesis (NP) to restore walking ability in spinal
cord injured (SCI) people is still challenging due to the intrinsic non-linear
characteristics of neuromuscular tissue: inherent time-variance, time-delay,
nonlinearities in muscle activation relation, muscle dynamics, and skeletal
dynamics [6]. Several closed-loop control strategies have been proposed in
literature: adaptative feedback control [16], model based control [20], itera-
tive PID control [21], sliding mode control [15], model predictive control [17],
neural networks and fuzzy control [16, 18] iterative error-based learning con-
trol [3–5,7], have been proposed. Despite all these approaches for NP control
of walking, accurate movement control is still difficult. Besides, most of these
proposed control strategies rely on accurate models of the system and are
time-consuming for tunning prior its use.
Hybrid exoskeletons are devices that combine NP and robotic technol-
ogy in an attempt to overcome the disadvantages of each approach [2]. The
presence of an external exoskeleton can provide measures of both joint move-
ment and leg-exoskeleton interaction forces for control and monitoring pur-
poses. Besides, exoskeleton’s actuators can compensate joint movement and

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 341
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_54, © Springer International Publishing Switzerland 2014
342 A.J. del-Ama et al.

the diminishing muscle performance due to fatigue. However, specific control


strategies that adequately combine both (NP and robotic) technologies ex-
ploiting the respective advantages are needed. In this sense, the specific role
played by the lower limbs during swing phase of walking, and the presence
of an external exoskeleton that provides joint support and monitoring capa-
bilities, can be exploited in order to select the most suitable controller for
the NP. While for stance phase1 an isometric control of knee extensors based
on a stability criteria must be performed by the NP, the swing phase can be
regarded as dynamically determined by joint trajectory and time.
The time- and trajectory- constraints of the swing phase fit exactly within
the Iterative Learning Control (ILC) approach. This was proposed for con-
trol of processes which continually repeat the same task over a finite interval
with resetting between trials [12, 13]. An iterative algorithm is applied to
the system, the muscles in this case, until perfect tracking is achieved by
iteratively reducing the error. With this approach, high performance can be
achieved with low transient tracking error despite large model uncertainty
and repeating disturbances. Applications of ILC for NP control have been
proposed in [3–5, 7]. The main drawback of iterative controllers is that re-
quire an initial learning period before they can be used to control limbs.
This is a major drawback for using NP for rehabilitation of walking, since
initial adjustment prevents for effective use. Placing a feedback controller in
parallel with the iterative controller (dual configuration) can partially solve
this drawback by providing control during the learning period. Besides, the
dual-control approach is expected to incorporate advantages of both feed-
forward and the feedback controllers: the feedforward controllers enable fast
movements without delay, whereas the feedback controllers are able to com-
pensate for disturbance.
In this work, a dual controller consisting of a feedback controller
(proportional-integral-derivative PID) and a ILC controller for control of
stimulation of knee flexor muscles of a hybrid lower limb exoskeleton is pre-
sented. This controller is intended for control of knee trajectory during swing
phase. The objective is to characterize the control performance of the dual
controller, specifically the influence of the ILC control settings and the influ-
ence of the PID controller in the dual configuration.

2 Material and Methods


Figure 1 shows the dual controller proposed in this work. This controller is
implemented in a hybrid lower limb exoskeleton (named Kinesis [1, 2]) which
provides real-time measures of the leg-exoskeleton interaction forces. The
control task assigned to the NP dual controller (hereinafter only controller)
is to minimize the interaction forces that arises while Kinesis drives user’s
leg following a kinematic reference during swing. As long as the leg does
1
Stimulation control of the stance phase is not presented in this work.
Characterization of a Dual PID-ILC FES Controller 343

Fig. 1 Dual PID-ILC controller for control of stimulation

not move along with the trajectory pattern due to insufficient muscle force
production, an interaction torque is therefore sensed due to weight and iner-
tia. This interaction is forwarded to the controller to generate control signals
for the stimulator. Note that within this approach, interaction force has two
complementary sources: insufficient power generated by knee muscles, and
the desynchronization between actual and exoskeleton’s leg movement.
The linear ILC algorithm has the general form given by equation 1 [12,13].
Non-linear ILC algorithms could provide better results in controlling non-
linear time-varying systems, as the stimulated muscles, linear ILC algorithms
have been implemented extensively for NP control [3–5, 7], providing good
results and affordable computational cost.
 
uL(n,j+1) = [F ] · [{uLn,j } + [L] · {en,j }] (1)
The algorithm of equation 1 establishes a causal relationship between the
controlled variable (interaction torque (en )) and the previous control signal
(uLn ). However, a well known characteristic of stimulated muscle force pro-
duction is the electromechanical delay between the stimulation onset and the
force production [10]. This feature is of the most importance given that the
interaction torque is influenced by the synchronism between the kinematic
pattern displayed by the robotic exoskeleton and the actual leg movement
achieved by the stimulated muscles. To cope with it, a non-casual learning
feature was introduced in the algorithm, in order to provide the ability to
take into account errors that the control signal will produce in future sam-
ples [13]. A semi-Gaussian window centered in the sample n in the learning
matrix [L] was introduced, which length (m) provides the number of future
samples that that are taken into account, and which module is the learning
rate L. At this point, the ILC algorithm comprises several degrees of freedom
that characterize its performance: learning rate constant L, time horizon for
non-causal learning m, and forgetting rate constant F . However, the forget-
ting constant F was deliberately not introduced as a control parameter in
the experiments for simplicity, and was fixed to a moderate value (F = 0.8).

2.1 Experimental Procedure


Six healthy subjects (age 31.2±2.2 y.o., weight 80.6±9.4 kg., height 1.8±0.2
m.) volunteered for participating in the experiments. The right leg of the
344 A.J. del-Ama et al.

exoskeleton was placed over the volunteer’s leg, and stood in a platform, with
the leg hanging freely (figure 2). The experiments consisted of replicating ten
consecutive swing cycles by the exoskeleton one second apart, while the sub-
ject kept the leg relaxed. The exoskeleton controller performed control of
knee trajectory. As result, the interaction force resulting from driving the leg
passively was feed to the NP controller to stimulate knee flexor muscles (fig-
ure 1). To characterize the performance of the controller, ten configurations
were tested in two non-consecutive days, randomly sorted for each volunteer.
Prior to conduct these experiments, control gains for the PID controller were
tunned following the Ziegler-Nichols heuristic procedure. The configurations
tested were the following:
C1: No stimulation: leg moved passively. This configuration was included as
control condition.
C2: on/off stimulation. The stimulation controller was set to activate the
knee flexor and extensor muscles following an intermittent stimulation
pattern, synchronized with knee trajectory.
C3: PID. The ILC controller is disabled.
C4: PID-ILC(L=5, m=02 ). Both PID and ILC controllers were active.
Learning was L = 5 and the number of elements of the semi-Gaussian
window (time-horizon) was m = 1.
C5: PID-ILC(L=10, m=0). Both PID and ILC controllers were active.
Learning was L = 10 and time-horizon m = 1 (causal learning).
C6: PID-ILC(L=10, m=50). Both PID and ILC controllers were active.
Learning was L = 10 and time-horizon m = 50.
C7: PID-ILC(L=8, m=50). Both PID and ILC controllers were active.
Learning was L = 8 and time-horizon m = 50.
C8: ILC (L=8, m=50). The PID controller was disabled. Learning was L =
8 and time-horizon m = 50.
C9: PID-ILC(L=8, m=100). Both PID and ILC controllers were active.
Learning was L = 8 and time-horizon m = 100 (1 second).
C10: ILC (L=8, m=100). The PID controller was disabled. Learning was
L = 8 and time-horizon m = 100.
The stimulator used in this work (Rehastim, Hasomed GmbH) delivers
biphasic current-controlled rectangular pulses, and allows controlling pulse
duration (PW) in real time. The range of the current amplitude is 0 to 126
mA, and the pulse duration 0 to 500 μs. It contains eight stimulation chan-
nels, electrically isolated from the processing and application components.
For the approach implemented here, train frequency and pulse amplitude
were fixed, while PW was used as control variable for modulation of muscle
2
The stimulator controller algorithm worked at 100Hz, thus the ILC was given a
time horizon of 0 (m = 0, configurations 4 and 5), 0.5 (m = 50, configurations
6, 7, and 8) and 1 seconds (m = 100, configurations 9 and 10) for improving the
performance and overcome the electro-mechanical delay of stimulated muscles.
Characterization of a Dual PID-ILC FES Controller 345

Fig. 2 Experimental set-up. The volunteer stands while the exoskeleton replicates
knee trajectories emulating the swing phase.

force (figure 1). Four surface electrodes were placed over the over the mo-
tor points of Semitendinosus and Biceps Femoris knee hamstring muscles.
The subjects were instructed to relax their leg as much as possible prior and
during the experiments.
Time integral of the interaction torque during the swing phase (TTI) was
calculated. TTI values were normalized to the TTI of the first cycle (NTTI).
Similarly, time integral of the ILC stimulation control signal (PW in figure
1) for the swing phase was also calculated. This value was normalized to
the maximum ILC output theoretically achievable, which corresponds to a
450μs saturated output for the entire swing phase (NILC). NILC gives a
representative value ∈ [0, 1] where 0 means no stimulation during the swing
phase, and 1 means a constant, saturated ILC stimulation output of 450μs
for the whole swing phase. Number of cycles for the ILC to converge was also
obtained. Convergence was assumed when the NILC varied within a ±5%
interval between consecutive swing cycles.

3 Results
Figure 3 shows a representative example from configuration number 4. Figure
3(a) shows the kinematics and interaction torque resulting from the exper-
iment, whereas figure 3(b) shows the stimulator output. Comparing across
cycles, decreasing of the interaction torque is appreciated. This leads to a
small decrease in the PID output as consequence of the decrease on the in-
teraction torque (figure 3(b), red curve), due to muscle contribution from the
stimulated muscle. Regarding the ILC controller, it can be appreciated that
there was no control output for the first cycle (no previous iteration for the
ILC). After the first cycle, the ILC progressively increased until a station-
ary value was achieved from cycle 7 (figure 3(b), blue curve). Table 1 shows
the results obtained for NTTI, NILC and number of cycles for the ILC to
converge belonging to the last (10th) swing cycle.
Figure 4 shows the NTTI for the last (10th) swing cycle for each con-
figuration. Configuration 1 shows a decrease of 0.90±0.09 in NTTI (table
1), confirming that the subjects relaxed their legs during the experiments.
346 A.J. del-Ama et al.

(a) Knee kine- (b) Knee kine-


matics (blue matic pattern
curve: pattern; (black curve) and
black curve: stimulator output
actual) and inter- (scaled; red curve:
action torque (red PID; blue curve:
curve). ILC).

Fig. 3 Representative example from configuration number 4

Fig. 4 NTTI at the last (10th) cycle for each configuration

Surprisingly, configuration 2 shows an increase on NTTI (1.03±0.08) which


could be attributed to both desynchronization between the stimulated mus-
cles and the kinematic pattern displayed by the exoskeleton, and insufficient
muscle contribution to the movement. Besides, the sudden on/off stimulation
pattern of configuration 2 could induce the subject to produce reflex actions,
that increase their leg’s stiffness by co-contracting the muscles. It should be
noted that even with no stimulation (configuration 1), non-volitional muscle
activations can take place.
Comparing configurations 3 and 4, similar results on NTTI are observed.
Both experiments resulted in similar decrease on NTTI (0.89±0.10 and
0.88±0.06 respectively). Hence in configuration 4 the PID control was pre-
dominant and the ILC contribution was negligible. Given that both configura-
tions resulted in a similar decrease on NTTI to configuration 1 (0.90±0.09),
the PID stimulation did not contributed significantly in these cases. Con-
figurations 5 to 10 show decreased NTTI for the 10th cycle with respect to
configuration 1, coincident with increments in the learning constant L and/or
the time horizon m, and also depending on the role of the PID controller.
The role of the PID can be discussed comparing configurations 7 versus 8,
and 9 versus 10. It can be noticed that the dual controller (configurations 7
and 9) leads to higher NTTI at the last cycle (figure 4) with similar stimula-
tion intensity (figure 5(a)) than the ILC controller alone (configurations 8 and
10). Furthermore, the dual controller needed more cycles to converge than the
ILC controller alone (figure 5(b)). Thus, in this experimental conditions, the
Characterization of a Dual PID-ILC FES Controller 347

(a) NILC. Data rep- (b) Number of cy-


resent mean±SD. cles to converge.
Data represent med-
ian and inter-
quartile range.

Fig. 5 NILC and number of cycles to converge

Table 1 Experimental results. NTTI and NILC are mean±SD. Cycles to converge
are median±IQR. Data belongs to the 10th cycle.

Configuration NTTI NILC Cycles to converge


1 0.90±0.09 N.A. N.A.
2 1.03±0.08 N.A. N.A.
3 0.89±0.10 N.A. N.A.
4 0.88±0.06 0.20±0.07 7±0
5 0.83±0.06 0.34±0.09 6±3
6 0.80±0.09 0.57±0.07 3±2
7 0.70±0.13 0.50±0.16 5±3
8 0.65±0.09 0.50±0.15 3±3
9 0.68±0.15 0.57±0.14 4±2
10 0.58±0.05 0.56±0.15 3±3

PID controller decreases overall stimulation performance, interfering with the


ILC control task, as measured with these variables. The impact of increasing
the learning rate L can be analyzed comparing configurations 4 versus 5, and
6 versus 7. Increasing L increases also the NILC (figure 5(a)) and decreases
the number of cycles to converge (figure 5(b)). This increase on stimulation
intensity leads also to a decreased NTTI (figure 4).
Lastly, the influence of the time horizon m can be assessed by compari-
son between configurations 5 versus 6, and 8 versus 10. Increasing the time-
horizon m has a similar effect to increasing L on NTTI (5 versus 6 and 8
versus 10, figure 4). However, in this case, the number of cycles to converge
decreases (5 versus 6, figure 5(b)) or remains constant (8 versus 10, figure
5(a)), while the NILC increases greatly (5 versus 6, figure 5(a)) or moderately
(8 versus 10, figure 5(a)). Thus, increasing m improves stimulation perfor-
mance, as more muscle contribution is obtained increasing the convergence
velocity.
348 A.J. del-Ama et al.

4 Conclusion
The influence of the ICL control parameters and the influence of the parallel
PID of a dual PID-ILC NP controller of a hybrid exoskeleton have been inves-
tigated. Results showed that increasing the learning rate and time-horizon
(non-causal learning) of the ILC improves muscle contribution while per-
forming flexion-extension knee movements, reducing the interaction forces.
Specifically, the non-causal learning feature allowed to overcome the elec-
tromechanical delay of knee flexor muscles. It was found that PID controller
decreases stimulation performance, interfering with the ILC control task.
Nevertheless, the PID possess better capabilities of rejection of random per-
turbances that can occur during real walking conditions. More experiments
are needed increasing the ranges of the parameters in order to better char-
acterize the performance of the dual control approach. Furthermore, experi-
ments with spinal cord injured patients have to confirm the performance of
the proposed approach for control of NP for rehabilitation of walking.
Acknowledgment. This work was supported by grant CSD2009-00067 CON-
SOLIDER INGENIO 2010.

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Physiological Recruitment of Large Populations
of Motor Units Using Electrical Stimulation
of Afferent Pathways

Jakob Lund Dideriksen, Silvia Muceli, Strahinja Dosen, and Dario Farina

Department of Neurorehabiliation Engineering,


Bernstein Focus Neurotechnology Göttingen,
Bernstein Center for Computational Neuroscience,
University Medical Center Göttingen,
Georg-August University, 37075 Göttingen, Germany
jakob.dideriksen@bccn.uni-goettingen.de

Abstract. Neuromuscular electrical stimulation (NMES) is commonly used in


rehabilitation settings and technologies, but the evoked muscle activation patterns
are different from voluntary contractions in several undesirable ways. In this
study, we propose a novel scheme for NMES that relies on low-amplitude
stimulation of afferent pathways using high stimulation frequencies. Experimental
and simulated results indicated that temporal summation of the consecutive
synaptic inputs to motor neurons from the stimulated afferent fibers evoked
contractions involving many motor neurons, each generating action potentials at
relatively low discharge rates. These results indicate that this type of stimulation
may be used for functional purposes to overcome the large degree of fatigability
normally associated to NMES applied to motor fibers.

1 Introduction

NMES is commonly used in research and in clinical settings to mimic voluntary


muscle contractions in the rehabilitation of a large variety of conditions [1]. The
muscle activation is achieved via direct stimulation of alpha motor axons that
causes a synchronous recruitment of motor units, some of which are activated at
rates much greater than those occurring physiologically in most conditions. This
characteristic of NMES likely explains the high fatigability typically observed
which limits its application. A more natural recruitment pattern may be achieved if
the muscle activation occurs via the spinal cord [2] (as e.g. the Ia excitatory
pathway). The classical H-reflex recruitment curve, however, implies that only
low amplitudes of muscle activation can be achieved without activating motor
axons (as indicated by the M-wave).
In this study, we propose a novel scheme for NMES relying on high-frequency,
low level stimulation of the Ia pathway. This scheme assumes temporal
summation in the motor neurons of excitatory post synaptic potentials (EPSP)

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 351
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_55, © Springer International Publishing Switzerland 2014
352 J.L. Dideriksen et al.

associated to each stimulus. Here, we provide evidence based on experiments and


computer simulations that this stimulation scheme activates large numbers of
motor neurons at physiological discharge rates.

2 Methods

2.1 Subjects
Seven men (30.3±4.8 yrs) participated in the experiment. The subjects had no
known neurological disorders and were taking no medication at the time of the
experiment. Ethical approval for the study was granted by the local Ethics
Committee.

2.2 Experimental Procedure


The subject was seated with the lower part of the left arm resting on a foam-
padded box. The arm was held extended in front of the subject, palm facing down
and a 100 g load was fixed to the hand to induce a constant low level of voluntary
activation. Stimulation electrodes (Krauth+Timmermann, Hamburg, Germany;
circular, diameter: 32 mm) were attached distal to the lateral epicondyle at the
motor point for the Extensor Carpi Radialis muscle (evoking wrist extension).
Stimulation pulse width was set to 400 μs to optimize the selectivity of afferent
axons [3]. Muscle activity was recorded with bipolar surface EMG electrodes
(ø11mm, AMBU, Denmark) and bipolar intramuscular EMG electrodes (custom
made, Teflon coated stainless steel) inserted in the muscle using EMG amplifiers
(OT Bioelettronica, Italy). EMG signals were high-passed filtered at 120 Hz
(surface) and 1000 Hz (intramuscular) to minimize overlap between stimulation
artefacts and neural responses.
The experiment consisted of three parts. In the first part, the H-reflex
recruitment curve (see [4]) was obtained by measuring the response in the surface
EMG amplitude at a latency of 12-22 ms after the stimulus. Stimulation intensities
were 4-28 mA in steps of 4 mA. Each of the intensities was repeated eight times
with an inter-pulse interval (IPI) of 4 s and the surface EMG responses were
averaged. In this way, the currents required for 0% and 50% of maximal H-reflex
(Hmax) amplitude were identified.
In the second part, four current levels evenly spaced in the interval between 0%
and 50% of Hmax were used. For each of the intensities, eight repetitions of 1-5, 10
and 20 stimuli were delivered at 30 Hz and 100 Hz, respectively. In this way, eight
trials (4 intensities ˣ 2 frequencies) were performed in which each number of
stimuli was repeated eight times with an IPI of 4 s. For each number of stimuli the
surface EMG responses were averaged. The order of these trials was randomized.
Finally, in the third part, the load was increased in steps of 100 g to identify the
recruitment threshold of one clear and consistent motor unit in the intramuscular
Physiological Recruitment of Large Populations of Motor Units 353

EMG recording. When this level was identified 100 g was removed and it was
assumed that the excitability of that motor neuron was just below its threshold for
generation of action potentials. For most subjects, the applied load was 200 or 300
g. Starting at the stimulation intensity equivalent to 0% of Hmax, 1-6 stimuli were
delivered at 100 Hz. This procedure was repeated with increasing intensities in
steps of 1 mA until the motor unit was recruited at the 12-22 ms latency with
respect to the stimuli.

Fig. 1 The surface EMG recordings during 1-3 stimuli (A-C, respectively) delivered with
100 Hz from one representative subject. Thin grey lines indicate the 8 individual recordings
and the black line indicate average response, from which the reflex amplitudes were
estimated. The stimulation intensity was 9 mA, equivalent to elicit an H-reflex of
approximately 50% of the maximum amplitude with one stimulus. In A the different
components of the signal are indicated. The stimulation artifact is a high-amplitude tri-
phasic burst, almost completely overlapping with the M-wave due to the very short distance
between the stimulation electrode and the EMG electrodes. The H-reflex occurs after 12-22
ms. The vertical dashed lines indicate the period in which the H-reflex was identified across
conditions with different number of stimuli. Finally, the long-latency reflex occurs with a
delay of approximately 30 ms with respect to the stimuli. The red lines in B and C
represents the estimated response purely to the 2nd and 3rd stimulus. The pure response to
the 2nd stimulus (red line) was obtained by subtracting the response to the 1st stimulus
(black line in A) from the compound response to the 2nd stimulus (black line in B), and
similarly for the following number of stimuli. In this way, the influence of any overlap of
e.g. the long-latency reflex from the 1st stimulus on the H-reflex of the 2nd stimulus was
eliminated.
354 J.L. Dideriksen et al.

2.3 Analysis
In continuous stimulation at high frequencies the H-reflex response to each
individual stimulus cannot be estimated due to contamination by the stimulation
artifact and possibly the M-wave from the following stimuli. The current protocol,
however, allowed us to estimate this effect using the response to the last stimulus
in each burst of stimuli. For example, when stimulating with two pulses at 100 Hz,
the response to the second stimulus was assumed to be the same as to the second
stimulus in a longer train of pulses. In this way, performing individual trials with
either 1-5, 10 or 20 stimuli allowed estimation of the response to each of these
number of pulses. Furthermore, to avoid overlap of a long-latency reflex from the
preceding stimulus in recordings with N stimuli, the response to N-1 stimuli was
subtracted. Figure 1 illustrates this procedure.

Fig. 2 The simulated H-reflex recruitment curves (muscle activation vs. stimulation
intensity) for one, two and three stimuli at 100 Hz (red, blue and green lines respectively)
along with the M-wave amplitude (black, dashed line). Muscle excitation level was
approximately half that required for recruitment of the first motor unit. Stimulation
intensity is expressed in arbitrary units as the range of intensities required for activation of
the first axon (0) to the intensity required for activation of all axons (1).

2.4 Computational Model


A population of 180 Hodgkin-Huxley type motor neuron models [5] innervated by
a descending command and 54 Ia fibers was implemented. Each Ia fiber was
synaptically connected to all motor neurons. A Ia action potential arriving at the
synapse gave rise to an EPSC in the neuron modelled as an exponential decline
with time constant of 1.5 ms [6]. To represent variability in the synaptic strength,
each connection was randomly assigned an amplitude from a lognormal
distribution (mean: 0.3 µA, variance: 1 µA) [7].
Physiological Recruitment of Large Populations of Motor Units 355

Axon length was set to 1 m and the stimulation site to 10 cm from the distal
end. Motor neuron conduction velocities were distributed in the range 70-110 m/s,
according to their soma diameter, while Ia conduction velocity was randomly
selected from a normal distribution (105±20 m/s) [8]. Axon rheobase current was
set as inversely proportional to the conduction velocity [9]. When activated, the
action potential propagated in both directions of the axon from the stimulation
site. Motor neuron action potentials were extinguished in case of antidromic
collisions.

3 Results

3.1 Simulation Results


Figure 2 shows the simulated H-reflex recruitment curves for 1-3 stimuli at 100 Hz.
Due to a low background excitation level, a relatively high stimulation intensity
was required for activation of any motor neurons using one stimulus. At multiple
stimuli, however, much less current was required for a substantial response. This
reflects the fact that even though the first stimulus was not sufficient for the motor
neuron membrane potentials to reach their thresholds, it served to depolarize the
neurons so there was a high probability that one of the next EPSCs could trigger an
action potential.
When simulations with continuous 100 Hz stimulation below the motor axon
rheobase current (35% of total axonal recruitment; see Figure 2) during low-level
voluntary contractions (average motor neuron discharge rate: 12.2±2.1 pulses pr.
second (pps); 128 recruited motor neurons) were performed, the motor neuron
action potentials tended to occur in bursts near the latency of the H-reflex for each
stimuli. The number of action potentials in each burst was relatively stable
(18.9±6.8). However, between each consecutive burst different motor neurons were
active. In total, 137 motor neurons were recruited by the stimulation with an
average discharge rate of 14.4±2.0 pps. When stimulation frequency was increased
to 150 Hz the average discharge rate was 15.8±1.7 pps (140 motor neurons).

3.2 Experimental Results


Figure 3 depicts the H-reflex amplitudes in response to 1-5, 10 and 20 stimuli
when delivered at stimulation intensities equivalent to approximately 0-50% of
Hmax at 30 Hz and 100 Hz, respectively, for one representative subject. When
multiple stimuli were delivered at 30 Hz the H-reflex amplitude tended to
decrease, which is commonly referred to as post-activation depression [10].
Conversely, the H-reflex amplitude increased substantially at multiple stimuli at
100 Hz, peaking at between 2-4 stimuli. This indicated that the degree of muscle
activation evoked by a given number of stimuli depends strongly on the
stimulation frequency.
356 J.L. Dideriksen et al.

Figure 4 depicts the increment in the H-reflex for all subjects when delivering
three stimuli instead of one across the stimulation intensities for both frequencies.
As indicated by linear regression, an average increase in the H-reflex amplitude of
45% of the response obtained in the single-stimulus case was observed when
stimulating at 100 Hz. In comparison, an 8% increase was obtained at 30 Hz
stimulation. Across all number of stimuli, the average increment in the H-reflex at
100 Hz was 25%, while the average increment across the two frequencies was
32%.
Figure 5 illustrates the results of the third part of the experiment involving
intramuscular recordings for one subject. Here, the amplitude of the response
indicates if the observed motor unit was recruited. When stimulating at 4 mA, no
response was observed for any number of stimuli. However, at 5 mA the motor unit
was in most cases recruited after either three or four stimuli. This implies that the
input from a number of consecutive stimuli was necessary for recruitment of this
motor unit. A similar behavior was observed in four other subjects. In the final two,
highly variable background excitation levels did not allow to perform the analysis.

4 Discussion
This study investigated the impact of high-frequency afferent stimulation on the
output of a motor neuron population using experiments and a computational model.
Two important properties of high-frequency stimulation below the threshold of
motor axon recruitment were illustrated by the model simulations. First, when
multiple stimuli are delivered, the excitability of the motor neuron pool increases
and thus provides a higher motor output. Second, the motor neurons contributing to
consecutive H-reflex responses are not the same. Instead a large number of motor
neurons “rotate” and are recruited only by every Nth stimuli, where N depends on
the amount of synaptic input from the Ia fibers and the background excitation level.

Fig. 3 The H-reflex amplitude in response to 1-5, 10 or 20 stimuli delivered (see color
coding) at four different stimulation intensities (approximately equivalent to 0-50 % of the
intensity required for to achieve the maximum single-stimuli H-reflex amplitude) at 30 Hz
(A) and 100 Hz (B) for one representative subjects. As the condition indicated by the black
line (one stimulus) is similar across the two frequencies, the average (and std) of these two
measurements are shown.
Physiological Recruitment of Large Populations of Motor Units 357

Fig. 4 The change in H-reflex amplitude when multiple stimuli is delivered at 30 Hz (A)
and 100 Hz (B) with respect to the amplitude achieved with only one stimuli for all
subjects. Each dot represents one stimulation intensity for one subject. Stimulation intensity
(x-axis) is represented as the amplitude of the equivalent single-pulse H-reflex obtained
with one stimulius. Here, the results from 3 stimuli are shown. The black line indicates the
best linear fit to the data, while the dashed line represents 0 H-reflex increment.

Fig. 5 Boxplot-representations of the H-reflex as measured by intramuscular EMG


Intramuscular H-reflex for different numbers of pulses delivered at 100 Hz. For each
subject, two stimulation intensities were employed; the lowest intensity required for
recruiting motor units (black) and the intensity one mA below this level (grey). * indicates
data points located outside 1.5 ˣ inter-quantile quartile range.

Using a novel stimulation protocol, the H-reflex response to individual stimuli in


a high-frequency train of stimuli was estimated. The results showed that the
amplitude of the H-reflex increased substantially when stimulating at 100 Hz
compared to at 30 Hz, indicating recruitment of more motor units in each reflex
response. While the simulations indicated temporal summation as the underlying
mechanism, a super-normal excitability of Ia axons due to the 100 Hz stimulation
may also have contributed [11]. Furthermore, the intramuscular recordings
indicated that the activation pattern of motor neurons recruited by the stimulation
was not time-locked to every stimulus, but instead required the synaptic input from
a number of stimuli to be recruited (at least at low stimulation intensities).
358 J.L. Dideriksen et al.

These observations confirm the simulation results as they imply that more motor
units are recruited in response to each stimulus during high-frequency stimulation
and that two consecutive H-reflex responses (both reflecting activity in more motor
units than would be achieved at low-frequency stimulation) comprises different
groups of motor units. In this way, large groups of motor units are recruited over
the course of several 100 Hz stimulation pulses with discharge rates below the
stimulation frequency and possibly in the physiological range.
These findings have several implications for NMES. Although the classical H-
reflex recruitment curve indicates that only a low level muscle activation can be
achieved exclusively via stimulation of the Ia pathway (below the threshold for
motor axon stimulation), this activation level increases substantially when the
stimulation occurs at high frequencies. In this way, the results suggest that NMES
should rely on frequency-modulation of the stimuli at low amplitudes, rather than at
amplitude-modulation at low frequencies, as is typically applied [1]. Since
physiological reasonable single motor neuron discharge rates were evoked by the
stimulation, the well-known problems regarding fatigability may be diminished.
Further research is required to investigate the range of forces that can be
achieved using this stimulation paradigm, as well as the level of muscle fatigue
induced, and the degree to which the evoked forces can be controlled.

Acknowledgment. This work was funded by the EU Commission through the project
NeuroTREMOR (contract #287739).

References
[1] Bickel, C.S., Gregory, C.M., Dean, J.C.: Motor unit recruitment during neuromuscular
electrical stimulation: A critical appraisal. Eur. J. Appl. Physiol. 111, 2399–2407
(2011)
[2] Bergquist, A.J., Wiest, M.J., Collins, D.F.: Motor unit recruitment when
neuromuscular electrical stimulation is applied over a nerve trunk compared with a
muscle belly: Quadriceps femoris. J. Appl. Physiol. 113, 78–89 (2012)
[3] Veale, J.L., Mark, R.F., Rees, S.: Differential sensitivity of motor and sensory fibres
in human ulnar nerve. J. Neurol. Neurosurg. Psychiatry. 36, 75–86 (1973)
[4] Schieppatti, M.: The Hoffmann reflex: A means of assessing spinal reflex excitability
and its descending control in man. Prog. Neurobiol. 28, 345–376 (1987)
[5] Cisi, R.R.L., Kohn, A.F.: Simulation system of spinal cord motor nuclei and
associated nerves and muscles, in a web-based architecture. J. Comput. Neurosci. 25,
254–520 (2008)
[6] Finkel, A.S., Redman, S.J.: The synaptic current evoked in cat spinal motoneurones
by impulses in single group Ia axons. J. Physiol. 342, 615–632 (1983)
[7] Mendell, L.M., Henneman, E.: Terminals of single Ia fibers: location, density, and
distribution within a pool of 300 homonymous motoneurons. J. Neurophysiol. 34,
171–187 (1971)
Physiological Recruitment of Large Populations of Motor Units 359

[8] Heckman, C.J., Binder, M.D.: Analysis of effective synaptic currents generated by
homonymous Ia afferent fibers in motoneurons of the cat. J. Neurophysiol. 60, 1946–
1966 (1988)
[9] Rubinstein, J.T.: Analytical theory for extracellular electrical stimulation of nerve
with focal electrodes. Biophys. J. 60, 538–555 (1991)
[10] Clair, J.M., Anderson-Reid, J.M., Graham, C.M., Collins, D.F.: Postactivation
depression and recovery of reflex transmission during repetitive electrical stimulation
of the human tibial nerve. J. Neurophysiol. 106, 184–192 (2011)
[11] Kiernan, M.C., Mogyoros, I., Burke, D.: Differences in the recovery of excitability in
sensory and motor axons of human median nerve. Brain 119, 1099–1105 (1996)
Extending a Dynamic Muscle Model
for Usage with Amputees

Stefan Erber1, Markus Schachinger2, Thomas Mandl3 , and Peter Michael Goebel2
1 University of Applied Sciences, Technikum Wien and Otto Bock Healtcare Gmbh,
Vienna, Austria
ster4135@gmail.com
2 Otto Bock Healthcare Products GmbH, Vienna, Austria
{Peter.Goebel,Markus.Schachinger}@ottobock.com
3 University of Applied Sciences, Technikum Wien, Vienna, Austria
mandl@technikum-wien.at

Abstract. When muscles are used during ordinary work, the fibers of a particular
muscle are recruited by the corresponding motor-neurons of the spine. From the total
number of fibers in the muscle, only parts are recruited to be active for work accord-
ing to the required force which the cortical system has estimated. Thus, using the
activated fibers by applying force over a period of time, the fibers get more and more
fatigued and are replaced by newly activated ones. J. Z. Liu et al. developed a tech-
nically sound theoretical model for muscle activation, fatigue and recovery which
describes how many motor units are in the states of rest, activation and fatigue. In
this work, Liu’s theoretical model is adopted and extended in order to simulate and
investigate fatigue. The actual state of a muscle is estimated by the measurement
of surface Electro-Myo-Graphy (sEMG), force and torque. In the model, using the
input parameters sEMG, or force and torque, with amputees the number of Motor
Units (MU) are estimated in the states: rest, activation and fatigue. A method for
muscle state estimation at amputees is presented in this work.

1 Introduction
The goal of this work is to find a method for quantifying the actual fatigue state
of forearm muscles in amputees. J. Z. Liu et al. [1] developed a technically sound
theoretical dynamical model of muscle activation, fatigue, and recovery, which we
have extended to simulate and investigate fatigue and recovery among amputees.
Liu’s muscle force model was chosen, because it considers the whole cycle of fa-
tigue and recovery and requires only a few parameters. Several other fatigue models
[1, 2, 3, 4, 5, 6, 7, 8] exist which also describe methods for detecting fatigue in
muscle contraction data-sets, recorded during muscle contractions. However, most
of these models require too many parameters, or do not consider recovery effects,
which make them unsuitable for practical use. Liu’s model considers three pools
of fibers, corresponding to the states rest, fatigue and activation. The driving force
in Liu’s model is the brain effect B, which drives a number of Motor Units (MU)
from the rest- to the activation state. The number of MU in each state is estimated

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 361
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_56,  c Springer International Publishing Switzerland 2014
362 S. Erber et al.

Fig. 1 Input and output of Liu’s dynamical model of muscle activation, fatigue and recovery.
The model input parameter is the constant Brain-effect (B). The output parameter, the number
of Motor Units (MU) in the states rest (NR(t)), activation (NA(t)) and fatigue (NF(t)), describe
muscle behavior during voluntary movements.

under constant brain-effect condition (B). Over time, more and more MU change
from the active to the fatigue state. Later, MU in the fatigue state are recovered back
into the activation state. This cycle is continued, until all available MU are fatigued.
The model delivers the estimated number of MU in the states rest (nR(t)) activation
(nA(t)) and fatigue (nF(t)) over time. The fatigue and recovery factors F, R are also
assumed to be constants by the model [1]. The model of J. Z. Liu et al. describes
the behavior of muscles as a group of motor units activated by voluntary effort with
a set of dynamical equations The model provides a macroscopic view for under-
standing biophysical mechanisms of voluntary drive, fatigue effect, and recovery in
stimulating, limiting, and modulating the force output from muscles [1].

2 Methods
The state of a certain skeletal muscle is of interest in determining muscle-fatigue,
and also to get informed on how much a subject may rise contraction force up under
some conditions. Therefore, we adopted Liu’s idea, and extended it in the following
points, :
i The Brain effect (B) is thought to be the factor which activates the number of
MU needed to produce the desired muscle force output.
ii sEMG data are the input parameters of the muscle state model instead of the
brain-effect.
In the presented muscle state model, the latent muscle states - (as a function of
time) - of a subject are thus estimated from surface Electro-Myo-Graphy (sEMG)
data. The muscle states are represented by the estimated number of Motor Units
(MU) in the states of: rest, activation and fatigue. For the calibration and ground
truth proof of the model, we measured force and torque from able-bodied subjects
and verified the proportionality between the RMS (Root Mean Square) value of the
EMG signal and corresponding Force/Torque values. We performed force/torque
and sEMG measurements with six male and four female right-handed subjects be-
tween 20 and 60 years during wrist movement (w. supination, w. pronation, w. ex-
tension, w. flexion, w. abduction and w. adduction) exercises. The desired brain
input, which is an input and hence assumed to be a known parameter in Liu’s model,
was presented visually to the subjects (in terms of a given target contraction item,
see Figure 3) and the state of the muscle (in terms of nR(t), nA(t) and nF(t)) was
estimated.
Extending a Dynamic Muscle Model for Usage with Amputees 363

FX
MX
FZ

MZ
Oberflächen EMG
Elektroden
Surface EMG MY
Electrodes
Force/Torque
Sensor System
FY

Fig. 2 Sensor system. sEMG is detected by the Scissor-fence, with its eight embedded dry
electrodes, who is placed around the forearm. Muscle force is detected by the force/torque
sensor system, including six force and six torque sensors.

2.1 Sensor System


During measurement and data collection of a wrist movement, force/torque and
sEMG was detected. Force and torque data were detected by an in-house developed
sensor system. The sensor system includes three force and three torque sensors. It
additionally includes a handle to transmit muscle force to the sensors and an armrest
(see Figure 2). The three force sensors detect force in X (FX ), Y (FY ) and Z (FZ ) di-
rection. The three torque sensors detect torque around X (MX ), Y (MY ) and Z (MZ )
direction. sEMG data were detected by eight dry electrodes. The eight electrodes
were embedded into a scissor-fence and can be arranged around the forearm with-
out the need of a prosthesis stem. Force and torque data were detected to validate
the muscle state model with Liu’s model and the sEMG to extend Liu’s model for
muscle state estimation with amputees.

2.2 Experimental Structure and Visual Feedback


The measuring cycle of one wrist movement measurement was structured in the fol-
lowing way: First, the subject‘s individual Maximum Voluntary Contraction (MVC)
was measured. Next the desired brain input was presented visually in terms of a
given target contraction. The MVC value was used to determine the maximum of
the given target contraction. Next, visual feedback, in terms of an advanced train-
ing paradigm, was provided to the subjects during measurement. Visual feedback
helps subjects by giving them more awareness of their actions during measurement
[9]. The visual feedback included three graphs: the given target contraction item,
the force/torque graph and the sEMG graph as shown in Figure 3. The force/torque
and the sEMG were calculated in real time. The real time graphs present the current
measured data on the screen. The Root Mean Square (RMS) feature was calculated
from the digitized and filtered analog sEMG data, and the amount of the vectorial
sum of all detected force and torque data (VSum ) was calculated before they were
presented on the screen. Subjects were instructed to follow the given target contrac-
tion item slope with their actual visualized muscle force. As soon as the MVC value
was reached the Brain-effect (B) goes into saturation. Therefore the muscle force
generated by the actual muscle fibers does not rise after MVC value is reached.
364 S. Erber et al.

Wrist Supination – Muscle State Estimation 100 % MVC


B - Saturation at MVC

Given target
RMS
contraction item
VSUM

Wrist
Supination

Fig. 3 The graphs presented on screen during measurement. In blue: given target contraction
item that should be performed. In red: detected sEMG data and green one: detected force and
torque data.

After reaching the maximum of the muscle force subjects were instructed to hold
the force without activating any additional MU, because the muscle state model
would restart for the additional activated MU. Measurement time was two minutes.

2.3 Comparison of Force/Torque and sEMG Data


Force and torque data and sEMG data were compared quantitatively by calculating
the correlation between the vectorial force and torque sum and the RMS sEMG
feature (see Figure 5), before the muscle state model was extended by the muscle
state estimation with sEMG data. Muscle force can not be detected directly from an
amputated hand. Therefore sEMG data are used as model input.
Muscle states are estimated by analyzing the rise and fall in RMS between a local
minimum and a local maximum. Fatigue occurs when the delta between minimum
and maximum of the RMS declines; whereas recovery occurs when this delta values
rises. In Figure 4 the estimation delta values for muscle state are shown. The delta
values serve as an estimate of the number of MU in the states of rest (NR ), activation
(NA ) and fatigue (NF ).

Wrist Supination – Subject 2

sEMG
∆FF
%MVC

∆t Recovery
∆FR
Fatigue

∆t

Time * 103 Local Maixima Local Minima

Fig. 4 The RMS graph of sEMG data (dark green) of wrist supination of subject 2. Also the
local maxima and minima. Figure depicts the RMS of measured sEMG data (dark green) of
wrist supination of subject 2. Also depicted are local maxima (purple dashed) and minima
(yellow dashed), the delta fatigue (Δ FF ) and recovery (Δ FR ) force and the rise time. Muscle
state is estimated by the delta fatigue and recovery values at time points where local minima
and maxima values occur.
Extending a Dynamic Muscle Model for Usage with Amputees 365

Input Output
4a)
3a) Fatigue
NA -
effects
2) Local NF +
1) Vectorial Æ Δ values -
B MU sEMG maxima NR = NMVC - NA Muscle
sum of all
activation at different and state
time points sensors 4b)
minima 3b) Recovery
NA +
effects
NF –
Æ Δ values +
NR = NMVC - NA

Fig. 5 Basic setup muscle state estimation. Motor Units (MU) and their innervated muscle
fibers are activated by the Brain-effect (B). Muscle force is generated by the activated muscle
fibers. Action potential accrues in the activated muscle fibers during muscle force generation.
Six electrodes detect sEMG signals. Where one detected sEMG signal represents the com-
pound action potential of one or more muscles. The model input are the sEMG signal-data
delivered from the six electrodes. The Root Mean Square (RMS) is respectively computed
from these sEMG signal-data (1). from force and torque sensor data. Local maximums and
minimums (2) are found in the computed signal. The number of MU in the states of rest (NR ),
activation (NA ) and fatigue (NF ) (4) are estimated by analyzing the rising or falling delta
values between local maximums and minimums (3). The model output is the muscle state at
different time points.

Muscle state
nR(t) 100

90
B Muscle F/T nA(t)
Muscle state 80
fiber
model nF(t) 70
Number of MU in % RT

activation 60

50

40
nR(t)
30

B Muscle sEMG nA(t) 20


Muscle state
fiber 10
model nF(t)
activation 0

0 20 tRT 40 60 80 100
Time (10^3) [ms]

Fig. 6 Muscle state model output. The Brain-effect (B) leads to MU activation. MU activation
leads to AP which leads to muscle force. Force/Torque (F/T) and sEMG can be detected from
activated muscle fibers (Left figure). The model output are estimates muscle states at different
time points (MU in activation state sEMG (red), MU in activation state F/T (green), MU in
fatigue state sEMG (brown), MU in fatigue state F/T (violet) MU in rest state sEMG (light
blue) and MU in rest state F/T (dark blue)). Estimated from the detected force/torque and/or
sEMG data (right Figure).

2.4 Model Output


The model output are the estimated muscle states represented by the number of MU
in the states: rest (NR ), activation (NA ) and fatigue (NF ) (see Figure 8).
366 S. Erber et al.

2.5 Model Validation


The muscle state estimation using force and torque data is applied to validate the
muscle state model by comparing the output with Liu’s theoretical muscle model,
which was developed for fatigue estimation with muscle force measurement. The
model is validated quantitatively by the calculation of the correlation coefficient of
the curve shapes.

3 Results and Discussion


Figure 7 shows the mean correlation coefficients of the correlation between the vec-
torial sum of force and torque sensor data and the sEMG RMS. The correlation was
calculated to determine if sEMG RMS data can be used instead of force and torque
data. All mean correlation coefficients are greater than plus 0.70 and show there-
fore a strong uphill (positive) linear relationship. The mean correlation coefficients
suggest that RMS data values can be used instead of force/torque data as model in-
put. Therefore, the model can be used to estimate muscle states of amputees. Our
results are qualitatively similar to theoretical predictions by Liu’s model. (see Fig-
ure 8). One difference to Liu’s model is an equilibrium state which occurs when
fatigue behaves approximately the same as recovery. The duration of this equilib-
rium state depends on the physical condition of the subject. While in Figure 8 -
B lower panels the equilibrium state lasts until the end of the measurement, in the
figure upper panels (Figure 8 - A) the equilibrium lasts only 15 seconds. This dif-
ference in the duration of the equilibrium state occurs because the subject on which
the fifth flexion measurement was taken (Figure 8 lower panels), possesses more
type I muscle fibers (regularly practice the sport of climbing), and the subject with
which the fourth supination measurement was done (Figure 8 upper panels), pos-
sesses untrained type I muscle fibers. Also, the RMS declines after the occurring
equilibrium state in the figure upper (Figure 8 - A) left panel, because the subject
on which the fourth supination measurement was done possesses untrained mus-
cles. Figure 9 show the mean correlation coefficients of the correlation between the
muscle state model output and the output of Liu’s theoretical model. All mean cor-
relation coefficients are greater than plus 0.70 and therefore show a strong uphill

No W. W. W. W. W.
movement supination flexion extension abduction adduction
1

0,98

0,96
0,94

0,92
0,9

Fig. 7 Mean correlation between all detected RMS and vectorial force torque sum VSum of
all measurements. The mean correlation coefficients show a strong uphill (positive) linear
relationship. Therefore RMS data can be used to describe muscle force.
Extending a Dynamic Muscle Model for Usage with Amputees 367

Wrist Supination Subject 04


A 100
120
120
Fatigue > 80

Recovery

Number of MU
80
60
% MVC
80

Number Of MU [%]
40
40
40 20

0 0

0 -20
0 20 40 60 80 100 120
0 50 100 0 50Time [s] 100 Time [s]
Time (10^3) [ms]
Liu´s Model Muscle State
Decline in torque - typical Equilibrium state MU in Activation State Model
MU in Fatigue State
for Type I fibers Fatigue ~ Recovery MU in Rest State

B Wrist Flexion Subject 05


120100
120
80

80

Number of MU
60

Number Of MU [%]
% MVC

80
40
40
20

40
0 0

-20
0 20 40 60 80 100 120
0 0 50Time [s] 100 Time [s]
0 50 100
Time (10^3)
Time [ms]
(10^3) [ms]

Fig. 8 The Figure left panels shows the amount of the vectorial sum of force and torque
data (yellow) and sEMG RMS data (red), which is used for muscle state estimation. Also
depicted are the local maxima and minima between which the delta fatigue and recovery are
defined. Figure right panels shows the estimated muscle states, i.e. the number of MU in the
rest (blue), activation (green) and fatigue (purple) states and the output of Liu’s model; the
number of MU in the states rest (blue), activation (green) and fatigue (purple).

No W. W. W. W. W.
movement supination flexion extension abduction adduction
1
N R:
0,98
N A:
0,96 N F:

0,94

0,92
0,9
0,88

0,86

Fig. 9 Mean correlation between the muscle state model output and the output of Liu’s
model.The mean correlation coefficients show a strong uphill linear relationship. That proves,
that Liu’s theoretical model can be used practically.

(positive) linear relationship. This suggests that Liu’s theoretical model can be used
practically by estimating the muscle states with force and torque or sEMG data input
instead of the theoretical brain-effect, which cannot be detected with state-of-the-art
measurement methods (see 8). In general, it can be stated that the calculated corre-
lation coefficients are worse than the mean correlation coefficient, when subjects
do not reach the maximum of the given target contraction (calculated from a sep-
arate MVC measurement shortly before the actual force/torque measurement) with
their actual detected force/torque data during measurement. When subjects do not
reach the maximum of the given target contraction their brain-effect does not go into
saturation (the subjects do not use their full muscle force potential).
368 S. Erber et al.

4 Conclusion
Results show that the muscle state model is useful for muscle state estimation. The
adopted muscle state model presented delivers the output almost as Liu expected.
Next the model should be extended for repetitive movements. During repetitive
movements the model would start over again for each movement and the result
would be the estimated mean muscle states. Hence, in conclusion the implemented
model is considered useful for research in new adaptive control concepts and for the
influence of muscle fatigue influence on prosthesis control where the investigation
of the user’s latent muscle state is of importance.

References
1. Liu, J.Z., Brown, R.W., Yue, G.H.: A Dynamical Model of Muscle Activation, Fatigue,
and Recovery. Miophysical Journal 82, 2344–2359 (2002)
2. Wan, B., Xu, L., Ren, Y., Wang, L., Qiu, S., Liu, X.: Study on Fatigue Feature from Fore-
arm SEMG Signal Based on Wavelet Analysis. In: International Conference on Robotics
and Biomimetics, Tianjin, China, December 14-18, vol. 82 (2010)
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fatigue estimation. Journal of Electromyography and Kinesiology 21 (2011)
4. Vukova, T., Vydevska-Chichova, M., Radicheva, N.: Synthetic structure of industrial
plastics (Book style with paper title and editor) Fatigue-induced changes in muscle fiber
action potentials, estimated by wavelet analysis. Journal of Electromyography and Kine-
siology 18, 397–409 (2008)
5. Bonato, P., Galgliati, G., Knaflitz, M.: A Time-frequency Approach to Assessing Muscle
Fatigue, estimated by wavelet analysis. Journal of Electromyography and Kinesiology 18,
397–409 (1996)
6. Bigland-Ritchie, B., Donovan, E., Roussos, C.: Conduction velocity and EMG power
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7. Ma, L., Chablat, D., Bennis, F., Zhang, W., Guillaume, F.: A new muscle fatigue and
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9. Gbel, P., Honeder, J.L., Erber, S., van Vliet, H.W.: Visuelles Biofeedback fr anwen-
derorientiertes Training und Steuerung von mulitfunktionalen Oberflchen-EMG Prothe-
sen. Rthopdie-Technik 2(13) (2013)
Measuring the Effectiveness of an Intensive
Rehabilitation Treatment on Balance
Parameters in Patients with Parkinson’s
Disease through a Stabilometric Platform

Davide Ferrazzoli1, Rossana Bera1, Roberto Maestri2, Gloria Perini1,


Letizia Spina1, Roberto Gargantini1, Gianni Pezzoli3, and Giuseppe Frazzitta1
1
Department of Parkinson Disease Rehabilitation,
Ospedale Generale di Zona “Moriggia-Pelascini”,
Gravedona ed Uniti (CO), 22015, Italy
davideferrazzoli@gmail.com
2
Fondazione Salvatore Maugeri IRCCS,
Dipartimento di Bioingegneria e Tecnologie Biomediche, Montescano (PV)-Italy
3
Parkinson Institute, Istituti Clinici di Perfezionamento, Milano, Italy

Abstract. Falls are the most disabling symptom in patients with PD, and balance
disorder is the most important factor involved in its genesis. We have studied the
effects of our multidisciplinary intensive rehabilitation treatment (MIRT) on
balance disorders in PD. 30 PD patients underwent clinical and instrumental
evaluations at the beginning (T0) and at the end (T1) of the MIRT. To determine
some variables as index of postural stability, we used a stabilometric platform.
With respect to the average centre of gravity, total, antero-posterior [AP] and
mediolateral [ML] standard deviations (SD) of trunk sway were calculated. We
have also obtained a statokinesigram and the area of the ellipse containing 90% of
the sampled positions of the center of pressure. Statistical analysis showed
significant differences in the SD of trunk sway between T0 and T1. These
preliminary results are consistent with literature data and confirm the disruption of
the complex mechanisms of balance control in PD. There is increasing evidence
that physical therapy can improve postural stability and reduce the risk of falls.
We are confident that our findings will provide new knowledge and highlight the
importance of an early balance training in PD.

1 Introduction

Falls in people with Parkinson's disease (PD) have a multifactorial cause, but
balance impairment is a major contributor to this frequent and disabling
complication (1-2). Balance impairment in PD is associated with poor reactive
responses following external perturbations (3). As degeneration of the basal
ganglia affects many physiological systems essential for posture control, balance
disorders in PD result from an impairment of multiple systems. Pharmacotherapy

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 369
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_57, © Springer International Publishing Switzerland 2014
370 D. Ferrazzoli et al.

with dopaminergic medications and deep brain stimulation cannot provide


significant improvements in postural instability, whereas previous reports of
physical interventions have suggested promising results (4). At the present time
there is no standardized protocol for the treatment of postural instability in
parkinsonian patients. The aim of our study is to identify a useful tool to monitor
the effectiveness of a rehabilitation treatment on postural instability in PD.

2 Materials and Methods

2.1 Intervention
We have studied the effects of our multidisciplinary intensive rehabilitation
treatment (MIRT) [4] on balance disorders in PD. We defined our interventions as
“intense” on the basis of the total time spent doing it. In fact, MIRT consisted of a
4-week inpatients cycle of physiotherapy that entailed 3 daily sessions (2 sessions,
not consecutive in the morning, and 1 session in the afternoon), for 5 days a week.
The total duration of each session, including recovery periods, was about 1 hour,
for a total of 3 hours per day. The first session comprised cardiovascular warm-up
activities, relaxation exercises, muscle stretching exercises (scapular muscle
group, hip flexor, hamstring, and gastrocnemius muscles), exercises to improve
the range of motion of spinal, pelvic and scapular joints, exercises to improve the
functionality of the abdominal muscle and postural changes in the supine position.
The second session included exercises to improve balance and gait using a
stabilometric platform with a visual cue (patients are asked to follow a circular
pathway on the screen by using a cursor sensitive to their feet movements on the
platform) and treadmill plus (treadmill training with both visual and auditory cue).
All treadmill therapy was aerobic with a heart rate reserve ≤ 60% and a maximum
speed of treadmill scrolling of 3,5 km/h. Subjects received training for 30 minutes
every day for 4 weeks (20 sessions in all). Maximum tolerated walking speed was
determined before the training session. This speed was reduced (-40%) and used
for a 2-day warm-up period. After that the belt speed was increased every 3 days
by 0.05 stride cycles/second. The third was a session of occupational therapy
aimed at improving autonomy in daily living activities.

2.2 Patients and Balance Evaluation


30 patients (12 M, 18 F, mean age 66,8 ± 8,7) diagnosed with PD in stage 3 of
Hoen&Yahr (mean UPDRS III 18.8±10.5) according to the UK Brain Bank
criteria underwent clinical and instrumental evaluations at the beginning (T0) and
at the end (T1) of the MIRT. Berg Balance Scale (BBS) was performed to assess
static and dynamic balance abilities. In order to determine some variables as an
index of postural stability, we used a stabilometric platform with standardized
method. With respect to the average centre of gravity the standard deviation (SD)
Measuring the Effectiveness of an Intensive Rehabilitation Treatment 371

of trunk sway (total, in antero-posterior [AP] and in medio-lateral [ML] direction)


were calculated. We have also obtained a statokinesigram, that is the layout of a
line connecting the successive positions of the center of pressure during the
recording, and the area of the ellipse containing 90% of the sampled positions of
the center of pressure. These measurements were calculated with open eyes (OE),
and while the patient was performing a cognitive task (counting, [OEC]). All
physical measurements were obtained during the ON phase of levodopa
medication and at the same time of the day to reduce the influence of medication
fluctuations.

2.3 Statistical Analysis


Statistical analysis with Wilcoxon signed rank test for non parametric data was
performed to analyze differences between T0 and T1 values of all variables. Data
are presented as mean ± SD. Results were considered statistically significant for
p < 0.05.

3 Results

We found that in patients who underwent MIRT, BBS values were significantly
increased at T1 respect to T0 (52.60±10.73 vs 46.56±11.74, p <0.0001), with a
mean BBS increase of 6.03±4.18. Statistical analysis showed significant
differences in the SD of trunk sway between T0 and T1. In particular, PD patients
had significantly lower values of AP and ML SD with EO at T1 respect to T0 (AP:
4.4±2.1 vs 6.0±3.3, p=0.021; ML: 4.2±2.3 vs 5.6±3.1, p=0.034). Also the values
of the area of the ellipse were significantly lower at T1 than at T0 (400,0 mm2 vs
714,1 mm2, p=0,015). No statistically significant differences were found in OEC
parameters.

4 Discussion and Conclusion

Taken together, these data indicate a global improvement of trunk stability after
MIRT. These preliminary results are consistent with literature data and confirm
the disruption of the complex mechanisms of balance control in PD.
There is increasing evidence that physical therapy can improve postural
stability and reduce the risk of falls: our study, although preliminary, individuates
a useful tool to quantify the amount of disability and to monitor the effectiveness
of a rehabilitation treatment through several parameters. The mechanisms of
posture and balance control are extremely complex. The described rehabilitation
treatment seems to act on the central and peripheral factors. Probably, this dual
action is involved in the modulation of these factors and it is responsible for the
improving of balance control. The above conclusions need to be taken cautiously
372 D. Ferrazzoli et al.

because of the limited size of our sample, and should be confirmed in a larger
study. Nevertheless, we are confident that our findings will provide new
knowledge and highlight the importance of an early balance training in PD.

References
[1] Kim, S.D., et al.: Postural instability in patients with Parkinson’s disease:
Epidemiology, pathophysiology, management. CNS Drugs 27(2), 97–112 (2013)
[2] Schoneburg, B., et al.: Framework for understanding balance dysfunction in balance
dysfunction in Parkinson’s disease. Mov. Disord. 28(11), 1474–1482 (2013)
[3] Deliagina, T.G., et al.: Nervous mechanism controlling body posture. Physiol.
Behav. 92(1-2), 148–154 (2007)
[4] Frazzitta, G., et al.: Short-and long-term efficacy on intensive rehabilitation treatment
on balance and gait in parkinsonian patients: A preliminary study with a 1-year follow-
up. Parkinsons Dis. 2013, 583278 (2013), (Epub. May 26, 2013)
Detection of Common Synaptic Inputs Shared
by Populations of Motor Neurons Innervating
Different Muscles: Methodology and
Considerations for Neuroprosthetic Treatment
of Tremor

Juan Álvaro Gallego1, Jakob Lund Dideriksen2, Ales Holobar3,


Juan Pablo Romero4, Julián Benito-León4, Félix Bermejo-Pareja4,
José Luis Pons1, Eduardo Rocon1, and Dario Farina2
1
Bioengineering Group, Spanish National Research Council (CSIC),
Madrid 28500 Spain
ja.gallego@csic.es
2
Department of Neurorehabilitaion Engineering,
Bernstein Center for Computational Neuroscience (BCCN),
University Medical Center Goettingen, Georg-August University,
Goettingen 37075 Germany
3
Faculty of Electrical Engineering and Computer Science,
University of Maribor, Maribor SI-2000 Slovenia
4
Dept. of Neurology, University Hospital “12 de Octubre,” Madrid 28041 Spain

Abstract. A large proportion of tremor patients do not benefit from any treatment.
This is partly motivated by the fact that current therapies may not be sufficiently
specific because the pathophysiology of each type of tremor is not fully
understood. In particular, the ultimate mechanisms (common synaptic inputs) that
generate the tremorogenic muscle activity are yet unknown. Therefore, in this
paper we present a novel methodology to investigate whether motor neuron pools
innervating different muscles receive the same common synaptic inputs, and what
are their properties. We illustrate the potential of the approach by demonstrating
that motor neuron pools innervating antagonist muscles of one essential tremor
and one parkinsonian patient share the same common synaptic input at the tremor
frequency. We finish discussing what are the potential implications of our findings
when designing a neuroprosthesis for tremor suppression based on the stimulation
of afferent pathways.

1 Introduction

Pathological tremor is the most common movement disorder, affecting up to 14.5


% of people with age 50–89 years [1]. It arises from a number of conditions being
essential and parkinsonian tremors the most prevalent. In spite of recent advances,

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 373
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_58, © Springer International Publishing Switzerland 2014
374 J.A. Gallego et al.

much is yet unknown about the pathophysiology of tremors [2], [3], which
translates into a lack of effective treatment for many patients.
Most types of tremor are caused by pathological oscillatory activity originating
at different brain structures [2], [4]. Projections of these oscillations interact with
other circuitries of the nervous system (e.g., spinal afferents) to determine the
properties of the tremulous movement [4]. This is ultimately mediated by the
integration of the synaptic inputs they provide by the population of motor neurons
that innervate the affected muscle [5].
Evidences gathered from the analysis of the coherence between interference
surface EMG signals [6]–[8] suggest that in most cases antagonist muscle pairs
receive the same common synaptic input related to tremor [9]. However the use of
this methodology suffers from intrinsic drawbacks, mainly: 1) when detecting
common inputs the signal-to-noise ratio of the surface EMG is significantly lower
than that of the pooled motor unit discharges [9], and 2) the analysis of EMG data
from neighboring muscles is limited by cross-talk, a physiological phenomenon
that cannot be successfully eliminated with current techniques [10], [11].
Because the surface EMG is used as an estimator of spinal motor output [11],
[12], it is not surprising that recent studies show that the direct characterization of
the neural drive to muscle as the pooled discharges of several motor units
immediately circumvents limitations arising from surface EMG analysis [13],
[14]. This approach also yields a better estimate of muscle force variability [15]
and permits to identify common synaptic inputs more accurately [5], [9], [16], as
mentioned above. This is partly explained because motor unit analysis
circumvents issues related to motor unit action potential shape and size, and their
cancellation in the surface EMG [11], [12], [14].
Here we present a new methodology to investigate the existence of common
synaptic inputs shared by motor neuron populations innervating different muscles
that circumvents the abovementioned limitations because it is based on motor unit
spike train analysis. Our approach also provides information about characteristics
of the shared common synaptic inputs. We illustrate the feasibility of the approach
by analyzing data from one essential tremor (ET) and one Parkinson’s disease
(PD) patient. We interpret our findings in the contexts of: 1) furthering our
understanding of tremor neurophysiology, and 2) development of a
neuroprosthesis for tremor suppression through the stimulation of afferent
pathways.

2 Detection of Common Synaptic Inputs Shared by


Populations of Motor Neurons

It has been shown that building a composite spike train (CST) as the pooled
activity of several motor units improves the estimation of the output correlation
between motor unit discharges [17]. Further, the average coherence between CSTs
of motor units innervating a muscle reflects the existence, and frequency content
of eventual common synaptic inputs to the muscle [17]. Here we extend this
Detection of Common Synaptic Inputs Shared by Populations of Motor Neurons 375

methodology and propose to identify the existence of common synaptic inputs


shared by populations of motor neurons innervating different muscles by
computing the coherence, , between the CSTs that represent each the neural
drive to one of the two muscles considered:
| 12 |
| 11 || 22 |
1 

where is the cross-power spectrum of the neural drives to muscles 1 and 2, and
and the auto-spectrum of the neural drives to muscle 1 and 2.
The frequency of the shared common synaptic inputs (i.e. significant peaks in
the coherence spectrum) is directly computed from the coherence spectra. This
permits to elucidate their origin, because tremors normally occur at a higher
frequency (typically 3–12 Hz [18]) than that employed for the transmission of
voluntary motor commands (< 2–3 Hz [17], [19]). The amplitude of the coherence
at each frequency represents to what extent the common synaptic input is shared
by the CSTs.

Fig. 1 Example of neural drive to muscle defined as the spike trains of the 4 motor units
identified for this muscle group (right flexors, PD patient). From top to bottom the panels
show: 1) the discharges of all the motor units identified (panels MU1–MU4 [for motor unit
1, paired discharges are marked with a circle on top]), 2) the resultant CST and its filtered
version (3–10 Hz, bandpass) to represent the tremor input to the muscle (panels CST and
filt CST respectively), and 3) the power spectral density (PSD) of each of the motor unit
spike trains (gray) and of the CST (black). The peaks at the tremor frequency and its
harmonics become stronger when pooling the 4 motor units in the CST.
376 J.A. Gallego et al.

3 Methods

3.1 Patients
We present results for two patients, one suffering from PD (65 years-old male
suffering from severe tremor at the right limb), and the other from ET (75 years-
old male suffering from severe bilateral tremor). The ET patient was diagnosed as
definite ET according to the criteria of the Tremor Investigation Group [18], and
exhibited no sign of parkinsonism. The PD patient fulfilled the London Brain
Bank criteria [20]. None of them had a neurological condition except for that
causing the tremor. Both patients were informed beforehand and gave their written
informed consent to participate in the study. The protocol was approved by the
ethical committee at Hospital Universitario “12 de Octubre,” Madrid, Spain,
which warranted its accordance to the Declaration of Helsinki.

3.2 Recordings and Procedure


Hand tremor was recorded bilaterally using two multichannel surface EMG
electrodes (13 x 5 detection points; one missing) with an inter-electrode distance 8
mm (LISiN–OT Bioelettronica, Torino, Italy). Each of the grids was centered
above the extensors and flexors of the wrist. Previously, the skin was abraded with
gel (Meditec-Pharma, Parma, Italy) and cleansed afterwards. EMG signals were
amplified (EMGUSB2, OT Bioelettronica, Torino, Italy), band-pass filtered (10–
750 Hz), and sampled at 2,048 Hz by a 12-bit A/D converter. A wrist bracelet
soaked in water served as common reference. The experiments were performed at
Hospital Universitario “12 de Octubre,” Madrid, Spain. The data were analyzed
using Matlab (The Mathworks Inc., Natick MA, USA).
Patients were sitting in a comfortable chair during the recordings. In the case of
the ET patient, we elicited postural tremor bilaterally by asking him to keep both
hands extended parallel to the ground, with the fingers outstretched, while the
forearms were supported by an armrest. For the PD patient, we elicited rest tremor
by asking him to leave the hands hanging freely while the forearms were lying on
the armrests. Both patients performed one 4-min repetition of the corresponding
task. For the analysis we chose the longest window with stable motor unit
discharges and visible tremor.

3.3 Surface EMG Decomposition


We identified motor unit spike trains from the multichannel surface EMG signals
using the convolution kernel compensation (CKC) technique [21]. The CKC
algorithm has been both largely validated in healthy subjects (e.g., [22]), and in
synthetic and experimental tremor signals [5], [23]. Automatically produced
decomposition results were manually verified by an experienced operator (Fig. 1).
Detection of Common Synaptic Inputs Shared by Populations of Motor Neurons 377

Among the motor unit spike trains identified, we only considered for the analysis
those that were detected with great accuracy (pulse to noise ratio ≥ 26 dB [24]
after manual inspection), and that were detected during ≥ 85 % of the 1-s epochs
that formed the analysis window.

3.4 Data Analysis


We first calculated, for all muscle groups analyzed, the properties of the common
synaptic inputs to each motor neuron pool, following the methodology described
in [17]. Then we employed the technique here proposed (described in Section 2) to
verify if pairs of motor neuron pools innervating antagonist muscles received the
same tremor-related common synaptic input. We also verified if the voluntary
drive was shared across motor neuron pools.
The coherence function was calculated in disjoint 1-s windows (Hann window,
zero-padded) as proposed in [25]. Peaks in the coherence spectrum were accepted
as representing a common synaptic input if their magnitude exceeded a confidence
threshold, calculated following [26].
The significance level for coherence was set to = 0.01; for other statistical
tests we considered = 0.05. All results are reported as mean ± SD.

4 Results
The left extensors and flexors from the PD patient were discarded from the
analysis because he did not exhibit tremor in that limb. In total, we detected 37
motor units in the 6 remaining muscles groups (mean per group: 6.2 ± 3.1; range
2–10). Paired and tripled motor unit discharges were clearly visible, as expected
from previous works [5] (see examples in Fig. 1). The average duration of the
analysis windows was 29.1 ± 1.2 s (range 28–30 s).
The spectrogram of all the motor unit spike trains exhibited a clear peak at the
tremor frequency, which height varied across motor units. The height of this peak
(and its harmonic, if present) became larger as CSTs were formed by pooling the
discharges of all the motor units identified (Fig. 1). This was expected because
motor unit pooling improves the sampling of the common voluntary drive [16],
[17], and the tremor drive [5].
When investigating the common synaptic inputs to each motor neuron pool, all
6 muscles analyzed received a strongly shared input at the tremor frequency
(coherence: 0.950 ± 0.029; range: 0.904–0.978), which appeared together with a
weaker (P = 0.002; Wilcoxon signed-rank test) common voluntary drive
(coherence: 0.513 ± 0.121; range: 0.387–0.685) (Fig. 2). Notice that the coherence
was very strong over the entire frequency band (Fig. 2) because the motor unit
spike trains were highly correlated (Fig. 1). As expected, the coherence peaks
representing the tremor-related common synaptic input to the muscle appeared at
the same frequency as the tremorogenic neural drive did in the power spectral
density of the CST (Fig. 2).
378 J.A. Gallego et al.

Fig. 2 Common synaptic inputs shared by populations of motor neurons innervatin


antagonist muscles. The figure shows the results for the PD and the ET patient. For each of
them, we show from top to bottom: 1) the common synaptic inputs to each motor neuron
pool (in gray; mean ± SD) and the power spectral density of the CST (dashed black lines),
together with the amount of motor units deteced, and 2) the properties of the common
synaptic inputs shared by the motor neuron pools (solid black lines). The confidence limits
(P < 0.01) for the coherence are shown as dotted black lines. CSI = common synaptic input.

All 3 pairs of motor neuron pools innervating antagonist muscles shared the
same common synaptic input at the tremor frequency (Fig. 2). Such shared input
was very strongly shared in all 3 cases analyzed (coherence: 0.854 ± 0.109; range:
0.730–0.930). For the ET patient it appeared together with a weaker (coherence:
0.205 and 0.260 for the left and right arms respectively) shared common input at
frequency < 2–3 Hz [17], [19].
Detection of Common Synaptic Inputs Shared by Populations of Motor Neurons 379

5 Discussion

We have presented a new approach to investigate the existence and properties of


common synaptic inputs that are shared by motor neurons pools innervating
different muscles. Given that it is based on the definition of the neural drive to
muscle as the pooled discharges of several motor units, this methodology
intrinsically circumvents many limitations derived from traditional interference
EMG analysis, as discussed in the Introduction.
We illustrate the performance of the technique by demonstrating that motor
neurons innervating antagonist muscles of two tremor patients (suffering from ET
and PD respectively) received a shared common synaptic input related to tremor.
Although we present results for only two patients, we anticipate this methodology
will help to better understand the neurophysiology of healthy and patho-logical
conditions, and eventually lead to the development of novel motor neuroprostheses.
Next we summarize some ideas about these topics for the case of tremor.

5.1 Implications for Tremor Neurophysiology


Our analysis directly proves that antagonistic motor neuron pools share the same
common synaptic input at the tremor frequency, as indirectly suggested in previous
studies using the interference EMG [6]–[8]. This implies that the same oscillator is
projected to both muscles, although our experimental setup impedes assessing
whether such projection is purely spinal, supraspinal, or a combination of both. In
this regard, in a previous study on ET patients we showed, using concurrent EEG
recordings, that corticospinal projections alone are unlikely to account for the
observed common synaptic input strength at the tremor frequency [5]. We further
suggested, given that Ia fibers provide common projections to the motor neuron
pool [27], that primary spindle afferents may selectively enhance the tremorogenic
descending input, largely contributing to the generation of the tremor as suggested
for physiological tremor [28]. Analogously, relying on the fact that the observed
tremorogenic common inputs were strongly shared (average: 0.854 ± 0.109; notice
they range from 0 to 1) we speculate that corticospinal projections are unlikely to
fully explain our findings themselves. The reason for this is that descending
corticospinal projections normally occur through a population of interneurons [29]
that distort the linear transmission of neural commands [30] and thus render the
existence of such strong common inputs originating uniquely from supraspinal
pathways unlikely. We thus interpret our results as reflecting that homonymous
afferent pathways to antagonistic motor neurons pools contribute to the
manifestation of the tremor via their mechanical link.
Interestingly, we observed no qualitative differences between the ET patient
and the PD patient, in spite of the different pathophysiology of both diseases [2],
[4], and the fact that they behave differently under inertial loading [31] (which
alters peripheral circuitries). However, the study needs to be replicated with a
sufficiently large sample of patients to investigate potential discrepancies.
380 J.A. Gallego et al.

5.2 Implications for Neuroprosthetic Tremor Treatment


Our hypothesis that spinal afferents contribute significantly to the generation of
tremor in ET and PD encourages the development of neuroprostheses that target
these pathways as a means to suppress the tremor. Such a solution would improve
the usability of current FES neuroprostheses, because it would be more
comfortable, and would avoid the potential effects of muscle fatigue. For example,
we hypothesize that tremor can be attenuated by means of low-level stimulation of
Ia fibers, aiming to simultaneously increase motor unit excitability in the
homonymous motor neuron pool and decrease motor unit excitability in the
heteronymous motor neuron pool [32].
The hypothesis that afferent pathways contribute to determine tremor severity
also helps to interpret some of the results obtained with prototypes for tremor
suppression through mechanical loading [31]. For example, when suppressing
upper limb tremor through modulated muscle co-contraction we observed that
when tremor amplitude is decreased to a very mild level, it needs a few seconds to
start going back to its originally higher amplitude [33]. This may be interpreted as
the spinal afferent circuitries acting as a positive feedback loop that amplifies the
descending oscillations [5], [34].

Acknowledgment. This work has been funded by the EU Commission through the grant
ICT-2011-287739, “NeuroTREMOR.”

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A Novel Robot-Aided Therapy for Shoulder
Rehabilitation after Stroke: Active-Assisted
Control of the RehaArm Robot Using
Electromyographic Signals

Clara Genna1, Strahinja Dosen2, Liliana Paredes3, Andrea Turolla3,


Bernhard Graimann1, and Dario Farina2
1
Otto Bock HealthCare GmbH,
Duderstadt, Germany
clara.genna@ottobock.de
2
Department of Neurorehabilitation Engineering,
University Medical Center Göttingen, Georg-August
University, Göttingen
dario.farina@bccn.uni-goettingen.de
3
Laboratory of Kinematics and Robotics,
IRCCS San Camillo Hospital Foundation, Venice, Italy
andrea.turolla@ospedalesancamillo.net

Abstract. In this work, we introduced a novel experimental protocol for shoulder


rehabilitation after stroke using RehaArm, a three Degrees of Freedom compliant
robot. We implemented a control framework based on sensorimotor integration by
developing an electromyographic (EMG) driven operation of the robot. EMG
signals from five muscles were collected during experimental protocol consisting
of four principal rotations of the shoulder joint. The subject movement intention
was detected by monitoring the EMG activity of the primary agonist muscle for
the selected task. Whenever the EMG activity was above the threshold set to 20%
of maximum voluntary contraction, the robot provided assistive forces towards the
target position. The system was tested in four healthy subjects and one stroke
survivor. All subjects were able to produce continuous EMG activation in target
muscles in order to smoothly control the robot. Healthy subjects exhibited normal
on-off pattern of activity, while in the stroke patient an abnormal activation was
observed characterized by a loss of selective recruitment of some muscles. The
results of this preliminary evaluation suggested that the developed closed loop
framework is a suitable platform for novel robotic treatments for shoulder
rehabilitation after stroke.

1 Introduction
After a brain damage such as stroke, patients go through an intensive
rehabilitation program comprising different therapeutic exercises during which the
patient and therapist engage in a physically demanding one-to-one manual

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 383
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_59, © Springer International Publishing Switzerland 2014
384 C. Genna et al.

interaction. This is a long and arduous process for both stroke survivors and
therapists. Recently, a novel approach in stroke rehabilitation is the robot-aided
therapy than can replicate intensive physical treatments situating the therapist as
supervisor of the therapy. Further, it was demonstrated that brain plasticity and
functional recovery can be induced if the robot-based training involves repetitive
task-oriented movements combined with significant attention demands [1]. Recent
developments in the robot rehabilitation have been directed towards the so-called
active-assisted control mode that seems to lead more significant improvements
when compared to Continuous Passive Movement (CPM) treatments [2]. In this
approach, the subject is actively involved in the exercise, and less or more
demanding tasks (e.g., assistive vs. resistive mode) can be programmed according
to the level of the patient’s motor impairment. A common example of active–
assisted control in robot rehabilitation is the electromyography (EMG)–driven
robot [3]. The subject’s movement intention can be inferred from EMG since
these signals appear prior to an action initiation. Therefore, the detection or even
the prediction of movement can be implemented by acquiring and processing the
EMG. The goal of this preliminary work was to implement and test EMG driven
control of the RehaArm robot (FerRobotics Compliant Robot Technology GmbH,
AT), a novel compliant robot for shoulder rehabilitation. The robot was integrated
within a closed loop framework and an experimental protocol consisting of four
principal shoulder rotations was performed by healthy subjects and one stroke
patient. During the experiment, EMG activity from five shoulder muscles was
recorded for online movement detection.

2 Methodology

2.1 RehaArm in Closed-Loop Control Framework


RehaArm is pneumatic-driven robot designed specifically for the shoulder
rehabilitation (see Figure 1A). The device has three Degrees of Freedom (DoFs)
where each DoF corresponds to one of the principal rotations of the shoulder:
horizontal abduction/adduction (H-ABD), abduction/adduction (ABD) and
internal/external rotation (IE) (red, green and yellow rotation axis in Figure 1A,
respectively). The maximum movement speed of the robot is 5°/s and the default
range of motion for H-ABD, ABD and IE DoFs are 135°, 160° and 170°,
respectively. RehaArm can be calibrated to support the subject arm against gravity.
The robot joints are actuated by the pairs of antagonistic artificial muscles (Festo,
UK). The interaction with the robot is soft and safe due to the inherently compliant
properties of the artificial muscles which are able to absorb and/or reduce the
contact forces between the subject and robot. Figure 1B shows the closed-loop
control framework that we implemented for the execution of subject-driven
exercise protocols using the RehaArm robot. The communication between the
A Novel Robot-Aided Therapy for Shoulder Rehabilitation after Stroke 385

robot and a host computer was implemented in Matlab using unidirectional TCP/IP
connections in order to send the desired trajectory (e.g., DoF angles) and receive
sensor data for each DoF sampled at 100 Hz (e.g., DoF angles and torques).
Concurrently, the EMG activity was recorded by means of a multichannel EMG
amplifier that was connected via USB to the same host computer. All tests have
been done in a clinical environment and therefore a simple and user friendly robot
control and configuration program has been developed. The program allows
connecting to the robot and/or the EMG amplifier, so that each component can be
individually controlled, configured and tested. Once the robotic arm is attached to
the subject and before running the protocol, several calibration steps are
implemented. First, the robot moves to a predefined reference position and starts an
internally programmed calibration procedure for the gravity compensation. The
therapist then activates the soft mode and manually moves the robot to the limits of
the subject’s range of motion along each DoF, recording the limit positions that are
considered for the next exercises. Finally, EMG baseline for the relaxed subject can
be recorded as well as the maximum voluntary contraction (MVC). The therapist
can now select an exercise task and training modality from the respective menus.
The modality can be passive or active. The passive mode means that the robot
moves the arm of the relaxed subject along a trajectory, while in the active mode
the robot drives the subject arm but only if his/her intention to move is detected.
The subject movement intention can be detected by assessing the subject-robot
interaction force (torque-driven control) or the muscle activity (EMG-driven). So
far, two types of protocol have been implemented and controlled in both passive
and active mode. The first one is a single DoF activation in which the subject
performs movements along the only DoF selected. In the second type, the subject
performs movements along trajectories comprising a sequence of straight segments,
i.e., the exercise therefore involves a sequential activation of several DoFs. When
the desired parameters are selected (i.e. task and modality), the therapist can run the
protocol. Visual feedback shown during the exercise is depicted in Fig. 1C-1 and
1C-2 for the single DoF and sequential multi-DoF activation protocols,
respectively. In Fig. 1C-1, the red ball represents the current position whereas the
green ball is the target, and the task is to move the robot from the start to the end of
the trajectory (gray pathway). The trajectory is oriented according to the selected
DoF (i.e., horizontal line for flexion/extension, vertical line for adduction
/abduction). In the multi-DoF task (Figure 1C-2), the goal is to write the word
‘CIAO‘ on the blackboard where the letter segments correspond to the movements
along a single DoF. Importantly, new exercises can be defined easily by changing
the shape and/or lengths of the segments. If the robot is in the active mode, a
feedback about the current level of muscle activation is provided (see Figure 1C-3).
In this paper, we will show only the results related to single DoF movements for
EMG driven robot.
386 C. Genna et al.

Fig. 1 RehaArm interfacing in closed loop framework. A) RehaArm robot and the three
rotation axes (red, green and yellow for H-ABD, ABD and IE DoF, respectively). B)
Scheme of the closed-loop control framework. C) Visual Feedback. 1 and 2 represent the
position feedback for the single DoF activation and sequential DoF by DoF activation,
respectively. In figure C2, the blue and green arrows represent the flexion (left) / extension
(right) and abduction (up) / adduction (down) movements, respectively. Panel C3 shows the
EMG feedback representing the actual level of muscle activation in per cent of MVC.

2.2 Experimental Protocol


Four healthy subjects (three men, mean age = 29 yrs; one woman, 27 yrs) and one
stroke survivor (67 yrs, 4 months after stroke, lesion in left hemisphere) have been
recruited in IRCCS San Camillo Foundation (Venice, Italy). The experiment was
approved by the Ethical Committee in Venice. The upper limb motor deficit of the
stroke patient was evaluated by means of Fugl-Meyer scale for upper limb motor
impairment (FM = 53 out of 66) and Modified Ashworth Scale for spasticity (MAS
= 0 out of 5 for each muscle). The experimental protocol consisted of exercises
along four principal shoulder rotations as reported in Table 1 to perform in active
mode.
Five repetitions were performed along each DoF in each direction in order to
avoid fatigue and therefore the whole protocol lasted approximately one hour.
During the exercises, the EMG activity of five shoulder muscles (Pectoralis,
Anterior, Middle and Posterior Deltoids and Teres Major) was recorded in bipolar
configuration (SENIAM guidelines for superficial electrode placement [4]).

Table 1 Experimental protocol

Involved Primary agonist


Task
DoF muscle
Horizontal Abduction / Pectoralis Major /
H-ABDa
Adduction Posterior Deltoid
Middle Deltoid /
Abduction / Adduction ABD
Teres major
Anterior Deltoid /
Flexion / Extension H-ABDa
Teres Major
Anterior Deltoid /
Internal/External Rotation IE
Posterior Deltoid
a H-ABD DoF is involved in both tasks with movements parallel to the axial and sagittal planes, respectively
A Novel Robot-Aided Therapy for Shoulder Rehabilitation after Stroke 387

The EMG signals were amplified with a gain of 2000, band-pass filtered
(bandwidth 10–500 Hz), and sampled at 2048 Hz using a multichannel EMG
amplifier (OT Bioelettronica, Turin, Italy). A reference electrode was placed
around the wrist.

2.3 Active Control by EMG Signals


A predefined trajectory was programmed for each DoF in Table 1 according to the
range of motion of each subject. Continuous EMG-driven control of the robot was
implemented to move the robot along the trajectory. When the movement
intention of the subject was recognized by the system, the next trajectory point
(i.e. next angle position for each DoF) was sent to the robot (see Figure 1B). The
robot started moving and provided an assistive force towards the new reference
position. Importantly, the subject had to provide the command continuously in
order to keep the robot moving. Otherwise, if the movement intention was not
detected, the robot stopped at the current position. For the intention detection, we
computed the root mean square (RMS) in intervals of 100 ms of the EMG signal
acquired from the primary movement agonist for the current task. The muscles
were selected taking into account the kinesiology of the shoulder (see Table 1).
The obtained RMS value was compared to the threshold set to 20 % of MVC in
order to avoid fatigue. If the current value was above the threshold, the movement
intention was detected triggering the robot assistance.

Fig. 2 EMG activation during abduction from a representative healthy subject. A) When the
gradually increasing EMG crossed the threshold (panel 1, point indicated by the blue
arrow), the robot started moving (panel 2, blue line) and pushing the subject arm (panel 2,
green line). B) EMG activations during sequential repetitions of abduction/ adduction. *The
scale of Pectoralis and Teres Major was increased in ratio 1:3. In the bottom, the angle
position of ABD-DoF is depicted.
388 C. Genna et al.

2.4 Offline EMG Processing


The mean value across trials of Root Mean Square (RMS) was computed for each
muscle in order to evaluate the level of muscle activation. In particular, the relative
increment of RMS between two different movements in the same task (e.g.
abduction (RMS1) / adduction (RMS2); flexion (RMS1) / extension (RMS2);
internal (RMS1) / external (RMS2) rotation) was calculated for each muscle as
following:
RI = 100*(RMS1 – RMS2)/RMS1 (1)
Positive values of RI index indicate that the overall muscle activity was higher
in the movement 1 respect to the activity during the movement 2. On the other
hand, negative values indicate higher muscle activation in the movement 2 respect
to the activity of the same muscle in the movement 1. Finally, the envelope shown
in Figure 2 A1 was computed by high pass filtering the EMG signals at 50 Hz (3rd
order Butterworth zero phase filter), rectifying and then low pass filtering at 3 Hz
(3rd order Butterworth zero phase).

3 Results

All participants were able to accomplish the full experimental protocol and
generate the desired level of muscle activity to trigger and move the robot,
successfully reaching the desired final position in all exercises in Table 1. In
particular, an example of the active control by EMG described in the previous
paragraph is shown in Figure 2 A1. The blue arrow shows the time instant when
the gradually increasing muscles activity (red line) crossed the threshold (black
dotted line). In that moment, the robot started moving (see Figure 2 A2) and
driving the subject’s arm by a gradual increase in the recorded interaction torque
(Figure 2 A2). Figure 2B shows a representative example of EMG generated in the
muscles of a healthy subject performing abduction/adduction movements
continuously. During abduction, the primary agonist muscle is Middle Deltoid
(see Table 1). Indeed, while the subject was lifting the arm, this muscle showed
higher activation (RI index = +97.1%). Note that Anterior and Posterior deltoid
were also activated due to the their synergistic role in the movement and shoulder
stabilization [5] and therefore the RI indexes were positive for both Anterior (RI =
+94.1%) and Posterior Deltoid (RI = +83.7%). On the other hand, Teres Major
assisted Pectoralis in adducting the shoulder [5] and therefore both muscles were
selectively activated only during those movements. The RI was negative for those
muscles, indicating higher activation in adduction respect to abduction movements
(RI Pectoralis = -74.7% and RI Teres Major = -108.3%). Further, the observed
higher activation of Middle Deltoid in respect to Teres Major and Pectoralis could
depend on the highest muscle force-generating properties of the deltoids due to the
A Novel Robot-Aided Therapy for Shoulder Rehabilitation after Stroke 389

largest volume fraction [6]. Indeed, the scales of Pectoralis and Teres Major were
increased three times respect to the other muscles (Figure 2B). Finally, the angle
positions of figure 2B for ABD – DoF demonstrate that the subject was able to
generate fluid movements producing consequently a smooth trajectory.
Figure 3 shows the sequential trials of the stroke patient during
abduction/adduction exercises. The subject successfully kept the EMG of primary
muscles, i.e. Middle Deltoid for abduction and Teres Major for adduction, above
the threshold producing a continuous movement along the trajectory. However,
only Deltoid muscle group exhibited the clear on-off activation congruent with the
current task (i.e., active during abduction and silent otherwise) reporting properly
positive RI indexes (RI Anterior = +93.7%, RI Middle = +88.3%, RI Posterior = +
77.2%). On the other hand, Teres Major and Pectoralis were activated non-
selectively, i.e., during both exercises and it could be related to the inability of the
stroke survivor to coordinate the muscle activity due to the loss of dexterity after
stroke [7]. Thus the subject could have applied some compensation strategies in
order to accomplish the task resulting in abnormal pattern of muscle activations.
Indeed, RI index was positive for both Pectoralis (+1.5%) and Teres Major
(+39.6%) demonstrating that the activity of those muscles was not silent during
shoulder abduction as expected by the role of antagonists to this movement [5].
Furthermore, it has also been demonstrated that stroke leads to physical disability
in upper limb due to weakness and muscle co-contraction, which correlate
significantly with the motor impairment [8]. Therefore, the observed unexpected
activations could reflect an abnormal co-contraction of agonist (i.e. Middle
Deltoid) and antagonist (i.e. Teres Major / Pectoralis). This co-activation was
moderate due to the lower motor impairment of the stroke survivor (FM = 53 out
of 66). We provided a representative example of one volunteer and the stroke
patient only in one task, but the similar results with respect to main
agonist/antagonist muscles have been observed in all subjects and exercises in
Table 1.

Fig. 3 An example recording of muscle activity in the stroke survivor performing EMG-
driven shoulder abduction/adduction. Note the non-selective recruitment of Teres Major
and Pectoralis muscles which are active at similar levels both during Abd and Add
movements. Notation: Abd and Add mean Abduction and Adduction, respectively.
390 C. Genna et al.

4 Discussion

Rehabilitation robots can contribute significant advantages when included in


stroke rehabilitation programs [1]. Indeed, robot can provide intensive,
reproducible and task-specific movements customizing the interventions based on
individual physical impairments. Moreover, robotic rehabilitation can generate
complex and controlled multisensory stimulation of the patients providing both
active control of the device and multimodal feedback over different sensory
channels such as haptic, visual, and auditory [9]. In this work, our aim was to
introduce a novel experimental protocol with the RehaArm robot for the shoulder
rehabilitation after stroke. RehaArm is a three DoFs pneumatic-driven robot that
allows smooth movements of the shoulder due to its inherently compliant
properties and therefore it is very well indicated for treating shoulder
complications such as subluxation and pain. The novel approach in our protocol
was to implement the active-assisted control of the RehaArm robot by EMG
signals, thereby providing sensorimotor integration during exercises. We received
positive verbal feedback from both the healthy subjects and the stroke patient.
They reported that RehaArm is a comfortable robot, the task and visual feedback
were intuitive and easy to understand, and the robot was responsive, successfully
reacting to a low-effort triggering through EMG control and providing assistance
to the subject. Indeed, by observing the experimental session and also the signal
traces, we could see that the subjects easily interacted with the robot receiving the
proper assistive force by producing EMG activation in the primary agonist muscle,
i.e., the generated EMG was continuous and the angle trajectory (robot movement)
was smooth. However, more experiments with stroke survivors need to be
performed in order to assess the efficacy of the proposed protocol as treatment
after stroke. Subsequently, additional exercises could be introduced for a full
rehabilitation programs, e.g., including multiple DoF activations of the robot or
movements along arbitrary trajectories in 3D spaces. On the other hand,
complicate task could require more sophisticated algorithms for intention
detection such as pattern recognition or simultaneous and proportional control [3].
Finally, a crucial point in robot rehabilitation concerns also the visual feedback. In
this work, we provided simple visual feedback (see Figure 1C) allowing the
subjects to monitor his/her progress and obtain a better control of the system.
However, more complex tasks (e.g., 3D movement) could require enriched
feedback such as a virtual reality environment. Therefore, the integration of
RehaArm in the virtual reality environment currently used with significant clinical
results at the San Camillo Hospital Foundation [11], is an important future step.
Finally, future analysis will consist in correlating the clinical scales of the stroke
survivors such as FM and MAS with kinematic and EMG data recorded during
robot assisted exercises. Indeed, the abnormal pattern of activation observed in
Figure 3 could be quantified using the index of co-contraction that when computed
longitudinally can provide important information about the motor recovery. For
instance, we could observe that a decrease of co-contraction index is in line with
A Novel Robot-Aided Therapy for Shoulder Rehabilitation after Stroke 391

an increase in FM score, highlighting the positive effects of the therapy under


investigation. In this way, a new tool of motor recovery assessment can be
provided to clinicians for a better understanding of stroke survivor progress during
rehabilitation programs.

Acknowledgment. The work is supported by MYOSENS, European Commission via the


Marie Curie program, Industrial Academia Partnerships and Pathways program (IAPP)
Grant No. 286208.

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(2011)
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(2000)
[8] Chae, J., Yang, G., Park, B.K., Labatia, I.: Muscle Weakness and Cocontraction in
Upper Limb Hemiparesis: Relationship to Motor Impairment and Physical Disability.
Neurorehabil. Neural Repair 16(3), 241–248 (2002)
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movement training after neurologic injury. J. Neuroeng. Rehabil. 6, 20 (2009)
[10] Nudo, R.J.: Functional and structural plasticity in motor cortex: Implications for
stroke recovery. Phys. Med. Rehabil. Clin. N. Am. 14, article ID 1, S57–76 (2003)
[11] Turolla, A., Daud Albasini, O.A., Oboe, R., Agostini, M., Tonin, P., Paolucci, S.,
Sandrini, G., Venneri, A., Piron, L.: Haptic-based neurorehabilitation in poststroke
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Comput. Math. Methods Med. 2013, 895492 (2013)
Analysis of Eye Movements, Kinematics and
Dynamic Aspects of Performance during
Activities of Daily Living in Stroke Patients

Philipp Gulde1, Charmayne Hughes1, Manish Parekh2, Martin Russell2,


Manuel Ferre3, Alan Wing2, Marta M.N. Bieńkiewicz1, and Joachim Hermsdörfer1
1
Technische Universität München, Lehrstuhl für Bewegungswissenschaft,
Georg-Brauchle Ring 60/62, 80992 München, Germany
p.gulde@gmx.de, joachim.hermsdoerfer@tum.de
2
University of Birmingham, The University of Birmingham, Edgbaston,
Birmingham, B15 2TT, UK
t3hmun@gmail.com, {M.J.RUSSELL,a.m.wing}@bham.ac.uk
3
Centro de Automática y Robótica, Universidad Politécnica de Madrid,
ETSI Industriales, 28040, Madrid, Spain
m.ferre@upm.es

Abstract. Apraxia is a neuropsychological symptom occurring as a consequence


of cerebrovascular accidents (CVA). Apraxic individuals suffer from compromised
access to motor concepts relevant for execution of activities of daily living (ADL).
The CogWatch project aims to develop an automatized rehabilitation system that
would facilitate performance of ADL. This study investigates signals which the
CogWatch system can use to recognize human actions and intentions as well as
apraxic errors during the performance of ADL tasks. Eye movements, hand
kinematics and the dynamics of manipulated objects are recorded during the task
of tea-making as an example of ADL. Data analysis is demonstrated using a
performance example and first analysis results are shown for movement paths and
times for the whole task and its sub-segments. CVA patients showed similar path
lengths but prolonged movement times and less executed sub-segments in
comparison with age-matched control subjects.

Keywords: Apraxia, CVA, Eye-movements, Kinematic analysis, ADL.

1 Introduction

Apraxia describes a symptomatic of loss of performance in using tools for goal


achievements, which can be caused by stroke [1]. In this study we try to identify
characteristics in apraxic patients’ eye movements as well as hand kinematics in
the everyday activity of tea making. In stroke patients, kinematics of upper limp
performance in ADL have been intensively tested in the context of paresis, effects
of apraxia and action disorganization syndrome on movement kinematics have
however only rarely been analyzed [7]. In particular, deficits in the different
segments of a multi-sequential ADL have not been evaluated so far. The study is

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 393
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_60, © Springer International Publishing Switzerland 2014
394 P. Gulde et al.

part of the CogWatch (www.cogwatch.eu) project that is to develop a technical


solution to promote independency in execution of ADL. The goal of the analysis of
eye movements, hand kinematic and dynamics of manipulated objects is to provide
an insight into apraxia in complex sequential tasks and support the development of
action recognition algorithms. Recent studies report 24% incidence of persistent
features of apraxia in CVA patients [2] and the project aims to deliver new
technological solutions that would promote devices that restore function or assist
task execution. Thus, offering a new approach to rehabilitation after dismissal from
the hospital unit.

2 Methods

2.1 Experimental Design


Task protocol is based on a tea-making scenario. Participants are instructed to
prepare a cup of tea using water, a kettle, teabags, milk and sugar (see Fig. 1).
Additional a distractor item (instant coffee jar) is placed on the working surface.
The task is performed six times, twice bimanual, twice with the ipsilesional hand
(dominant hand in control subjects) and twice with the contralesional hand (non-
dominant hand in control subjects), if possible.

2.2 Subjects
Until now 7 CVA patients (3 with left and 4 with right brain damage) were tested.
Patients were recruited from the Clinic for Neuropsychology at the Hospital
München-Bogenhausen in Munich. In addition, 9 age-matched controls were tested
in the same task scenario. Ethical approval was obtained by a local ethics
committee.

Fig. 1 Experimental setting


Analysis of Eye Movements, Kinematics and Dynamic Aspects of Performance 395

2.3 Apparatus
Subjects are asked to wear a SMI-ETG eye tracking device during the task
performance. The eye-tracking glasses incorporate a HD scene camera (sampling
rate 30Hz). Fixations are identified and assigned to fixated objects off-line. In
addition, positional data of both hands are recorded with the use of 5 Oqus Motion
Capture cameras (Qualysis) at a sampling frequency of 120Hz (three passive
markers are attached to each hand, mid-palm section). The mug, milk jug and
kettle (base and body) have force and acceleration sensors attached (custom made
by CogWatch technological partners, sampling rate 200Hz). Therefore additional
dynamic data are recorded from 4 object sensors and synchronized with the spatio-
temporal data from eye-tracking and motion capture. Figure 3 shows the
synchronized data streams of the fixations, coasters and motion capturing devices
for the tea making task in a healthy control subject during the bimanual task
condition.

2.4 Analysis
Data are segmented into discrete actions and analysed using three different
approaches:
• Analysis of fixations
• Analysis of kinematic and dynamic features
• Qualitative scoring of the performance

2.4.1 Segmentation

The whole task is segmented into the following action segments [4]:
1. Pour water in the kettle
2. Switch the kettle on
3. Place a teabag in the mug
4. Pour the heated water into the mug
5. Remove the teabag
6. Add milk
7. Add one sugar cube
8. Stir the tea

In a first step, boundaries of action segments are identified via the force and
acceleration signal of the object sensors (coasters) according to defined thresholds
of sensor signals [4]. The fine adjustment of action-segments is then performed
with the use of hand kinematics [5]. An example of all recorded signals and of the
resulting segments is shown in Figure 2 with numbers referring to the action
segmentation above.
396 P. Gulde et al.

Fig. 2 Example of segmentation via coaster data of the data streams for the task of making
a cup of tea (bimanual). In the upper row the fixated objects are indicated using a color
code (see legend on the right side). The lower two lines (yellow and green, baseline at ‘0’)
show the tangential velocities of right and left hand movements. In the blue and orange
lines of the graph the most relevant signals of the coasters are depicted (see legend on the
right side). The waiting time until the water in the kettle was boiling was cut from the data
stream as indicated by the thick vertical lines. The resulting duration of the task was 132s.
The numbers above the coaster signals refer to the action segments defined.

2.4.2 Analysis of Fixations

The number and duration of fixations is assessed for the complete task and for the
action segments The type of fixations can be determined using the categorization
of Land and Hayhoe (2001) (directing, guiding, checking, locating, see [3]).
Further, data are screened for irregularities in look-aheads and look-backs as well
as other disruptions in the task execution i.e. hand fixations.

2.4.3 Analysis of Kinematics

Positions and velocities of the hands are determined from the motion recordings
and smoothed using a 1s LOESS filter (‘local regression’). Following measures
are determined for the complete action and action segments (see Fig. 2):
• Velocity
o Maximum Peaks
o Mean peaks
o Number of peaks
• Movement times
• Path lengths
Analysis of Eye Movements, Kinematics and Dynamic Aspects of Performance 397

2.4.4 Scoring

Videos of the subjects’ performance are coded to define apraxic behavior.


Analysis assesses four error characteristics:
• Presence of errors
• Error patterns
• Eye movements in the context of timing of errors
• Sub-segment transitions analysis

The apraxic error classification will be based on the proposal by Hughes et al.
[6] with 12 categories of apraxic errors previously reported in the tea-making task.
The analysis of eye movements in error context will be focused on the exploration
eye fixation pattern before, during and after the occurrence of errors. The sub-
segment transition analysis will use Markov process-matrices to simulate tea-
making and will offer insight into error emergence.

Fig. 3 Example for the sub-segment 4 (‘Pour heated water into the mug’) extracted from the
synchronized data streams for the task of making a cup of tea (see Fig. 2). Eye tracking data
refers to fixations over time, coaster data to force and acceleration courses and hand
kinematics to velocities. The sub-action lasted 14s.

3 Analysis Example
Figure 3 shows an extract of Figure 2. The sub-segment 4 (‘pour the heated water
into the mug’) is shown for a control subject (bimanual performance). Note that
398 P. Gulde et al.

the kettle body’s acceleration sensor is giving distinct signals when the water
starts boiling and the kettle is lifted with the left hand. When the kettle is put back
on its base the irregular signals’ peaks are visible in the coaster data of the mug
and the milk’s carafe. While pouring the water into the mug, the mug’s force
sensor amplitude is raising due to the added water. Before lifting, the kettle is
fixated and while pouring, the subject is looking at the mug until putting back the
kettle. The segmentation is done via a threshold for the kettle base force sensors
(not displayed) and the kettle body acceleration sensors for segment 4 [4].

4 Progress
Action-segmentation and kinematic analyses have been done for path lengths and
movement times. Figures 4 to 6 show the normalized values (basis control) for the
control group (blue bars) compared with the CVA patients (orange bars) in
unimanual trials, where controls used their non-dominant hand and CVA patients
their ipsilesional hand. Analysis for segment 2 (‘switch the kettle on’) is missing
since it could not always be differentiated from segment 1 (‘pour water in the
kettle’).

Fig. 4 Path length and movement time for the complete task of tea-making before
segmentation. The values were normalized. T-test revealed asignificant difference for the
movement time with a p-value of .0004 and an effect size of .37.

Fig. 5 Comparison of path lengths for 7of 8 sub-segments in the tea-making task. T-test
revealed significant differences for segments 4 and 6 with p-values of .002 /.001 and effect
sizes of -.3 / .33.
Analysis of Eye Movements, Kinematics and Dynamic Aspects of Performance 399

Fig. 6 Comparison of movement time for 7of 8 sub-segments in the tea-making task. T-test
revealed significant differences for segments 1, 4, 6, 7 and 8 with p-values of .0003 /.001 /
.00002 / .003 / .001 and effect sizes of .39 / .39 / .47 / .32 / .53.

Figure 4 shows that patients needed longer to complete the whole task than the
control group. This prolongation could not be attributed to paresis since the
performance of the ipsilesional non-paretic hand is shown. Longer movement
times did not correspond with longer path lengths as obvious from figure 4. The
behavior of CVA patients therefore was characterized by slower but not by more
or longer hand movements. In the segmental analysis only two segments showed
significant differences in path lengths and five in movement times. Not every
segment was affected in the same manner. Interestingly, the sub-task of pouring
liquids into the mug revealed opposing effects for segment 4 (water) and 6 (milk).
While path length was significantly reduced in segment 4, it was significantly
prolonged in segment 6. It has to be considered that the validity of comparisons is
still suffering from data losses due to missing sub-actions in their action-patterns
in the CVA group (i.e. missing stirring of the tea or not removing the teabag, see
Fig. 7) and the difficulty of isolating segment 2 (‘switch the kettle on’) from
segment 1 (‘pour water in the kettle’) in both groups.

Fig. 7 Comparison of executed sub-segments for the whole tea-making task. T-test revealed
a significant difference with a p-value of .005 and an effect size of .28.
400 P. Gulde et al.

Figure 7 displays the average number of executed sub-segments for the whole
tea-making task. CVA patients showed omissions and repetitions, but also the
control group showed deviations from the number from the optimal number of 8
sub-segments, sometimes adding or omitting one sub-segment. In both groups
mainly omissions of removing the teabag or stirring the tea occurred. However, in
total controls performed less mistakes. The difference between the groups in the
number of sub-segments executed in the tea-making task is significant with a p-
value of .005, but of small effect (effect size of .28). A possible factor in
committing mistakes in the preparation of tea with milk and sugar could be lack of
familiarity of this type of tea in Germany. Nonetheless, clear instructions were
given by the investigator and the experimental setting offered well-defined
affordances.

5 Future Directions and Technological Challenges

Data collection for the paradigm is still in progress. The goal is to extend the
number of subjects with CVA to 20. Current development is focused on resolving
problems like synchronisation of the data streams (from coasters, motion capture
and eye tracking – see Fig.2). It is expected that findings will provide valuable
input into the further development of the CogWatch system. Kinematic data may
be used to indicate skill and security of task execution. Gaze fixations data may
emerge as an early indicator of upcoming apraxic errors that can be used in future
versions of the system to prevent errors before they occure.

Acknowledgment. This work was funded by the EU STREP Project CogWatch (FP7-ICT-
288912). Authors would like to thank the patients of the Clinic for Neuropsychology at the
Hospital München-Bogenhausen for participation in the research, the head of department
Georg Goldenberg for his support and the department’s staff as well as the student
assistants for their help.

References
[1] Goldenberg, G., Hermsdörfer, J., Spatt, J.: Ideomotor apraxia and cerebral dominance
for motor control. Cognitive Brain Research 3, 95–100 (1996)
[2] Bickerton, W., Riddoch, J., Samson, D., Balani, A., Mistry, B., Humphreys, G.:
Systematic assessment of apraxia and functional predictions from the Birmingham
Cognitive Screen. Journal of Neurology, Neurosurgery & Psychiatry with Practical
Neurology 83(5), 512–552 (2012)
[3] Land, M., Hayhoe, M.: In what ways do eye movements contribute to everyday
activities? Vision Research 41, 3559–3565 (2001)
[4] Hughes, C., Parekh, M., Hermsdörfer, J.: Segmenting instrumented activities of daily
living (IADL) using kinematic and sensor technology for the assessment of limb
apraxia. Communications in Computer and Information Science 374, 158–162 (2013)
Analysis of Eye Movements, Kinematics and Dynamic Aspects of Performance 401

[5] Forde, E.M.E., Rusted, J., Mennie, N., Land, M., Humphreys, G.W.: The eyes have it:
An exploration of eye movements in action disorganization syndrome.
Neuropsychologia 48(2010), 1895–1900 (2010)
[6] Hughes, C.M.L., Baber, C., Bienkiewicz, M., Hermsdörfer, J.: Application of Human
Error Identification (HEI) Techniques to Cognitive Rehabilitation in Stroke Patients
with Limb Apraxia. In: Stephanidis, C., Antona, M. (eds.) UAHCI/HCII 2013, Part III.
LNCS, vol. 8011, pp. 463–471. Springer, Heidelberg (2013)
[7] Hermsdörfer, J., Li, Y., Randerath, J., Roby-Brami, A., Goldenberg, G.: Tool use
kinematics across different modes of execution. Implications for action representation
and apraxia. Cortex 49, 184–199 (2013)
Historical Background from 1986 – 2005
for the Development of the ActiGait System

Jens Peter Haase, Morten Haugland, and Thomas Sinkjær

Introduction: Stroke is one of the most common forms of acquired brain injuries
that lead hemiplegia/morbidity needing neurorehabilitation.

History: The so-called “dropfoot” i.e. a paretic elevation (dorsiflexion) of the foot
leads to reduction of walking speed and stability, and the patient becomes less
socially independent. In the 80´ties and 90’ties prof. Thomas Sinkjaer and Dr.
Morten Haugland at Aalborg University, Denmark, developed an implantable
dorsiflexion device, as part of the SensoGait system. Sensory impulses detected
from a nerve through a cuff-electrode were transformed into motor stimulation of
the peroneal nerve above the knee. This idea was later changed into the ActiGait
system where a heel switch placed in a sock replaced the sensory feedback. The first
prototype of the ActiGait system was implanted in 3 patients in 1999 at Aalborg
University Hospital. In collaboration between Aalborg University, three major
hospitals in Denmark and the spin-off company Neurodan (established in late 1994)
further 15 hemiplegic patients in Denmark had an ActiGait system implanted by JH
in 2003-2004. 13 of these implants were successful. Based on the preliminary
experiences ActiGait has undergone design revisions through a close follow-up
system that will be demonstrated, along with examples of complications and means
of mitigation that were included in the system, in the documentation and in training
material.

Conclusion: The ActiGait system is an adjuvant to treatment of patients with


hemiplegia and moderate spasticity resulting from brain/spine injury. Before
implantation a period of training with external stimulators is advocated.
Since 2005 the company Otto Bock bought Neurodan and till today close to 300
patients have been implanted throughout Europe.

Acknowledgement. The company Neurodan was established by two of the authors


(MH, TS). None of the authors have any commercial interest in the Actigait system.
The third author (JH) has today a commercial interest as a consultant with
nstim/Otto Bock.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 403
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_61, © Springer International Publishing Switzerland 2014
404 J.P. Haase, M. Haugland, and T. Sinkjær

References
Sinkjaer, T., Haugland, M.K., Haase, J.: Natural neural sensing and artificial muscle control
in man. Exp. Brain Res. 98, 45–542 (1994)
Larsen, J.O., Thomsen, M., Haugland, M.K., Sinkjær, T.: Degeneration and regeneration in
rabbit peripheral nerve with long-term nerve cuff electrode implant: A stereological study
of myelineated and unmyelinated axons. Acta Neuropathologica 96, 365–378 (1998)
Sinkjær, T.: Integrating sensory nerve signals into neural prosthesis devices.
Neuromodulation 3(1), 35–41 (2000)
Sinkjær, T., Haugland, M.K., Haase, J.: Improved control of activated muscles using FES.
Pan Arab Journal of Neurosurgery 5(2), 8–21 (2001)
Haugland, M.: Natural Sensory feedback for closed-loop control of paralyzed muscles, PhD,
Dept. Medical Informatics and Image Analysis, HST, Aalborg University, Denmark
(February 2004)
Burridge, J.H., Haugland, M., Larsen, B., Pickering, R.M., Svaneborg, N., Iversen, H.K.,
Brøgger Christensen, P., Haase, J., Brennum, J., Sinkjaer, T.: A phase II trial to evaluate
the ActiGait implanted drop-foot stimulator in established hemiplegia. J. Rehabil.
Med. 39, 18–212 (2007)
Haase, J., Patriciu, A., Larsen, B., Emborg, J.: Historic review – ActiGait: A new FES
(Functional Electrical Stimulation) improves gait among patients with apoplectic
hemiplegia. Abstract from Anniversary Congress of the International Neuroscience
Institute, INI, Hannover, Germany (2010)
Impact of Problem Solving Therapy on Brain
Networks Associated with Depressive Symptoms
in Poststroke Older Adults

Niloufar Niakosari Hadidi1, Leah Jappe2, Kathryn Cullen3, and Kay Savik1
1
University of Minnesota, School of Nursing
hadi0001@umn.edu
2
Clinical Psychology Clinical Psychology, University of Minnesota
3
University of Minnesota, Department of Psychiatry

Abstract. Problem-solving therapy (PST) shows promise as an evidence- based


approach to treat depression of stroke survivors. The purpose of this study was to
determine the impact of PST on brain networks associated with depressive
symptoms in older stroke survivors. This study employed the use of a functional
magnetic resonance imaging (fMRI) task, in which participants matched either
emotion faces or neutral shape, which has been previously used in the study of
depression. [1,2] This pilot study was designed as a two-arm randomized trial
(intervention vs. attention-control group), where the treatment group received six
weekly PST sessions each sessions (1-1.5 hrs each), and the attention-control
group received six weekly stroke education sessions (1 hr each). Both groups
underwent fMRI procedures before and after assigned interventions. Results of the
Hariri task indicated that bilateral amygdala activity decreased among those
receiving stroke education but increased in those receiving PST at post-treatment.
Increased amygdala activation correlated with a drop in depression scores. This
may explain mechanism of action of PST on amygdala by rejuvenating a blunted
system of emotional reactivity.

1 Introduction

Stroke is the fourth leading cause of death and greatest cause of disability world
wide. [3] With advancements in stroke treatments coupled with the overall aging
of the U.S. population, there are increasing numbers of stroke survivors living
with the effects of stroke. These trends have led to more stroke survivors being
discharged to home settings who are in need of rehabilitation and interventions to
cope with the physical and emotional impact of stroke at home.
Depression is a common consequence of stroke that causes increased morbidity
and mortality.[4] Poststroke depressive symptoms affect 33% of stroke survivors5
contributing to morbidity and mortality, lower functional status and increased
cognitive impairment. [6-8] Poststroke depressive symptoms is defined as any
depressive symptoms after occurrence of stroke with a cutoff point of 5 on Center

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 405
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_62, © Springer International Publishing Switzerland 2014
406 N.N. Hadidi et al.

on Epidemiologic Studies Depression (CES-D) 10 item scale[9]. While some


patients may be diagnosed with depression, many more have depressive symptoms
and often express feelings of sadness and lack of motivation to participate in
rehabilitation.
Studies demonstrate a strong relationship between depression and poorer
health, especially as it relates to older adults. Depression reduces energy level,
concentration, self-efficacy and motivation. Annually, 75% of stroke victims are
over the age of 65.[10] Older stroke survivors who are depressed see their primary
health care provider more frequently and have higher rates of emergency room
visits and longer hospital stays. [11] Depression further impacts these individuals’
ability to fully participate in rehabilitation. Studies suggest that PSD is correlated
with decline in function, and that it negatively impacts quality of life. [12] Thus,
reduced quality of life after stroke appears to be related to both physical disability
and depressive symptoms.
Treating PSD is important not only to reduce excess morbidity and mortality in
patients, but also to potentially alleviate caregivers’ emotional distress and caregiving
burden. Depressed stroke survivors who refuse to participate in rehabilitation become
isolated and dependent on caregivers for accomplishing activities of daily living,
placing additional burden on caregivers.

2 Problem-Solving Therapy

PST is a program of intervention that has been shown to reduce depressive


symptoms in non-stroke populations; [13] however, its impact on neural network
of stroke survivors is unknown.PST is based on D’Zurilla’s (1986) model of social
problem-solving. The premise of this theory is that depression can occur because
of the interaction of four major stress related variables: major negative life events,
daily problems, negative emotional states, problem-solving coping. PST enhances
problem solving effectiveness by reducing emotional distress, reducing ineffective
behavior and improving quality of life.
Stroke survivors are often faced with a multitude of problems which could lead
to frustration when remained unresolved and accumulated. Those problems can
vary from basic accomplishing activities of daily living (i.e., dressing, grooming,
etc) to more complex tasks of instrumental activities of daily living (i.e., financial
responsibilities, social networking). Often stroke survivors view the latter
problems as complex and difficult to resolve. PST emphasizes breaking down the
complex problems into simpler and thus more manageable problems.
There is evidence that the use of PST reduces anxiety and depression of family
caregivers of individuals with chronic illness such as depression, dementia, cancer
and spinal cord injuries [14,15]. Emerging research has suggested that PST may
be a useful treatment of depression in stroke patients16, but the neural mechanisms
of this treatment are unknown. Two key brain regions that have been implicated in
depression include the amygdala and the dorsolateral prefrontal cortex (DLPFC).
The impact of PST on amygdala was the focus of the present application.
Impact of Problem Solving Therapy on Brain Networks 407

3 Method
A 2-group randomized controlled design was used to investigate the potential
impact of PST on brain networks associated with depressive symptoms in older
adults post stroke. Ten stroke survivors with ischemic stroke (where stroke was
required to have occurred within 3 months to 2 years) were recruited and
randomized via simple randomization to either the treatment group receiving 6
weekly PST sessions from the principal investigator (PI) or control group
receiving 6 weekly stroke education sessions administered by a doctoral student
following a stroke education booklet developed specifically for this study. To
account for fMRI variability with time, all patients underwent fMRI according to
standardized protocol at baseline, and at 6 weeks following therapy termination.
fMRI activity reported for this paper included a task in which the participants
were asked to match either emotion faces or neutral shapes. A whole-brain
analysis was carried out to regress the model of the task against the BOLD signal
in each voxel. We extracted the average z-scores from the emotion-minus-shape
contrast for two regions of interest: bilateral amygdala.

4 Results
There were no differences between the 2 groups in demographics. Median
baseline depressive symptoms in the treatment group was 4(0-10) and reduced to a
median of 0(0-9) after treatment. For the control group, median baseline
depressive symptoms was 2 (1-4) and increased after education to a median of
3(0-5). In the treatment group, amygdala activation both right and left were
increased (left amygdala (t=3.4, p=0.044, right amygdala, t=2.5, p=0.088). In the
whole sample, an increase in amygdala activation was correlated with a drop in
depression scores. There was no significant change in amygdala activation within
the control group. This may suggest that PST enhances and rejuvenates areas in
the brain related to emotional processing.
There was a significant group x time interaction for the Hariri task in the L-
Amg (F(1,8)=9.82, p=0.014) where BOLD % signal change increased
significantly more for the treatment than for the control group (i.e. there was
greater change in the patients undergoing active therapy). BOLD % signal change
for each condition is listed below.
Control Active Treatment
Pre-Treatment -.023 -.399
Post-Treatment -.125 .176
408 N.N. Hadidi et al.

It should be noted that treatment and control group did not receive the same
length of intervention. While treatment group had on average 1.5hrs of PST, the
control group had on average an hour of stroke education. This may have affected
the results. Further, this was a small study and the result should be interpreted with
cautious.

Fig. 2 Differences Between Groups in Amygdala Activation Hariri Task

5 Conclusion

This pilot study is the first in stroke research to provide preliminary analysis on
how PST impacts functional brain activity in stroke survivors. Our findings
indicate that the study of neuron connectivity utilizing fMRI in stroke population
is feasible. Further, depressive symptoms decreased in the treatment group as
compared to control group which was supported by our previous pilot study.[17]
There needs to be larger scale studies on the impact of PST on older stroke
survivors’ depressive symptoms and impact on amygdala activity in the brain
utilizing fMRI.

Acknowledgment. We would like to acknowledge and thank Drs. Scott Crowe, Farah
Ikramuddin, and James Agre for their collaboration.
This study was supported by the National Center for Advancing Translational Sciences
of the National Institutes of Health Award and Center on Aging, University of Minnesota.
The content is solely the responsibility of the authors and does not necessarily represent the
official views of the National Institutes of Health.

References
[1] Cullen, K.R., Gee, D.G., Klimes-Dougan, B., et al.: A preliminary study of functional
connectivity in comorbid adolescent depression. Neurosci. Lett. 460, 227–231 (2009)
[2] Greicius, M.D., Flores, B.H., Menon, V., et al.: Resting-state functional connectivity
in major depression: Abnormally increased contributions from subgenual cingulate
cortex and thalamus. Biol. Psychiatry. 62, 429–437 (2007)
Impact of Problem Solving Therapy on Brain Networks 409

[3] American Stroke Association. About stroke: Impact of stroke (Stroke statistics),
http://www.strokeassociation.org/STROKEORG/AboutStroke/
Impact-of-Stroke-Stroke-statistics_UCM_310728_Article.jsp
(retrieved from, 2014)
[4] Depression and Stroke: Cause or Consequence. Semin. Neurol. 25, 396–409 (2005)
[5] Hackett, M.L., et al.: Frequency of depression after stroke a systematic review of
observational studies. Stroke 36(6), 1330–1340 (2005)
[6] Carod-Artal, J., Egido, J.A., Gonzalez, J.L., Varela de Seijas, E.: Quality of life
among stroke survivors evaluated 1 year after stroke: Experience of a stroke unit.
Stroke 31, 2995–3000 (2000)
[7] Carod-Artal, F.J., Trizotto, D.S., Coral, L.F., Moreira, C.: Determinants of quality of
life in Brazilian stroke survivors. J. Neurol. Sci. 284, 63–68 (2009)
[8] Williams, L.S., Ghose, S.S., Swindle, R.: Depression and other mental health
diagnoses increase mortality risk after ischemic stroke. Am. J. Psychiatry. 161, 1090–
1095 (2004)
[9] Steffens, D.C., et al.: Cerebrovascular disease and evolution of depressive symptoms
in the cardiovascular health study. Stroke 33(6), 1636–1644 (2002)
[10] Rahimi, A.R., Wrights, B., Akhondi, H., Richard, C.: Clinical correlation between
effective anticoagulants and risk of stroke: Are we using evidence-based strategies?
South. Med. J. 97, 924–931 (2004)
[11] U. S Department of Health and Human Services. Mental Health: A Report of the
Surgeon General-Executive Summary. Rockville, MD: US Department of Health and
Human Services, Substance Abuse and Mental Health Services Administration,
Center for Mental Health Services, National Institute of Health, National Institute of
Mental Health (1999)
[12] Cassidy, E., O’Connor, R., O’Keane, V.: Prevalence of post-stroke depression in an
Irish sample and its relationship with disability and outcome following inpatient
rehabilitation. Disability & Rehabilitation 26, 71–77 (2004)
[13] Mynors-Wallis, L.M., Gath, D.H., Day, A., Baker, F.: Randomised controlled trial of
problem solving treatment, antidepressant medication, and combined treatment for
major depression in primary care. BMJ 320, 26–30 (2000)
[14] Nezu, C.M., Nezu, A.M., Friedman, S.H., Houts, P.S., DelliCarpini, L.A., Nemeth,
C.B., Faddis, S.: Cancer and psychological distress: Two investigations regarding the
role of problem solving. Journal of Psychosocial Oncology 16, 27–40 (1999)
[15] Kennedy, P., et al.: Coping effectiveness training reduces depression and anxiety
following traumatic spinal cord injuries. British Journal of Clinical Psychology 42(1),
41–52 (2003)
[16] Robinson, R.G., et al.: Escitalopram and problem-solving therapy for prevention of
poststroke depression: A randomized controlled trial. JAMA 299(20), 2391–2400
(2008)
[17] Hadidi, N., Lindquist, R., Buckwalter, K., Savik, K.: Feasibility of a Pilot Study of
Problem-Solving Therapy For Stroke Survivors. Rehabilitation Nursing, 1–11 (2014)
Improved Detection and Force Decoding
through Combined Near-Infrared Spectroscopy
and Electroencephalographic Measurements

Mia H. Hansen, Eric Kassebaum, Marlena A. Plocharska,


Mads Jochumsen, and Ernest N. Kamavuako

Department of Health Science and Technology at Aalborg University,


9220 Aalborg Ø, Denmark
{mhha10,ekasse13,mkonow09}@student.aau.dk,
{mj,enk}@hst.aau.dk

Abstract. Stroke is the leading cause of acquired disability worldwide. Therefore,


several techniques have been suggested for the rehabilitation such as brain-
computer interface technology combined with assistive technology. To control the
assistive technology, the brain activity should be decoded to determine when the
patient intends to initiate a movement, moreover, the kinetic information should
be decoded. In this study, electroencephalography (EEG) was recorded
simultaneously with near-infrared spectroscopy (NIRS) to determine whether the
detection of foot movements and force decoding could be improved using a hybrid
approach (combination of EEG and NIRS). Fourteen healthy subjects performed
foot movements associated with two levels of force (20 % and 60 % maximum
voluntary contraction, MVC) from which subject independent features were
extracted and classified using linear discriminant analysis. The detection accuracy
was 76 ± 10 % and force decoding was 81 ± 15 % when using the hybrid
approach. The performance was on average improved with more than 10
percentage points. It was found that EEG and NIRS were almost as good as the
hybrid approach for movement detection and force decoding, respectively. This
study showed that BCI performance may be improved with simultaneous
recordings of EEG and NIRS.

1 Introduction

Stroke is a cerebrovascular incident causing neurological deficits by an abrupt


perfusion disturbance in the cerebral circulation [1]. Stroke is accounted for
approximately 10 % of deaths worldwide. Two thirds of strokes are not lethal, but
leave the survivors with disabilities [2] among which motor impairment (80 %) is
the most common. This injury is often persistent (35 %) [3-5]. Stroke
rehabilitation may help restoring motor function by restructuring the neuron
pathways around the damaged tissue and increase the capacity of the remaining
pathway [5, 6]. These changes may be enhanced using different types of

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 411
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_63, © Springer International Publishing Switzerland 2014
412 M.H. Hansen et al.

rehabilitation techniques. Over the past years, brain-computer interface (BCI)


technology has been proposed as a tool to induce plasticity and enhance the
recovery of motor impaired patients by allowing them to control external devices
using their brain activity [7, 8]. Such devices include virtual reality systems,
electrical stimulators and robotics [9]. An example of a neuromodulatory BCI is
electrical stimulation triggered by imagined movements in this way Hebbian-
associated plasticity may be induced [8]. Different recording modalities have
been used to assess the brain activity which is then translated into device
commands. Control signals extracted from electroencephalography (EEG) have
been widely used to control external devices in the rehabilitation. Examples of
some of the most common signals are sensorimotor rhythms and event-related
potentials [10]. The EEG can register the electrical changes in the brain and is one
of the most studied signal modalities in BCI research due to its high temporal
resolution and non-invasiveness. Brain activity may also be recorded using other
non-invasive techniques such as functional magnetic resonance imaging and near-
infrared spectroscopy (NIRS) where the hemodynamic response can be used as a
control signal [11-13]. One advantage of NIRS is that the technique is relatively
resistant to head movements and electrical artifacts arising from e.g. eye
movements, however, it suffers from a relatively slow response. The slow
response time will limit the information transfer rate in BCIs for e.g.
communication purposes or the applicability for neuromodulation where
somatosensory feedback must reach cortex shortly after the activation of the motor
cortical areas [8].
The different recording techniques have advantages and disadvantages. An
approach to utilize this difference is by combining them; this is known as a hybrid
BCI [14]. This approach may improve the performance of the BCI as both inputs
can provide complementary information and enhance the performance for users
that can not control e.g sensorimotor rhythms [15]. The two inputs may be
processed simultaneously, but they can also be operated sequentially where the
first signal can be used as an on/off switch while the other input can serve as a
selector to give more degrees of freedom [14]. An example of a sequntial
approach could be to use the movement-related cortical potential (extracted
through EEG) to detect movement intentions [16] and then use NIRS to provide
information about the movement direction [17]; this could be used for prosthetic
control. To improve such an approach further, the decoding of kinetics, such as the
level of force, may be utilized for more natural and sophisticated control of the
assistive devices [18]. To operate these successfully, the decoding of movements
and the kinetics should be maximized.
The aim of this study was to investigate the effect of combining EEG and NIRS
recordings for movement detection and force decoding. The combination of EEG
and NIRS was compared to each of the techniques separately.
Improved Detection and Force Decoding 413

2 Methodology

2.1 Subjects
In this study, 14 healthy volunteers were included: six females and eight males (25
± 1.6 years). All volunteers signed a consent form (N-20130081). They were all
naïve to the task.

2.2 Experimental Protocol


The subjects were seated in an armchair facing a computer screen at a distance of
1.5 meters. During the experiment their right foot was fixed in a custom made
pedal where a force transducer was attached. At the beginning of the experiment,
the maximum voluntary contraction (MVC) was determined when the subjects
performed an isometric dorsiflexion of the ankle joint. The MVC was recorded
three times with a 1-minute break in between each repetition. The highest value
was used as a reference later in the experiment. The subjects were asked to
perform two tasks: i) isometric dorsiflexions at 20 % MVC and ii) isometric
dorsiflexions at 60 % MVC. The tasks were performed in blocks. For each task,
the subjects prepared for three seconds before performing five movements that
should reach the desired level of MVC within a ten-second time frame. This was
repeated 15 times for each task. To make sure that the NIRS measurements had
recovered to the baseline, each repetition was separated by a rest period of 50
seconds. The subjects were cued by a custom made program (Knud Larsen, SMI,
Aalborg University) and provided with visual feedback on their performance
throughout the experiment.

2.3 Recordings
During the experiment EEG and NIRS were recorded simultaneously. The
recordings were performed in an electrically shielded room.
EEG: Monopolar EEG was continuously recorded (Nuamps Express/Scan 4.5,
Neuroscan, USA) using self-adhesive skin electrodes (Neuroline 720, Ambu,
USA) with a sampling rate of 500 Hz. The electrodes were placed at: FT7, FC3,
FC4, FT8, TP7, CP3, CP4 and TP8 according to the International 10-20-system.
The electrodes were referenced to the right mastoid process and grounded at
nasion. During the experiment the impedance was kept below 5 kΩ.

NIRS: NIRS (OXYMON MK III/OxySoft DAQ 2.1.6, Artinis, Netherlands) was


measured using a four-channel cross-setup in a custom built mount and sampled at
10 Hz. The receiver optode Rx was placed at Cz according to the International 10-
20-system for EEG. The four transmitter optodes Tx1, Tx2, Tx3 and Tx4 were
placed at FCz, C4, CPz and C3, respectively. The distance between transmitter
and receiver optode was set to 3.1 cm.
414 M.H. Hansen et al.

2.4 Data Processing and Feature Extraction


Two scenarios were analyzed: 1) discrimination between “movement” and “rest”
and 2) discrimination between movements performed with 20 % MVC and 60 %
MVC.
EEG: Initially, the continuous EEG signals were bandpass filtered from 0.05 to 5
Hz using a 3rd order digital Butterworth filter, and the mean value across the
channels was calculated. The continuous data was divided into epochs (15 in total
for both types): “movement” and “rest” (where no movement was performed). The
length of the two types of epochs was 15 seconds. The “movement” epochs
contained data from the three seconds of preparation until two seconds after the
last of the five movements. The “rest” epochs were extracted from the rest period
between the repetitions of the tasks.
To discriminate between “movement” and “rest” epochs, two features were
extracted for each epoch: i) mean amplitude and ii) maximum peak-to-peak
amplitude.
To discriminate between the two force levels (see Fig. 1), five features were
extracted: i) average power from 0-3 Hz using Welch’s power spectral density
estimate (Hamming window with 50% overlap of the segments), ii) mean
amplitude in the interval from 1-6 seconds, iii) mean amplitude from 10-15
seconds, iv) slope of linear regression in the interval from 0-3 seconds and v)
slope of linear regression in the interval from 2-5 seconds.

NIRS: The continuous data was divided into epochs in the same way as described
in the previous section. Only the deoxygenated (HHb) signal was used in the
analysis.
To discriminate between “movement” and “rest” epochs, two features were
extracted: i) maximum peak-to-peak amplitude and ii) temporal onset of the
maximum peak.
To discriminate between the two force levels, two features were extracted for
each epoch: i) maximum peak-to-peak amplitude and ii) mean amplitude.

2.5 Classification
To discriminate between the two scenarios outlined in the previous section, linear
discriminant analysis (LDA) was used to classify the features. Leave-one-out
cross-validation was used where the classifier was trained on 14 samples and
tested on the remaining one for each subject. The classification accuracy was
obtained for each scenario and signal type (EEG, NIRS or combined EEG-NIRS
(hybrid approach)).
Improved Detection and Force Decoding 415

Fig. 1 Grand average (across 14 subjects) of the extracted epochs. Two EEG traces (top)
and two NIRS traces (bottom) are shown for the mean value of the channels: movements
performed at 60 % MVC (solid line) movements performed at 20 % MVC (dashed line).

2.6 Statistics
The difference in classification accuracy between the different signal modalities
was tested using a 1-way repeated measures analysis of variance (ANOVA) with
the factor ‘signal modality’ with three levels: EEG, NIRS and hybrid. Statistical
significance was assumed when P<0.05. A statistical significant test was analyzed
with a post hoc analysis where Bonferroni correction was applied for multiple
comparisons.

3 Results

The detection accuracy and force decoding are presented in Table 1 (classification
accuracies from LDA). The values are presented as mean ± standard deviation
across the 14 subjects using the different signal recording modalities. For
movement detection and force decoding, the hybrid approach showed the highest
classification accuracy with 76±10 % and 81±15 %, respectively. It was found that
EEG had higher classification accuracy (74±13 %) for movement detection
compared to NIRS (65±10 %). The opposite was found for force decoding where
NIRS performed better (80±17 %) compared to EEG (61±11 %). Using the 1-way
416 M.H. Hansen et al.

repeated measures ANOVA a significant effect was observed for scenario 1


(F(1,27)=12.99; P=0.001) and scenario 2 (F(1,13)=16.51; P=0.001).
The test statistics of the post-hoc analysis revealed that the classification
accuracies in scenario 1 for EEG (P=0.026) and EEG-NIRS (P=0.000054)
recordings were significantly higher when compared to the NIRS recording. No
significant difference was observed between the EEG and hybrid recordings
(P=0.21). In scenario 2, the classification accuracies were significantly higher for
NIRS (P=0.008) and hybrid (P=0.001) recordings compared to the EEG recording.
No significant difference was observed between the NIRS and hybrid recordings
(P=1).

Table 1 Classification accuracies

Movement detection and force classification

EEG NIRS Hybrid


Scenario
[%] [%] [%]

1) Movement vs. rest 74±13 65±10 76±10

2) 20 % MVC vs. 60 %
61±11 80±17 81±15
MVC

Mean±SD Mean±SD Mean±SD

Classification accuracy (mean ± standard deviation) computed using LDA for movement detection
(scenario 1) and force discrimination (scenario 2).

4 Discussion

Hybrid recordings were used for the detection of movements and decoding of the
force level of repetitive foot dorsiflexions. The results obtained for the combined
recordings were compared to that of EEG and NIRS separately. By combining
EEG and NIRS measurements, the performance increased for both classification
scenarios: up to 76 ± 10 % for detection and up to 81 ± 15 % for force decoding.
The results revealed that NIRS was more suitable for discrimination of the two
force levels than EEG; EEG was more effective to detect movements. The highest
performance in both scenarios was obtained using the hybrid approach. However,
the hybrid performance was almost the same as the EEG for movement detection
and NIRS for movement classification.

4.1 Movement Detection and Force Decoding


The decoding of movements was lower compared to what have previously been
reported using EEG [19] and NIRS [20] where detection performance of more
than 80 % in the true positive rate was reported for healthy subjects. In the current
study, it was found that EEG was better for movement detection compared to
Improved Detection and Force Decoding 417

NIRS, and the hybrid approach performed slightly better than using EEG alone.
However, the lower performance compared to the findings in Jochumsen et al.
[19] may be explained by their application of a spatial filter with Cz as the center
electrode. Cz is the site overlying the motor cortical representation of the lower
limbs. EEG was not recorded from Cz in the current study since that area was
covered with the NIRS receiver optode. Since EEG was not recorded from Cz, and
the other sensors were positioned on each site of the vertex, the mean value of the
channels was used. However, with this approach the spatial information is reduced
compared to spatially filtered data around Cz. The results suggest that EEG is
more suitable for movement detection compared to NIRS which was recorded
closer to the vertex than the EEG.
Force, on the other hand, was better discriminated using NIRS compared to
EEG. It may be a bit misleading due to the electrode positioning, but it may also
be due to the penetration depth of the NIRS (up to 2 cm) and the physiological
encoding of force. The force discrimination is in the range of what has been
reported previously, but in this study a longer data segment and lower number of
movements were used for classification compared to other studies that decode the
kinetics of movements using a couple of seconds data before the movement onset
to determine the level of force [18, 19]. From the results, it seems that there might
not be a need for EEG-based features since the classification accuracies for force
decoding are almost identical when using NIRS compared to the hybrid approach.
Based on the performance of the EEG and NIRS separately, it is suggested that
the hybrid approach may be useful for applications where movements must be
detected and the force level decoded. Despite the low number of trials recorded,
the performance of the hybrid BCI is above the chance level which is affected by
the number of trials included in the analysis [22].
The performance of the hybrid approach may be improved by investigating
different types of features such as time-frequency/scale based features. Also, the
spatial information can be included in the analysis by performing the feature
extraction for each channel. This will lead to a larger feature vector, but the
dimensionality will still be rather low (<50).

4.2 Limitations
The subjects in this study were healthy volunteers with no prior history of
neurological disease, and the intended user group for BCIs in general has motor
deficits of varying degrees from locked-in patients to stroke survivors with
paresis. Patients should be included in future studies. The aim of this study was to
investigate if using a hybrid approach could optimize the performance compared
to using only a single recording modality. Since the EEG and NIRS were recorded
simultaneously a control should have been performed where the EEG and NIRS
were recorded from the same electrode positions to obtain the most accurate
estimate of the efficacy of the hybrid approach.
418 M.H. Hansen et al.

It has been shown that EEG can be used in BCIs for inducing plasticity where
sensory feedback must be provided with limited latency (in the range of a couple
100 milliseconds). NIRS, however, has a slower response time than EEG, so it
should be tested how the performance is affected when reducing the amount of
data (15 seconds in the current study) for feature extraction to obtain a faster
response. As outlined, the response time is too long to combine it with
somatosensory feedback from e.g. electrical stimulation to induce Hebbain-
associated plasticity, but with a reduction in response time it may be used as a tool
for neurofeedback [23].

5 Conclusion

This study showed that by combining NIRS and EEG, movement detection and
force decoding were improved compared to using each technology separately.
However, the performance of EEG for movement detection and NIRS for force
decoding was almost the same as for the combined approach. The simultaneous
recording of EEG and NIRS may improve brain-controlled assistive devices.

Acknowledgment. This work was supported by the Danish Technical Research Council.

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induces cortical plasticity. J. Physiol (Lond. ) 590, 1669–1682 (2012)
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[10] Wolpaw, J.R., Birbaumer, N., McFarland, D.J., Pfurtscheller, G., Vaughan, T.M.:
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Scherer, R., Zander, T.O., Müller-Putz, G., Neuper, C., Birbaumer, N.: The hybrid
BCI. Frontiers in Neuroscience 4, 3 (2010)
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Modeling the Functional Dependence of Stroke
Patients: The Outcome of an Improved Gait
Training

Kristian Hennings1,2, Sabata Gervasio1,2, Ole Kæseler Andersen2,


and Erika Geraldina Spaich2
1
Nordic NeuroSTIM ApS, Havneparken 2, 7100 Vejle, Denmark
{krhe,saba}@hst.aau.dk
2
Aalborg University, Aalborg, Denmark
{oka,espaich}@hst.aau.dk

Abstract. The present study developed a model that can predict the outcomes of a
gait rehabilitation method seen from a societal perspective. The model consisted
of a Markov model for the long-term functional dependency of the stroke patients
and a decision tree model for the consequences of a stroke. In this study, it was
applied for predicting the outcome of introducing reflex-based electrical gait
therapy. The model was validated using data for 1 month, 3 months, 1 year, 5
years and 10 years fatality of stroke patients, as well as data for the functional
independence of stroke patients. The model predicted that after the first stroke
with reflex-based electrical gait therapy, 51.7% of the patients treated will be
depending on care and 72.5% will live in their home, as compared with 60.1% and
63.0% for the control group, respectively. After five years, 26.8% of the patients
will be depending on care and 34.8% will live in their home following reflex-
based gait therapy, as compared with 30.6% and 29.4% for the control group,
respectively. Consequently, the study supports the assumption that better gait
rehabilitation lead to more functionally independent patients, and hence may lead
to lower costs for the society.

1 Introduction

Stroke is a major burden for society that affects approximately 1.3 million people
in Europe each year [1] and is in the top three causes of death [2] and acquired
adult disability [3]. The consequences for stroke survivors are significant in terms
of a decreased quality of life and dependence on support from caregivers.
One of the most common disabilities after a stroke is impaired gait that affects
two out of three patients [4]. Consequently, gait training has a major role in the
rehabilitation of stroke patients. Despite this, approximately half of stroke patients
still have some degree of walking disability even after completing their
rehabilitation programs [4]. This has led to the introduction of novel methods,
such as robot assisted gait training [5] and reflex-based electrical gait therapy [6],

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 421
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_64, © Springer International Publishing Switzerland 2014
422 K. Hennings et al.

which hold the promise of improving the quality and the walking speed of the
patients. However, while an improvement in an outcome measure, such as walking
speed, may be demonstrated, it is difficult to evaluate what this implies from a
societal perspective in terms of consequences for patients, health care system and
society.
The present study aimed to provide a model that can predict the consequences
and benefits associated with new gait training methods. The model was designed
so that a widely used outcome parameter, preferred walking speed, was used as a
predictor of functional independence [7], [8]. This allowed the model to predict
the functional dependency of stroke patients in 10 years from their initial stroke.
To demonstrate the usefulness of the model, this was used to predict the outcome
of introducing reflex-based electrical gait therapy for the population of stroke
patients in Denmark.

2 Methods and Materials

The model consisted of two sub-models: a short-term model that predicted the
consequences of initial and recurrent strokes, and a long-term model that predicted
the functional dependency of the stroke patients after they had their initial stroke.
The models assigned the patients to one out of four possible states: 1) Home
Independent (HI), 2), Home Dependent (HD), 3), Specialized Nursing Facility
(SNF), or 4) Dead. The short-term model was used to estimate the starting state
for the long-term model and to calculate the transition probabilities for the HI,

Home Independent
35.0%

No Gait Impairment
Home Dependent
33.3% 35.9%

Specialized Nursing Facility


29.1%

WS > 0.6m/s
Home Independent
C: 27.6% / T: 42.4%

Stroke Non-Fatal Gait Impairment 0.2m/s < WS < 0.6m/s


Home Dependent
86.0% 66.7% C: 46.8% / T: 48.7%

WS < 0.2m/s
Specialized Nursing Facility
C: 25.6% / T: 8.9%

Fatal
Dead
14.0%

Fig. 1 Decision tree model of initial and recurrent strokes (WS: walking speed, C: control,
T: treatment/reflex-based electrical therapy)
Modeling the Functional Dependence of Stroke Patients 423

HD, SNF states. When the short-term model was used to determine the transition
probabilities, the resulting probabilities were multiplied with the probability of
having a recurrent stroke for each of the HI, HD, SNF states.

2.1 Short-Term Model


A decision tree model was used to predict the consequences of a stroke (see Figure
1). The overall recurrent stroke probability (6.3%) was calculated as a mean of
experimental data [9]–[14]. Recurrent stroke probability for the HI, HD, SNF
states were set based on hazard ratios of 0.59, 1.00, and 1,85 by multiplying them
with the overall recurrent stroke probability, respectively [15]. This resulted in
recurrent stroke probabilities of HI state: 3.7%, HD state: 6.3% and SNF state:
11.7%, which lead to different recurrent stroke mortality rates of HI state: 0.52%,
HD state: 0.88% and SNF state: 1.63%.
A stroke was assumed either to result in gait impairment or not. If it did not
result in a gait impairment, probabilities of a patient entering the HI, HD, or SNF
state were extracted from results reported by Olai et al., 2009 [16].
When the stroke resulted in gait impairment, walking speed was used to
estimate these probabilities. This estimation was based on the following limits: HI
state, walking speed higher than 0.6m/s, HD state, between 0.6m/s and 0.2m/s,
and SNF state, walking speed less than 0.2m/s [7]. Walking speed was assumed
normally distributed.
Walking speed was taken from a previous randomized clinical trial of reflex-
based electrical gait therapy that showed a walking speed of 0.41 ± 0.32m/s
(control group), 0.55 ± 0.26m/s (reflex-based) five months after the patients
completed gait training [17].

2.2 Long Term Model


The long-term model consisted of a Markov model with a cycle length of 3 month
(see Figure 2). Probabilities where expressed as yearly and recalculated into rates
for the Markov model.
The patients could leave the HI, HD, and SNF states by either having a
recurrent stroke or dying from other unrelated causes.
The probability of dying from other unrelated causes was set to 90% of the
mortality rate for the general population, which was calculated from life tables
(EU-15), Eurostat [18]. The rate was decreased as the general mortality rate
includes stroke related deaths. Alternatively, the mortality rate would be
overestimated in the model. It was decreased by 10% as stroke account for
approximately one out of ten deaths [2].
424 K. Hennings et al.

Specialized
Home Home
Nursing
Independent Dependent
Facility

Dead

Fig. 2 Illustration of the long-term Markov model used for modelling the functional state of
the stroke patients

2.3 Validation
The predictions of the model were compared with case fatality for 30 days [19]–
[23], [13], [24], 3 months [19], [20], [25], [26], 1 year [16], [20], [22], [23], [13], 5
years [16], [23], [13], [9], and 10 year [23]. Furthermore, the predictions of the
model with respect to functional dependence were compared for; number of
patients that live at home 3 months after their initial stroke [22], female patients
discharged to their home [16], male patients discharged to their home [16], female
patients discharged to SNF [16], male patients discharged to SNF [16], and overall
dependent on support after stroke [16].

2.4 Implementation
The model was implemented in Excel 2013 using half-cycle corrections for the
Markov model.

Female Male

85+
75-84
65-74
55-64
45-54
35-44
25-34

-2.500 -1.500 -500 500 1.500 2.500

Fig. 3 Gender and age profile for the cohort of stroke patients used in the simulations
Modeling the Functional Dependence of Stroke Patients 425

2.5 Simulations
The model was used to simulate the functional dependence of stroke patients with
and without reflex-based electrical therapy for a cohort representative of stroke
patients in Denmark for 2015.
Estimation of stroke incidences was based on data reported by Truelsen et al.,
2006 [1] and demographic information from Eurostat. This resulted in an
estimated 14.049 annual strokes in Denmark (see Figure 3). The simulations were
calculated for 10 years after the initial stroke.

3 Results

The model using walking speeds from the control group reproduced the
experimental findings on stroke mortality (see Figure 4).
For the control group the model predicted that 73,0% of surviving patients
would be discharged to their home (from experimental data, male: 76.6%, female:
70.9% [16]) while 26.8% would be discharged to a specialized nursing facility
(from experimental data, male: 23.4%, female: 25.5%) [16], and that 69.9% would
be dependent on support after stroke (from experimental data: 65.0% [16]).
The model was used to estimate the functional dependency of both reflex-
based electrical gait therapy and controls in the years following their initial stroke
(see Table 1); it predicted that when the walking speed of the patients increased,
more patients would be functionally independent. Despite a higher mortality of
functionally dependent patients, the model predicted only a minor decrease in
mortality.

100%

80%

yt 60%
lia
tr
o
M 40%

20%

0%
0 2 4 6 8 10
Time [years]

Fig. 4 Mortality predicted by the model (solid-line) compared with experimental data
(circles)
426 K. Hennings et al.

Table 1 Predicted functional state

Control
HI HD SNF DE

1 month 25,9 37,1 23,0 14,0

1 year 22,0 32,0 20,4 25,6

5 years 11,6 17,8 12,8 57,8

10 years 5,6 9,2 7,5 77,7

Reflex-based Electrical Gait Therapy


HI HD SNF DE

1 month 34,3 38,2 13,5 14,0

1 year 29,2 33,2 12,0 25,5

5 years 15,6 19,2 7,6 57,5

10 years 7,7 10,3 4,6 77,4

4 Discussion

The results of this study demonstrate that it is possible to develop simple models
that are capable of predicting the functional dependency and progression of stroke
patients. The model was designed to use outcome measurements that can be
obtained from small-scale clinical trials without the need of following the patients
for extended periods. This implies that the model can make predictions on the
effect of novel training methods very early in their development. With time, the
model must be validated by comparing predictions of the model with experimental
observations not yet available on the outcome of alternative gait training methods.
However, it is interesting that it was possible to predict the mortality of the
patients based only on parameters set from experimental observations, without the
need for adjusting one or more free parameters.
The long-term model represent a drastic simplification of reality. One
significant simplification is that patients will only move between the HI, HD and
SNF states when the patients have a recurrent stroke, and they can only move to a
worse functional state. In reality, the patients are likely to improve with time if
they do not have a recurrent stroke. However, the patients will also be
progressively more functionally dependent as they age, and these two effects will
counteract each other. There is currently insufficient experimental observations to
assess whether they will negate each other; however, they are likely to affect both
treatment groups equally.
The validity of the model rests on the assumption that preferred walking speed
is an adequate predictor of functional state. This assumption is supported by the
finding that walking speed is a good predictor of the onset of functional
Modeling the Functional Dependence of Stroke Patients 427

dependence [27] and is correlated with dependence in activities of daily living


[28]. Therefore, walking speed has been labeled as a vital sign for the functional
state of patients [7], [8]. This is also supported by the observation that the model
was able to reproduce the experimental observations of functional state of patients
after their initial stroke.
Another consideration is whether the extrapolation from a limited size of the
control/intervention groups to the whole population of stroke patients is justified.
In the design of the model, the walking speed limits for the HI, HD, and SNF
states were taken from [8], which resulted in a distribution in these states that were
comparable with what was experimentally observed [16]. This supports the notion
that the control group is representative of the general population; however, the
model would be greatly enhanced with a better estimation of the distribution of
walking speeds for the control group and for the group receiving alternative gait
training.

5 Conclusion

The current study introduces a simple and yet effective model, to predict the
influence of novel methods for gait training on functional dependency of stroke
patients from small-scale clinical trials.

6 Scientific Disclosure

K. Hennings is the CEO of Nordic NeuroSTIM and is an adjunct associate


professor at Aalborg University. S. Gervasio is a Research Specialist at Nordic
NeuroSTIM and a Ph.D. student at Aalborg University.

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Startling Acoustic Stimuli Elicit Rapid Hand
Extension Following Stroke

Claire F. Honeycutt1, Ursina A. Tresch2, and Eric J. Perreault1


1
Rehabilitation Institute of Chicago, Chicago, IL 60611 USA
and
Northwestern University, Chicago, IL 60611 USA
2
Northwestern University while enrolled at ETH Zurich, Switzerland
claire.honeycutt@gmail.com, ursina.tresch@me.com,
e-perreault@northwestern.edu

Abstract. Loud startling acoustic stimuli can involuntarily elicit planned


movements faster than is possible voluntarily. This phenomenon, known as
startReact, is thought to be mediated through brainstem pathways. The startReact
can be elicited in stroke survivors with a cortical lesion. This has been
demonstrated for elbow motions, thought to have significant input from brainstem
pathways. This study sought to determine if the startReact can also be elicited for
hand movements following stroke, even though these are driven predominantly by
the motor cortex. Data were collected from 8 stroke survivors performing rapid
hand extension movements. StartReact responses could be elicited in 7 of 8
subjects. Across all subjects, the startling acoustic stimuli were able to decrease
movement times substantially (∆ 57ms; p ≈ 0) when indicators of startle were
detected. However, these responses were elicited less frequently than previous
reports for startReact at the elbow. Nevertheless, the intact startReact response
suggests that the integrity and actions of the pathways mediating this response
should be considered when rehabilitating the hand following stroke.

1 Introduction

Movement deficits following stroke are particularly prevalent in the hand, leading
to significant reduction in independence and the ability to participate in activities
of daily living [1]. Consequently, there have been many efforts to develop
therapeutic approaches for restoring hand function following stroke. One recent
suggestion is that startle-elicited movements may be a useful component of
therapeutic regimen, or as a tool for helping to design a subject-specific regimen.
This suggestion was based on the finding that startling acoustic stimuli
administered in the presence of a movement plan can lead to rapid movements
following stroke that are substantially faster than those elicited voluntarily [2].
These startle-elicited movements are often described as startReact responses [3], a
term used to distinguish this response from the classic startle response elicited in

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 431
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_65, © Springer International Publishing Switzerland 2014
432 C.F. Honeycutt, U.A. Tresch, and E.J. Perreauult

the absence of a movemeent plan. StartReact responses are thought to involve thhe
brainstem pathways know wn to contribute to the classic startle reflex [4]. Whiile
startReact responses havee been demonstrated for simple arm movements in strokke
survivors, it is unclear if they are present in the hand, which relies much less oon
projections from the brainnstem than do more proximal muscles.
Given that hand moveements are particularly impacted by stroke, our objectivve
was to determine if startRReact responses for hand movements are present in strokke
survivors. Our hypothesiss was that startling acoustic stimuli could be used to eliccit
rapid hand extension mov vements in this population. This was based on the findinng
that even though hand mo ovements rely predominantly on corticospinal projectionns,
a smaller number of reticu ulospinal projections do exist in non-human primates [55]
and are likely to be preseerved in humans [6]. Furthermore, it has been suggesteed
that humans may rely mo ore on reticulospinal pathways for movement executioon
following a stroke than before
b [7]. If true, our hypothesis would suggest that thhe
integrity and function of the reticulospinal pathways should be considered wheen
designing therapeutic inteerventions to restore hand function following stroke.

2 Methods

2.1 Subjects
Data were collected from
m 8 chronic stroke subjects, whose details are provided iin
Table 1. The Northwesteern University Institutional Review Board IRB approveed
all experiments (STU92044).

Table 1 Subject characteristiics

2.2 Protocols
Subjects were seated in a chair holding a ball in their right hand with the righht
elbow joint flexed at 90 degrees, and the hand in a slightly extended position at
rest. Each trial involved the subject ballistically extending all fingers and thhe
thumb. Auditory cues were
w used to indicate when the subject should movve.
Subjects were instructed to wait in a relaxed position for two non-startling, low
w-
intensity acoustic stimuuli (80 dB). A low-intensity (80 dB) warning cuue
(WARNING) indicated th hat the subject should prepare to perform the extensioon
Startling Acoustic Stimuli Elicit Rapid Hand Extension Following Stroke 433

task. A second low-intensity sound (GO) was used to cue the movement. The time
between the WARNING and GO cues was uniformly distributed between 1.5-3.5 s.
Subjects performed 10-15 training trials to become accustomed to the task.
Following training, each participant completed six blocks of fifteen trials. During
each block 3-5 trials were randomly selected to be startReact trials. During
startReact trials, the GO signal was replaced by a startling, high-intensity acoustic
stimulus (128 dB).
Bipolar electromyogram (EMG) electrodes were used to record activity from the
right extensor digitorum communis (EDC) and the left and right sternocleidomastoid
(SCM) muscles in all trials. EDC activity was used to detect movement onset, and
SCM activity was used to detect the presence of a startle response [8]. EMG signals
were amplified and filtered with a band-pass filter of 10-1000 Hz. The resulting
signals were anti-alias filtered by 5th order Bessel filters with a 500 Hz cut-off
frequency and sampled at 2500 Hz. An electro-goniometer was fixed on the right
index finger to quantify hand extension.

2.3 Analysis
The primary outcome measures for these experiments were the EMG onset
latencies for the EDC and SCM muscles. EMG signals were first rectified and
filtered. Onsets were identified automatically by detecting the time at which EMG
rose significantly above the background activity present before the GO cue. All
trials were visually inspected for accuracy, including excluding trials when the
subject did not move or moved before the GO signal. The reviewer was blinded
with respect to trial type during this process. The presence of a startle was detected
by activity in the right or left SCM within 120ms of the GO signal [8]. Trials where
a startle was detected were designated SCM+, while those without were designated
SCM-.
To determine if a startReact occured, it was necessary to differentiate between
intensity-dependent [9] and startle-dependent [3] effects of the high-intensity
stimulus, since both can lead to faster reaction times. The intensity-dependent
effect was quantified by comparing low-intensity SCM- (LI SCM-) trials to high-
intensity SCM- (HI SCM-) trials; the startle-dependent effect was quantified by
comparing HI SCM- trials to high-intensity SCM+ (HI SCM+) trials. SCM+ was
observed in 42% of high-intensity trials and 7% of low-intensity trials.
Our hypothesis was that startReact is intact in hand extension. An intact
startReact response would be indicated if the onset of muscle activity in the EDC
was significantly faster in the HI SCM+ trials than in the HI SCM- trials. This
hypothesis was tested using an ANOVA of a linear mixed-effect model with trial
type (LI SCM-, HI SCM+, HI SCM-) as the independent factor and onset latency as
dependent factor. Subjects were treated as a random effect. Tukey’s Honestly
Significant Difference (TukeyHSD) was applied for all post-hoc comparisons.
Differences with a probability lower than 0.05 were considered to be significant.
Error bars in figures relate to standard deviations across all collected trials.
434 C.F. Honeycutt, U.A. Tresch, and E.J. Perreault

3 Results

Our main finding was that hand extension was susceptible to startReact in stroke
subjects. The onset latencies for the EDC muscle were faster in the HI SCM+ trials
compared to HI SCM- and LI SCM- trials. Individual trials from one of the faster
subjects is shown in Fig. 1A. In this subject, average onset latencies for all trials
collected in the three illustrated conditions were 85±7 ms, 94±11 ms, and 187±51
ms, respectively. Group results showed a similar trend (Fig. 1B). The latency at
which the EDC was activated depended significantly on the trial type (F2,442 =
135.1; p < 0.0001). Post-hoc tests confirmed that the average response of the HI
SCM+ (115±45 ms) trials was significantly faster than that for the HI SCM-
(172±83 ms) and the LI SCM- (236±60 ms) trials (all p ≈ 0).
While HI SCM+ trials showed faster onset latencies, the kinematics of these
movements were nearly unchanged from those in the LI SCM- and HI SCM- trials.
Indeed, even spasticity was evident in all trials. The only difference was the time
required to complete the movement.

Fig. 1 Sample data and EDC onset latency. A) Typical EMG from the EDC muscle for
each trial type. Each response is from a single trial. B) Group results comparing EDC onset
latencies between HI SCM+, HI SCM-, and LI SCM- trial types. ***P < 0.0001.

4 Discussion and Conclusions

Our results demonstrate that the startReact response is intact following stroke, and
that it can be used to elicit hand extension movements that are more rapid than
those that can be made voluntarily. Though we have only performed a
preliminary, qualitative kinematic analysis at this point, it appears that these faster
movement onset times do not lead to a change in the quality of the movement that
is made. Together, these results suggest that the reticulospinal projections to the
hand, though sparse, remain intact in the subjects tested. An assessment and
Startling Acoustic Stimuli Elicit Rapid Hand Extension Following Stroke 435

possibly even targeting of these pathways may benefit the design of rehabilitation
therapies targeting the hand, though their ability to improve movement quality
seems limited to faster rather than better movements, at least in the hand.
Interestingly, the observed responses in the hand were weaker than previously
reported for the elbow [2]. The probability of eliciting a startReact during hand
extension was approximately only 50% of that for our previously reported elbow
movements. The lower probability does not likely relate to increased impairment,
as the population evaluated here was less impaired than the population for which
elbow startReact was evaluated. A diminished response at the hand is not
unexpected given that the startReact response is likely mediated through the
reticulospinal tract, which has fewer projections to the hand than it does to more
proximal muscles. The weaker response for hand extension could also reflect a
decreased proficiency at this task. StartReact responses cannot be elicited for
movements that cannot be prepared in advance [10]. Given that hand extension is
more challenging for stroke survivors than elbow movements, it also may be more
difficult to prepare.

Acknowledgment. This work was supported by the National Institutes of Health grants
R01 NS053813 and K99 HD073240.

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[8] Carlsen, A.N., Maslovat, D., Lam, M.Y., Chua, R., Franks, I.M.: Considerations for
the use of a startling acoustic stimulus in studies of motor preparation in humans.
Neuroscience and Biobehavioral Reviews 35, 366–376 (2011)
[9] Kohfeld, D.L.: Effects of the intensity of auditory and visual ready signals on simple
reaction time. J. Exp. Psychol. 82, 88–95 (1969)
[10] Carlsen, A.N., Dakin, C.J., Chua, R., Franks, I.M.: Startle produces early response
latencies that are distinct from stimulus intensity effects. Experimental Brain Research
Exp. Brain. Res. 176, 199–205 (2007)
Detection of the Onset of Voluntary
Movements Based on the Combination
of ERD and BP Cortical Patterns

Jaime Ibáñez1 , J. Ignacio Serrano1 , M. Dolores del Castillo1 ,


Esther Monge2 , Francisco Molina2 , Francisco Rivas2 , Isabela Alguacil2 ,
J. Miangolarra-Page2, and José Luis Pons1
1
Bioengineering Group of the Spanish Research Council,
La Poveda, Arganda del Rey, Madrid, 28500 Spain
jaime.ibanez@csic.es
2
LAMBECOM Group, Universidad Rey Juan Carlos, Alcorcón, Madrid, Spain

Abstract. The electroencephalographic activity allows the characterization


of movement-related cortical processes. This information may lead to novel
rehabilitation technologies with the patients’ cortical activity taking an ac-
tive role during the intervention. For such applications, the reliability of the
estimations based on the electroencephalographic activity is critical both in
terms of specificity and temporal accuracy. In this study, a detector of the
onset of voluntary upper-limb reaching movements based on cortical rhythms
and slow cortical potentials is proposed. To that end, upper-limb movements
and cortical activity were recorded while participants performed self-paced
movements. A logistic regression combined the output of two classifiers: a)
a naı̈ve Bayes trained to detect the event-related desynchronization at the
movement onset, and b) a matched filter detecting the bereitschaftspotential.
On average, 74.5±10.8 % of the movements were detected and 1.32 ± 0.87
false detections were generated per minute. The detections were performed
with an average latency of -89.9 ± 349.2 ms with respect to the actual move-
ments. Therefore, the combination of two different sources of information
(event-related desynchronization and bereitschaftspotential) is proposed as a
way to boost the performance of this kind of systems.

1 Introduction
The development of Brain-Computer Interfaces (BCIs) based on the elec-
troencephalographic (EEG) activity for the functional rehabilitation of pa-
tients with motor disabilities has gained special interest over the last years
[1, 2]. The main purpose of BCIs in such scenarios is to provide a way to
promote the neural rehabilitation of the patient. EEG systems allow the on-
line characterization of the cortical activity over the motor cortex while the
measured subject is performing motor tasks. This way, it becomes possible to
detect online when a person is attempting or imaging a movement [3, 4, 5],
and to predict certain properties of the movement to be performed [6, 7, 8].

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 437
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_66,  c Springer International Publishing Switzerland 2014
438 J. Ibáñez et al.

This information may in turn be used to close the loop with neuroprosthetic
or neurorobotic devices, thus providing a natural interface between the pa-
tient’s intentions and the actuation of external devices [9]. In this regard,
recent studies have proven the importance of the proprioceptive feedback
timing to achieve associative neural facilitation [10, 11].
In a series of previous studies, it has been proposed the use of the Bere-
itschaftspotential (BP) to detect the movement intention [4, 12, 13, 8, 14].
The BP is defined as a slow decay of the EEG voltage over the central regions
of the cortex right before a voluntary movement is performed [15]. Given the
nature of the BP as an identifiable pattern that is decaying until the move-
ment starts, it becomes suitable to achieve temporal precision in the detection
of the onset of the movement. In fact, previous studies showing results of on-
line systems based on this pattern indicate that average latencies of 315 ±
165 ms can be obtained [14].
The BP, nonetheless, presents some limitations. First, this pattern shows
a reduced amplitude (in the order of few μV), which makes it vulnerable
to external sources of noise. In addition, the BP is not always detectable,
since some subjects do not present a significant pattern during self-paced
movements.
A second cortical pattern associated to the execution of voluntary move-
ments is the event-related desynchronization (ERD). This pattern consists of
a decay of the power in some specific cortical rhythms that takes place mainly
over the sensorimotor cortex in areas contralateral to the limb (in case upper-
limb movements are considered) [16]. Although a variable anticipation may
be observed in the ERD of a specific channel and frequency in a subject
during consecutive movements, the spatio-tempo-frequential distribution of
the ERD observed when averaging a number of EEG segments preceding
voluntary movements shows a clear pattern attached to the movement event.
In this present study, a detector of the onsets of movements is proposed
based on the combined detection of the ERD and the BP patterns preceding
volitional movements. The design of the system as well as its validation with
data collected from healthy subjects performing self-paced reaching move-
ments is presented here.

2 Methods
2.1 Participants
Six healthy subjects (all males, right-handed and between 27 and 35 years
old) were measured for the present experiments. None of them had any prior
experience with BCI paradigms.
Detection of the Onset of Voluntary Movements 439

2.2 Experimental Protocol


Each participant was measured during one single session. The study was
performed in a sound and light-attenuated room. Participants sat in a com-
fortable chair with their arms supported on a table. During the measurement
phase, participants were instructed to remain relaxed with their eyes open
and their gaze fixated on a point on the wall. They were asked to perform
self-initiated reaching movements with the dominant arm. The average dis-
tance between consecutive movements was around 8-15 s. During the resting
state between movements, participants were asked to remain as relaxed and
quite as possible, whereas they were asked to start a movement as soon as
they felt the urge to do it.
The intervals containing at least 5 s of resting activity followed by a self-
initiated reaching movement were considered valid trials and were used in
the subsequent steps of the data analysis. On average, 53 ± 8 trials were
collected.

2.3 Data Acquisition


The movements of the arm were measured with solid-state gyroscopes. Three
gyroscopes (Technaid S.L., Madrid, Spain) placed on the hand dorsum, the
distal third of the forearm, and the middle of the arm measured the limb
kinematics. The data were sampled at 100 Hz.
EEG signals were recorded from 31 positions (AFz, F3, F1, Fz, F2,
F4, FC3, FC1, FCz, FC2, FC4, C5, C3, C1, Cz, C2, C4, C6, CP3, CP1,
CPz, CP2, CP4, P3, P1, Pz, P2, P4, PO3, PO4 and Oz, all according to
the international 10-20 system) using active Ag/AgCl electrodes (Acticap,
Brain Products GmbH, Germany). The reference was set to the voltage
of the earlobe contralateral to the arm moved. AFz was used as ground.
The signal was amplified (gUSBamp, g.Tecgmbh, Austria) and sampled at
256 Hz.

2.4 Detection of the Onset of the Movements


To detect the onsets of the movements, the data from the gyroscopic sensor
that activated the first during reaching movements in each subject was used.
The data were low-pass filtered (Butterworth, order 2, < 10 Hz). The peak
amplitude was estimated for each subject performing the reaching movement.
The threshold amplitude for the detection of the onsets of the movements was
set to 5 % of this reference amplitude.
440 J. Ibáñez et al.

2.5 Description of the Classifier Architecture and


Validation
The core of the detector was a combination of the information associated to
the ERD and BP patterns observed in the participants. The validation of the
system was carried out following a leave-one-out methodology, i.e. once the
trials had been identified, each of them was classified with a detector trained
with the rest of the trials of the session.

2.5.1 ERD-Based Detection of the Movement Onset


A naı̈ve Bayes classifier was used to detect the ERD pattern observed at
the onset of the movements. First the signals were bandpass filtered (Butter-
worth, 3th order, 6 Hz < f1, 35 > f2) and a small laplacian filter was applied
[17]. The channels from the frontal, fronto-central, central, centro-parietal
and parietal positions were kept. The power values were estimated for the
frequency interval 7-30 Hz in steps of 1 Hz. Welch’s method (Hamming win-
dows of 1 s, 50 % overlapping) was used to estimate the power values of
windows of 1.5 s. Estimations were performed at a rate of 8 Hz.
The power estimations obtained in all the training trials from -3 s to -0.5 s
(with respect to the movement onsets) were labeled as resting state examples,
whereas the estimations generated at t = 0 s where labeled as movement
examples. The Bhattacharyya distance was used for space dimensionality
reduction. The 10 best features according to this distance were selected to
build the classifier.
The classifier was applied to the test data. Estimations about movement
intention were generated every 125 ms.

2.5.2 BP-Based Detection of the Movement Onset


A similar procedure to the one proposed in [8] was used to detect the BP.
A finite impulse response (with linear phase) bandpass filter (0.05 Hz < f1,
1 Hz > f2, 15th order) was used. This solution was adopted since linear
preservation is crucial to extract the entire BP pattern.
Then spatial filtering and channel selection were performed. Three virtual
channels were computed from the original 31 channels in the experimental
set-up. These channels were extracted applying the same spatial filter as in
[8] to positions C1, Cz and C2, i.e. the average potential of channels F3,
Fz, F4, C3, C4, P3, Pz and P4 was subtracted to these three channels. The
average BP was computed for the three virtual channels using the training
data and the channel with highest absolute peak at the movement onset was
selected for the movement onset detection.
Using the training data set, a matched filter was obtained using the pre-
viously selected channel. To that end, the average BP was obtained from the
time interval between -1.5 s and 0 s (with 0 s being the movement onsets
Detection of the Onset of Voluntary Movements 441

estimated by the gyroscopes). The matched filter was applied to the virtual
channel in the validation data set.

2.5.3 Combination of the Two Estimations


The combination of the outputs from ERD and BP detectors (real-valued
signals from the application of the Bayesian classifier and the matched filter,
respectively) was carried out by a logistic regression classifier. To build the
classifier, the examples of the resting and movement conditions were extracted
from the training data set. The estimations of the two classifiers (ERD and
BP) from -3 s to -0.5 s with respect to the movement onset (in steps of 125 ms)
were used to model the resting state. The movement state was modeled from
the output estimations of the ERD and the BP classifiers at the movement
onset.

2.5.4 Threshold Selection


A threshold was applied to the output of the detector to decide at each mo-
ment whether movement intention was detected. The threshold was optimally
obtained from the training data set, following the criterion of maximizing the
percentage of good trials (GT), which were trials with a true positive (TP)
and no false positives (FP). The definition of these metrics is further elabo-
rated in 2.6

2.6 Metrics of the Detector Performance and


Threshold Selection
Three metrics were used to evaluate the ability of the system to reliably detect
movement intentions. The TP rate was defined as the percentage of trials with
a movement detection in the time interval from -0.75 s to +0.75 s with respect
to the movement onset. The precision of the detector was characterized as
the number of FP per minute (rate of detections during the resting intervals).
Therefore, one or more false activations could be encountered in a single trial.
The percentage of GT was obtained by counting the amount of trials in which
no FP were generated and a TP was achieved. Finally, the latencies of the
detections of the onsets of movements were also computed to analyze the
time accuracy of the system.

3 Results
The average BP observed in all subjects is shown in Fig. 1. The average
(across subjects) BP peak was found at -19.8 ± 57.6 ms with respect to the
onset of the movements. An homogeneous BP pattern could be found in all
measured subjects. In addition, Fig. 2 presents the spatial distribution of the
442 J. Ibáñez et al.

0.8
Normalized EEG amplitude
0.3 0.40.1 0.6

−1.6 −1.2 −0.8 −0.4 0


time (s)

Fig. 1 Average BP of all subjects (discontinuous lines, and average BP across


subjects (solid line)

ERD and BP patterns for all subjects measured. Unlike with the BP, the
ERD presented visible variations in terms of spatial distribution, although,
in general, a contralateral predominance was observed.
The results obtained in the detection of the onsets of movements using the
proposed methodology are summarized in Table 1. On average, in 63.3±13.8
% of the trials the movement was detected and no previous false activations
were generated in the same trial. In addition, 74.5±10.8 % of the movements
were detected with a rate of 1.32±0.87 false activations per minute during
the resting intervals.
The average latency of the TP was -89.9 ± 349.2 ms. The histogram of the
latencies of all detections is shown in Fig. 3. The figure shows a tendency of
the detections to anticipate the actual onsets of the movements.
Detection of the Onset of Voluntary Movements 443

αERD βERD BP

Fig. 2 First and second columns show the patial distribution of the α-ERD (be-
tween 8-12 Hz) and β-ERD (between 13-30 Hz) obtained by comparing a window
of 1.5 s ending at the movement onset with an equivalent window 4 s before the
onset. The third column shows the spatial distribution of the BP peak amplitude.
444 J. Ibáñez et al.

14

12

10
Observations (%)

0
-750 -375 0 +375 +750
Latency (ms)
Fig. 3 Latencies of the TP with respect to the actual onsets of the movements

Table 1 Results obtained with all subjects and average results

Code GT (%) TP (%) FP/min Latency (ms)


C1 81.3 82.8 0.47 -48±351
C2 63.8 81.0 1.34 -24±278
C3 39.0 56.1 2.63 -180±476
C4 64.6 70.8 0.38 -198±322
C5 69.8 84.9 1.13 -3±388
C6 61.5 71.2 1.96 -164±290
Average 63.3±13.8 74.5±10.8 1.32±0.87 -89±349

4 Discussion and Conclusions


A methodology to detect the onset of voluntary movements with time preci-
sion based on the EEG activity has been proposed. The novelty of the study
lies in the combination of the two most well-known movement related cortical
patterns: the ERD and the BP. These patterns are known to reflect different
underlying aspects of the motor planning process [18, 15]. Therefore, it is ex-
pected that a successful fusion of them may result in an improved estimation
of the onset of voluntary movement events, specially in those cases in which
either the ERD or the BP is not reliably detected in a given subject [19]. The
results obtained with the here proposed detector point to an improvement
in the temporal accuracy of the estimations, as compared with other similar
Detection of the Onset of Voluntary Movements 445

online-feasible techniques [14]. Nevertheless, the use of a significantly higher


number of electrode positions to detect ERD information in this study makes
it less suitable for clinical applications. Therefore, it should be further studied
the detection improvement associated with different number of EEG chan-
nels and how significantly the ERD-based classifier improves the detection of
movement intentions.
The use of gyroscopes to detect movement events has proven to be ade-
quate for functional tasks (as the reaching movements used for the present
experiments) since the average BP patterns show similar latencies than the
ones observed in studies using the electromyographic activity to detect move-
ment events.
In future studies it should be studied how reliably can this kind of EEG-
based systems work with patients suffering from brain damages (as stroke
patients), and how would a patient react to an external stimulus (electrical
or mechanical) driven by a system as the detector proposed here.

Acknowledgment. This work has been funded by grant from the Spanish Ministry
of Science and Innovation CONSOLIDER INGENIO, project HYPER (CSD2009-
00067), from Proyectos Cero of FGCSIC, Obra Social la Caixa (CSIC), from Project
CP Walker (DPI2012-39133-C03-01) and from the project PIE-201350E070.

References
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ordination and Motor. Rehabilitation 14(2), 168–171 (2006)
2. Buch, E., Weber, C., Cohen, L.G., Braun, C., Dimyan, M.A., Ard, T., Mellinger,
J., Caria, A., Soekadar, S., Fourkas, A., Birbaumer, N.: Think to move:
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Online detector of movement intention based on EEG - Application in tremor
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suitable to realize a “brain switch”? Clin. Neurophysiol. 120(1), 24–29 (2009)
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IEEE Trans. Neural Syst. Rehabil. Eng. 11(2), 145–147 (2003)
Flexible Thread-like Electrical Stimulation
Implants Based on Rectification
of Epidermically Applied Currents
Which Perform Charge Balance

Antoni Ivorra* and Laura Becerra-Fajardo

Dept. of Information and Communication Technologies


Universitat Pompeu Fabra, Barcelona, Spain
antoni.ivorra@upf.edu

Abstract. Miniaturization of implantable medical electronic devices is currently


compromised by the available means for powering them. Most common energy
supply techniques for implants – batteries and inductive links – comprise bulky
parts which, in most cases, are larger than the circuitry they feed. For overcoming
such miniaturization bottleneck in the case of implants for electrical stimulation,
we recently proposed and demonstrated a method in which the implants operate as
rectifiers of bursts of high frequency current supplied by skin electrodes. In this
way, low frequency currents capable of performing stimulation of excitable tissues
are generated locally through the implants whereas the auxiliary high frequency
currents only cause innocuous heating. The electronics of the prototype we
demonstrated previously consisted of a single diode. As a consequence, it caused
dc currents through it which made it impractical for clinical applications. Here we
present an implantable prototype which performs charge balance for preventing
electrochemical damage. It consists of a tubular silicone body with a diameter of 1
mm, two peripheral electrodes and a central electronic circuit made up of a diode,
two capacitors and a resistor. We also report that this circuitry works even when
water immersed, which may avoid the need for hermetic packaging.

1 Introduction

To build interfaces between the electronic domain and the human nervous system
is one of the most demanding challenges of nowadays engineering. Fascinating
developments have already been performed such as visual cortical implants for the
blind and cochlear implants for the deaf. Yet implantation of most electrical
stimulation systems requires complex surgeries which hamper their use in diverse
clinical scenarios. For instance, that is the case of movement restoration: currently
available implantable systems consisting of central stimulation units wired to the

*
Corresponding author.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 447
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_67, © Springer International Publishing Switzerland 2014
448 A. Ivorra and L. Becerra-Fajardo

stimulation electrodes are not adequate for applications in which a large number of
targets must be individually stimulated over large and mobile body parts, thus
hindering solutions for patients suffering paralysis due to spinal cord injury or
other neurological disorders.
An alternative to centralized stimulation systems could consist in developing a
network of addressable single-channel wireless microstimulators which could be
implanted with simple procedures such as injection, and which would be activated
in coordinated patterns by an external automated controller. In fact, such solution
was proposed and tried in the past [1,2]. However, these previously developed
microstimulators are stiff and considerably large (diameters > 2 mm) which makes
them unsuitable for some applications because of their invasiveness. Further
miniaturization was prevented because of the use of inductive coupling and
batteries as energy sources.
In [3] we proposed and in vivo demonstrated an alternative method for
performing electrical stimulation by using electronic implants: the implanted
devices rectify bursts of innocuous high frequency currents supplied to the tissue
of interest by remote electrodes so that low frequency (LF) currents are generated
locally through the implants and these resultant currents are capable of performing
stimulation of local excitable tissues without disturbing neighbor tissues. This idea
is schematically illustrated in Fig. 1. In comparison to inductive coupling – or to
electrochemical batteries – this method offers an unprecedented potential for
miniaturization. Note that only two peripheral electrodes are required both for
picking-up the high frequency (HF) currents and for performing stimulation. In
addition, all necessary electrical components, maybe with the exception of the
electrodes, can be integrated in a single integrated circuit or in a tiny hybrid
microcircuit.
The proposed method requires a minimum voltage drop to operate and this
implies that, in most applications, it will be necessary that both electrodes are
quite separated (from some millimeters to a very few centimeters). Consequently,
we propose elongated implant bodies in which most of their length consists of

Fig. 1 The proposed technology is based on externally applying an inert HF current which
is rectified by the implants into LF currents capable of stimulation
Flexible Thread-like Electrical Stimulation Implants 449

flexible and stretchable materials whose mechanical properties match those of


neighboring living tissues. Hence the implants may look like short pieces of
flexible and stretchable thread. Because of such feature, and because of their
intended functionality, we coined the name “Electronic Axons” (eAXONs) for
these implants.
We envision eAXONs with advanced communication, control and sensing
capabilities which can be deployed in large numbers thus forming a complex
network controlled by an external autonomous unit which delivers innocuous high
frequency currents [4]. These systems will be capable of executing complex
stimulation patterns such as those that would be required for fine movement
restoration in paralysis patients. The advanced eAXONs to be created will require
future development of Application Specific Integrated Circuits (ASICs) and
specific packaging and interconnection techniques [5]. Meanwhile, we have
demonstrated that those advanced eAXONs are feasible by developing non-
implantable bulky eAXONs based on discrete electronic components [6] which
can be seen performing individual stimulation of segments of an earthworm at
https://sites.google.com/site/electronicaxons.
In [3, 5] we demonstrated the method by testing implants consisting of just a
diode. We later discovered that such demonstration had already been performed in
vertebrates by at least to independent research teams in the 60s [7,8]. However,
those studies are barely cited and, in fact, no references to them are found after the
80s. No advanced rectifiers have been proposed until now. In historical
perspective it is easy to understand such neglect: at the time microelectronics was
at its infancy and, therefore, the coils and batteries were not the miniaturization
bottleneck but the electronics.
Simple rectifiers, such as diodes, do not allow the networked neuroprosthetic
system that we envision. However, implants consisting of a simple rectifier would
be applicable to cases in which a single target must be stimulated in a minimally
invasive manner. On the other hand, implants consisting of just a diode are not
adequate because they cause dc currents through them. Passage of dc current
through an electrode will cause electrochemical reactions that will damage both
the electrodes and the tissues [9]. For that reason, charge-balanced waveforms,
resulting in a null dc component through the electrodes, are employed in electrical
stimulation systems.
Here we present an implantable single-diode prototype which performs charge
balance. It consists of a tubular silicone body with a diameter of 1 mm, two
peripheral electrodes and a central electronic circuit made up of a diode, two
capacitors (acting as a single one) and a resistor.
This prototype may be the basis for minimally invasive systems in which a
single target needs to be stimulated (or in which multiple targets are sufficiently
separated so that the corresponding implants can be selectively powered from
multiple external electrodes). For instance, besides a few applications in the area
of Functional Electrical Stimulation, such as peroneal nerve stimulation for the
correction of drop foot [10], these systems would be very well suited for
applications in the area of peripheral nerve stimulation for treatment of chronic
pain [11].
450 A. Ivorra and L. Becerra-Fajardo

2 Proposed Simple Circuitry to Perform Charge Balance

2.1 The Circuit and Its Generic Design Constraints


The proposed circuit for performing charge balance is represented in Fig. 2. The
implant circuit is drawn in black whereas a simplified circuit corresponding to the
rest of the system (i.e. external generator and tissue impedances) is drawn in gray.
The nodes A and K represent the electrodes of the implant whose impedances are
neglected for the sake of simplicity.
At the beginning of the ac burst, the capacitor is discharged and rectified current
flows from K to A through the diode thus progressively charging the capacitor. As
the capacitor charges, higher voltage differences between K and A are required in
order to obtain conduction through the diode and, as a consequence, rectified
current decreases. Once the ac burst finishes, the capacitor discharges through the
tissues and the implant resistor.

Fig. 2 Proposed circuitry to perform charge balance (in black). The indicated numerical
values have been chosen for reproducing the experiment performed with the implemented
prototype (section 3).

A capacitor with a large enough capacitance value must be employed so that


rectified current flows for a significant amount of time during the ac burst. In other
words, a large capacitance is required in order to allow generation of long enough
current pulses capable of stimulation. However, it must be taken into account that
the capacitor must fully discharge in between ac bursts and, since the discharge
time constant is proportional to the capacitance, such value cannot be extreme. It
could be argued that the time constant also depends on the resistance value of the
implant resistor, but, it must be noted that such resistance cannot be reduced
excessively; otherwise the high frequency voltage to be rectified will be too low
because of short-circuiting. In addition, the capacitance value may be constrained
due to size limitations. Not many capacitors exist with submillimeter dimensions,
capacitances above 1 μF and the capability to withstand some volts or tens of volts
as it is required in this application.
Flexible Thread-like Electrical Stimulation Implants 451

Schottky diodes appear preferable to other diodes because of their lower forward
voltage drop and their very fast switching capabilities.

2.2 SPICE Simulation


Fig. 3 displays some results from a SPICE simulation of the circuit represented in
Fig. 2. Specifically, a time transient simulation has been performed and low
frequency current and voltage signals have been extracted by means of first order
low pass filters (cutoff frequency = 10 kHz). The simulator was LTSpice 4.16
(freely distributed by Linear Technology Corp.) and the SPICE model provided by
RHOM Semiconductor for its Schottky diode RB521ZS-30 was employed.

Fig. 3 SPICE simulation results for the circuit in Fig. 2

The simulation shows that a low frequency voltage signal is generated across the
implant electrodes which is associated with a low frequency current through the
implant (and through the tissue in between the two implant electrodes.) The peak
value of the low frequency current transient is about 8 mA and its pulse duration is
about 0.15 ms (50% peak crossings) which appears sufficient for electrical
stimulation of nerves [12]. Furthermore, note that higher generator voltage
amplitudes would be tolerated both by the circuit (the maximum voltage reached at
the capacitor is 2.6 V) and by the human body according to safety standards [4],
452 A. Ivorra and L. Becerra-Fajardo

hence even larger currents would be possible. However, the most important piece
of information from this simulation is that the average of the current is null which
indicates that it is charge balanced.

2.3 In Vitro Demonstration of Charge Balance and Non-critical


Hermeticity
The setup illustrated in Fig. 4 was built in order to demonstrate that the proposed
circuit performs charge balance and that it will prevent electrochemical damage.
The behavior of the proposed architecture (mounted on a PCB) was compared to
that of a system consisting of just a diode. Each system was connected to two
platinum-iridium wires (76700, A-M Systems, Sequim, WA, USA) which were
inserted at a distance of 3 cm (and a depth of about 5 mm) in a 2.5 cm diameter
agar cylinder made from a 0.9% NaCl solution. Two aluminum band electrodes
were placed on the agar cylinder at a distance of 10 cm and were energized by a
30 V peak sinusoidal signal delivered as 1 ms bursts at a rate of 50 bursts per
second. The signal was generated by a function generator (AFG 3022B by
Tektronix) followed by a high voltage amplifier (WMA-300 by Falco Systems BV,
Amsterdam, The Netherlands).
Low frequency currents through the circuits were obtained by capturing, with a
battery powered oscilloscope (TPS2014 by Tektronix), the voltage drop across the
parallel combination of a 10 Ω resistor and 1 μF capacitor (RC low pass filter,
cutoff frequency =16 kHz). As it can be observed in Fig. 4, the proposed circuit
performs charge balance whereas the diode does not.

Fig. 4 Setup for charge balance demonstration. The proposed circuit is compared to a
circuit consisting of just a diode. (References for the components are noted in section 3.1).
Flexible Thread-like Electrical Stimulation Implants 453

The high voltage signal was applied for four hours and, after this lapse of time, it
was clear the presence of entrapped gas bubbles around the Pt-Ir electrodes
connected to the diode whereas no bubbles (or any sort of corrosion indication)
were observable on the Pt-Ir electrodes connected to the proposed circuit.
Therefore, this experiment confirms that no irreversible electrochemical reactions
occur with the proposed circuit (or that they occur at an imperceptible rate
compared to that of those that occur with a diode.)
The same setup was employed for another experiment: while the high voltage
bursts were being delivered, the proposed circuit was immersed in distilled water
and no modification of current waveforms was observable. This result is relevant
because it shows that the circuit may be able to operate inside packages which are
not hermetic to water in contrast to the case of inductively powered micro-
stimulators whose resonant frequency strongly depends on the presence of water
[13]. It remains to be tested the long-term tolerance to water.

3 Implemented Prototypes
3.1 Physical Implementation
The prototype displayed in Fig. 5 was implemented as follows: two SMD
capacitors with a measured capacitance of 1.2 μF (02016D225MAT2A by AVX
and acquired from Mouser Electronics; supposedly 2.2 μF capacitors), a SMD
Schottky diode (RB521ZS-30 by RHOM Semiconductor) and a SMD 1 kΩ resistor
(ERJ-XGNJ102Y by Panasonic) were positioned as indicated in Fig. 6 and soldered
thus forming the proposed circuit. Two ~2.5 cm long Pt-Ir springs were soldered to
the circuit; one to each terminal. (These springs were made by coiling 41 AWG Pt-
Ir wire (76700 by A-M Systems) around a 30-gauge needle.) The assembly was
gently introduced in a 3 cm long biomedical silicone tube with an outside diameter
of 0.94 mm (806400 by A-M Systems). The tube was filled with a biocompatible
silicone (MED-6015 by NuSil Technology, Carpinteria, CA, USA) which has a low
viscosity when uncured. After curing, the Pt-Ir wire exiting the tube was bent
inwards on the tube and another Pt-Ir spring (made with 19-gauge needle) was
positioned over it to form an electrode of approximately 4 mm (one at each
extreme). Finally, a few drops of silicone were added and cured for securing the
electrodes.
As illustrated in Fig. 5 the prototype is highly flexible (bend radius <5 mm). In
addition, it can be reversibly stretched for small elongations (1 or 2 mm; ~ 5%). It
also survives much larger elongations (50%) but does not recover its length.

3.2 In Vitro Demonstration


The prototype was tested in the setup displayed in Fig. 4. In this case, however,
the device was implanted within the agar cylinder and low frequency voltage
across electrodes was captured by means of two thin wires (Fig. 7). Neither
bubbles nor any sort of corrosion were observable after four hours of continuous
operation.
454 A. Ivorra and L. Becerra-Fajardo

Fig. 5 Implemented prototype. The electronic components and the two connections to the
electrodes are contained within a silicone body. Both the connections and the electrodes
consist of coiled Pt-Ir wires.

Fig. 6 Electronic component placing (and the circuit formed after soldering). Two
capacitors are employed in order to double the voltage tolerance (6.3 V + 6.3 V) and for
geometrical symmetry.

Fig. 7 (a) Voltage recorded across the prototype’s electrodes and its comparison to
simulated voltage. (b) Simulated current for this scenario.
Flexible Thread-like Electrical Stimulation Implants 455

4 Inmediate Future Directions

We plan to in vivo test these implants during the next months for demonstrating
stimulation capabilities and minimal invasiveness. In particular, we are applying
for permission from the ethical committee of animal experimentation at our
institution for a study with rabbits.

Acknowledgment. AI’s research is supported by a Ramón y Cajal fellowship from the


Spanish government and a Marie Curie grant (IRG 256376) from the European
Commission. LB’s research is supported by a scholarship from the UPF.

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High-Frequency Oscillations in Chemically
Induced Spike-and-Wave Epileptic Seizures

Jianhang Jiao, Cristian Sevcencu, Kristian Rauhe Harreby, and Winnie Jensen

Department of Health Science and Technology, Aalborg University, Denmark


{jj,sevcr,krauhe,wj}@hst.aau.dk

Abstract. High-frequency oscillations (HFO, 100–600 Hz) are thought to play an


important role in epileptogenesis and development of seizures. HFO are
subclassified in ripples (R, 100–200 Hz) and fast ripples (FR, 200–600 Hz), but it is
unclear if both subclasses can be related to epilepsy. In this study, we have
investigated R and FR activity in normal conditions and during spike-and-wave
(SW) epilepsy seizures induced by pentylenetetrazole (PTZ) administration in three
Sprague-Dawley rats. Electrocorticogram (ECoG) and intracortical (IC) field
potentials were recorded from the right somatosensory hindlimb area. The power
spectral density (PSD) and the mean power (MP) of the IC signals in the HFO
frequency range were calculated during periods of normal brain activity (i.e.
baseline) and during the induced SW activity. The results showed that the MP of FR
increased by 184 % during SW compared to baseline whereas the MP of R did not
change significantly. These results suggest that FR are related to seizure activity
and therefore can be used as biomarkers for seizures.

1 Introduction

Epilepsy is a common neurological disorder which affects around 50 million people


worldwide [1]. In spite of treatment with e.g. antiepileptic medication or surgical
resection of the epileptic focus, the seizures remain poorly controlled in more than
30 % of epilepsy patients [2]. Future advances in diagnosis and treatment of
epileptic seizures are believed to depend on a better understanding of the underlying
mechanisms of epilepsy.
High-frequency oscillations (HFO, 100 – 600 Hz) such as ripples (R,
100–200 Hz) and fast ripples (FR, 200–600 Hz) have been extensively explored in
rodents [3] and humans [4] and associated with brain activity in both physiological
and pathological processes [5]. Earlier studies concluded that R play a significant
role in memory functions [6] and that FR may be a specific biomarker for epileptic
tissues [7]. Furthermore, FR were believed to play an important role in
understanding the mechanisms of epileptogenesis. However, later studies reported
that the FR were found in physiological cortical potentials [8], [9], whereas R
increased in epileptogenic foci of epilepsy patients [10]. Therefore, the distinction
between what is normal and abnormal HFO is still unclear [11].

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 457
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_68, © Springer International Publishing Switzerland 2014
458 J. Jiao et al.

In this study, our objective was to investigate the R and FR activity during normal
conditions and chemically induced spike-and-wave (SW) epileptic seizures.

2 Method
Three male Sprague Dawley rats (250–350 g, 2–3 months) were included in this
study. The rats were housed in plexiglas cages with free access to food and water
and were kept at a 12-12 h light-dark cycle. At the end of the experiments, the rats
were sacrificed by an overdose of anesthesia. All experimental procedures were
approved by the Danish Animal Welfare Committee.

2.1 Surgery
The animals were anesthetized using a ketamine/xylazine (90/10 mg/kg) mixture.
The rectal temperature was monitored and maintained within 37.5 ± 1 °C using an
ATC1000 Animal Temperature Controller (WPI, USA).
The rats were placed in a stereotaxic frame and their skull was exposed through a
midline incision. A hole was drilled 2.3 mm posterior and 2.6 mm lateral (right) to
the bregma and further extended using a rongeur. After removal of the dura in the
range of the bone window, a set of electrodes was placed in the hole to record the
electrocorticogram (ECoG) and intracortical (IC) field potentials. This set of
electrodes consisted of an ECoG electrode made from a hollow stainless steel rod
(1.3 mm and 0.8 mm outer and inner diameters, respectively) and an IC electrode
made from a Teflon-coated tungsten wire (50 µm bare and 100 µm coated in
diameter, PFA-Coated Tungsten, A-M systems, USA). The IC electrode was placed
in the hollow ECoG electrode with 0.8 mm vertical tip separation and fixed together
by dental cement. Using the micromanipulator, this set of electrodes was advanced
in the cranial hole so that the outer ECoG electrode was in contact with, and the inner
IC electrode penetrated 0.8 mm in the cortex. The location of the electrodes
corresponded to the right hindlimb region of the primary somatosensory cortex [12].
A cranial stainless steel screw was used as reference electrode and placed 1 mm
lateral (left) and 6 mm anterior to the bregma.

2.2 Data-Acquisition and Experimental Procedures


The signals were amplified (ECoG = 1000, and IC = 5000) and band-pass filtered
(ECoG = 1–4000 Hz and IC = 100–4000 Hz) using differential amplifiers
(AI 402 x50 & CyberAmp 380, Axon Instruments, USA) and sampled at 10 kHz
(Data Acquisition Board PCI 6251, National Instrument, USA). The animals were
allowed to stabilize for 10 min following the surgery before beginning to record the
signals. After a 5 min baseline recording, SW discharges were induced by 150 s
IV infusion of an initial dose of 10 mg/kg/min PTZ and maintained for 300 s by a
continuous infusion of 0.2 mg/kg/min PTZ. The first minute of baseline recording
and the last minute of SW activity recording were extracted and used for data
analysis.
High-Frequency Oscillations 459

2.3 Data Analysis


To evaluate the distribution of different frequencies, the power spectral density
(PSD) was derived from the IC signals using the Welch spectrum function in Matlab
(Hamming window = 4000) after a 50 Hz notch filter. To quantify the magnitude of
R and FR in baseline vs. SW activity, the IC recordings were further filtered during
offline analysis using Matlab (Butterworth filter, R = 100–200 Hz and
FR = 200–600 Hz) and the mean power (MP, i.e. an average of the squared IC data)
was calculated in the range of R and FR, and expressed as mean values ± SD. Due to
the limited number of animals included so far, no further statistical analysis was
performed.

3 Results

3.1 Baseline Recording


In baseline conditions (i.e. prior to PTZ administration), up to 4 Hz delta wave
activity was observed in ECoG with no clear link with R activity, but associated with
moderate FR activity (Fig. 1).

3.2 SW Activity Recording


PTZ infusion induced stable 2 Hz SW discharges in the ECoG (Fig. 2). Those SW
discharges were associated with increased FR activity synchronous with the spike
component and moderate FR activity synchronous with the wave component.
Neither of those SW components was clearly correlated with R activity (Fig. 2).

3.3 PSD Analysis


R: In the R range of frequency (100–200 Hz), a peak at around 130 Hz was observed
in the power distribution of baseline activity. Compared to baseline, a generally
lower level of power was evidenced during SW activity (Fig. 3).
FR: In the FR range of frequency (200–600 Hz), the power distribution of baseline
activity decreased gradually towards the end of this range. Compared to baseline, a
significantly higher level of power was evidenced during SW activity with a
maximum centered on 440 Hz (Fig. 3).
In addition to the investigated HFO components, a peak increase of the power
distribution centered on 60 Hz was observed in the gamma range of frequency
(40–80 Hz) of baseline activity. Compared to baseline, the power of gamma activity
decreased significantly during SW activity (Fig. 3).
460 J. Jiao et al.

0.5 mV
ECoG

delta wave

0.2 mV
IC
0.1 s

0.04 mV
Ripples

0.04 mV
Fast Ripples

Fig. 1 An example of baseline recording of ECoG, IC and the R and FR extracted from the
latter

spike wave

0.5 mV
ECoG

0.1 s
SW discharge

0.2 mV
IC

0.04 mV
Ripples 0.04 mV

Fast Ripples

Fig. 2 An example of SW recording of ECoG, IC and the R and FR extracted from the latter.
Note the synchronization between FR and the ECoG and IC spikes discharges

3.4 MP Analysis
R: In the R frequency range, the MP of the baseline activity (55.3 ± 7.1 μV2) was
similar to that of the SW activity (57.5 ± 32.8 μV2) (Fig. 4).
FR: In contrast to R, the MP of FR increased by 184% during SW activity
(50.2 ± 36.1 μV2) compared with baseline (18 ± 9 μV2) (Fig. 4).
High-Frequency Oscillations 461

Power Spectral Density


-40
Baseline
-45
SW
Power / frquency (dB/Hz) -50

-55

Gamma
-60

-65

-70

-75
Ripples FR
-80
0 100 200 300 400 500 600
Frequency (Hz)

Fig. 3 Power spectral density (PSD) of the IC signal averaged across the investigated rats

Mean power
100
Baseline
90
80
SW
IC Power (μV2)

70
60
50
40
30
20
10
0
Ripples Fast-Rapples

Fig. 4 Mean power analysis based on IC recordings from 3 rats (mean ± SD)

4 Discussion
In this study, we compared the presence and magnitude of R and FR in HFO
recorded from the somatosensory cortex of rats during baseline and SW discharges
indicative of absence epilepsy seizures [13]. Our results indicate that R are equally
associated with normal brain activity and SW seizures, whereas FR are stronger
during SW seizures.
462 J. Jiao et al.

Previous studies have shown that FR may play an important role in the
mechanisms of epileptogenesis. Thus, Bragin et al. reported that FR have more
potential to characterize epileptogenic areas than R in epilepsy patients and
hypothesized that the occurrence of HFO reflects fields of hypersynchronized action
potentials [14]. Our results are in line with those of Bragin et al. and indicate that this
hypersynchronization is best illustrated in the frequency range of FR rather than in
the whole band of HFO. In addition, our results suggest that a normal
synchronization of the cortical neurons results in moderate FR activity generating
delta waves in the ECoG whereas the increased FR activity observed during seizure
reflects episodes of hypersynchronization which generate the spike components of
the SW discharges (Fig. 2). Therefore, we consider that increased FR activity
represents a marker of SW seizures.
Normal R activity was thought to reflect summated synchronous inhibitory
postsynaptic potentials from a group of principal cells [15]. The degree of
synchronization during R is well controlled and never reaches a level where
discharging neurons lose their identity and form pathological spike discharges [11].
In our recordings, more R-type activity could be observed during baseline (Fig. 1)
than during SW discharges (Fig. 2) and the R-type activity was not associated with
spike discharges in ECoG (Fig. 2). This is consistent with the previously mentioned
view of controlled synchronization during R-type activity and the physiological
nature of R.
In this study, we have also noticed intensified gamma activity (40–80 Hz) during
baseline conditions (Fig. 3). Whereas physiological intensified gamma oscillations
are linked with cortical processing during vision, motor and language functions [16],
abnormal gamma band oscillations serve as a prominent marker of schizophrenia
[17] and subanesthetic administration of ketamine is used as a “gold-standard”
method for modeling this disease [18]. As in the present experiments we have used
ketamine as an anesthetic, this may explain the occurrence of a gamma peak in
baseline conditions. Since that gamma activity was apparently attenuated after PTZ
administration (Fig. 3), this may suggest that the gamma rhythms may be inhibited
by either this drug, or by the induced SW seizures.

5 Conclusion

In this study we investigated if FR and R are related to normal cortical activity or SW


seizures. Although the data available at this moment are limited and cannot support a
definitive conclusion, our results indicate that FR are more related to SW seizures
and R are more related to normal cortical activity. To better understand the
underlying mechanisms of epilepsy and epileptic seizures, further work should be
performed to explore the HFO activity not only during SW seizures, but also during
more severe tonic-clonic seizures and thus to investigate if the FR activity is
correlated with the severity of seizures.
High-Frequency Oscillations 463

References
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(2012)
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of epilepsy. Neurosurg. Focus 32(3), E13 (2012)
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oscillations and epileptogenesis in temporal lobe epilepsy. Neurobiol. Dis. 42(3),
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Oscillations in Focal Human Epilepsy. J. Neurophysiol. 55905, 1958–1964 (2013)
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with spike burst patterns detected in cortical neurons, pp. 2951–2959 (2011)
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markers for cortical spike bursts. J. Physiol. 550(Pt. 2), 529–534 (2003)
[10] Worrell, G.A., Gardner, A.B., Stead, S.M., Hu, S., Goerss, S., Cascino, G.J., Meyer,
F.B., Marsh, R., Litt, B.: High-frequency oscillations in human temporal lobe:
simultaneous microwire and clinical macroelectrode recordings. Brain 131(Pt. 4),
928–937 (2008)
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Diego (2007)
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Pathophysiological mechanisms of genetic absence epilepsy in the rat. Prog.
Neurobiol. 55(1), 27–57 (1998)
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epileptic brain. J. Neurosci. 22(5), 2012–2021 (2002)
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and low. Int. J. Psychophysiol. 79(1), 9–15 (2011)
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schizophrenia in humans and animals based on inhibition of NMDA receptors.
Neurosci. Biobehav. Rev. 32(5), 1014–1023 (2008)
Detection of Movement Intentions through a
Single Channel of Electroencephalography

Mads Jochumsen1, Imran Khan Niazi1,3, Helene Rovsing1, Cecilie Rovsing1,


Gebbie A.R. Nielsen1, Tina K. Andersen1, Nhung P.T. Dong1,
Marina E. Sørensen1, Natalie Mrachacz-Kersting1, Ning Jiang2,
Dario Farina2, and Kim Dremstrup1
1
Department of Health Science and Technology at Aalborg University,
9220 Aalborg Ø, Denmark
{mj,imrankn,nm,kdn}@hst.aau.dk,
{hrch12,crch12,gniels12,tiande12,
ndong12,meso11}@student.aau.dk
2
Department of Neurorehabilitation Engineering,
Bernstein Focus Neurotechnology Göttingen,
Bernstein Center for Computational Neuroscience,
University Medical Center Göttingen,
Georg-August University, Göttingen, Germany
{dario.farina,ning.jiang}@bccn.uni-goettingen.de
3
New Zealand College of Chiropractic,
Auckland, New Zealand

Abstract. In this study, the aim was to estimate the performance of a brain-
computer interface (BCI) system by detecting movement intentions using only a
single monopolar channel of electroencephalography (EEG). Seven healthy
subjects performed four types of cued palmar grasps with two levels of force and
speed. The movement intentions were detected using a technique where a template
of the initial negative phase of the movement-related cortical potential (movement
intention) was matched with the continuous EEG. On average 78 % of the
movements were detected (true positive rate) ~150 milliseconds before the task
onset. The number of false positive detections was 1.5 per minute. The estimated
system performance, using only a single monopolar channel, indicates that the
proposed setup can be used for neuromodulation paradigms in BCI where the
movement intention is paired with somatosensory feedback from e.g. functional
electrical stimulation or robot-assisted movements.

1 Introduction

Over the past years the interest of applying Brain-Computer Interface (BCI)
technology in stroke rehabilitation has expanded [1]. When using a BCI, motor
impaired patients can actively initiate an external device such as a rehabilitation

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 465
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_69, © Springer International Publishing Switzerland 2014
466 M. Jochumsen et al.

robot or functional electrical stimulation (FES) through their brain activity [2]. If
afferent feedback from one of these external devices is timed to arrive at the
cortical level when the user is intending to activate this (through motor imagery),
long-term potentiation-like plasticity can be induced [3]. These plastic changes
may be positively correlated to learning or relearning of motor tasks [4].
To time the arrival of somatosensory feedback at the cortical level according to
the findings by Mrachacz-Kersting et al. (2012), the movement intention must be
detected with a short latency with respect to the task onset since the afferent volley
needs time to reach the cortical level; this is in the range of 25 to 50 milliseconds
for the upper and lower limbs, respectively [5, 6]. In several studies, detection of
movement intent was combined with appropriately timed somatosensory feedback
using either electrical stimulation of the relevant nerve or passive movement of the
involved limb [7, 8].
The movement intention is encoded in the initial negative phase of the
movement-related cortical potential (MRCP) that is a brain potential associated
with the execution of a movement or imagination of a motor task [9-11]. The
potential is seen as a depression in the continuous electroencephalography (EEG)
preceding up to two seconds before the actual movement onset. The negative
amplitude is characterized by a steeper slope in the last 300 to 400 milliseconds
prior the onset of the executed or imaginary movement, and reaches its peak of
maximum negativity close to the movement onset [12]. The MRCP can be
recorded using two different paradigms: cue-based and self-paced. The potential
associated with cue-based protocols is known as the contingent negative variation
(CNV) [10], and the potential associated with the self-paced protocol is known as
the Bereitschaftspotential (BP) [9]. The two potentials share similar neural
generators, but they differ in the contribution from the dorsal premotor cortex and
supplementary motor cortex [13]. Also, a slight difference has been reported in the
morphology of the signals, where an earlier negative depression was observed in
the EEG for cue-based movement compared to self-paced movements [14].
Despite the differences between the two potentials, both of them represent a
movement preparation or intention.
The intention of self-paced and cue-based movements can be detected through
EEG recordings with latencies in the range of -500 to 300 milliseconds with
respect to the movement onset, which is important for inducing plastic changes
[15-18]. In these studies the lowest number of channels that have been applied is
nine. Using this number of channels still makes it possible to apply different
techniques such as spatial filters to improve the signal-to-noise ratio.
The aim of this study was to detect movement intentions using only a single
channel of EEG for executed palmar grasps using the methodology proposed in
Jochumsen et al. (2013). The results may estimate the system performance of a
BCI that can be used for neuromodultion.
Detection of Movement Intentions through a Single Channel 467

2 Methods

2.1 Subjects
Seven healthy subjects without any prior BCI experience participated in this study
(five women and two men: 28±10 years old). All subjects gave their informed
consent, and the procedures were approved by the local ethical committee (N-
20130081).

2.2 Experimental Protocol


The subjects were seated in a chair, in an electrically shielded room, with their right
arm and hand resting on a table. At the beginning of the experiment their maximum
voluntary contraction (MVC) of a palmar grasp was recorded using a Jamar
compatible handgrip dynamometer (Noraxon USA, Inc., Scottsdale, Arizona)
which was used throughout the entire experiment. They were instructed to perform
four types of cued isometric palmar grasps where each task was repeated 40 times
with 10 seconds of rest between each repetition. The tasks were: (i) 0.5 s to reach
20% MVC, (ii) 0.5 s to reach 60% MVC, (iii) 3 s to reach 20% MVC and (iv) 3 s to
reach 60% MVC.
The subjects were restricted to spend the given time to reach the desired level of
MVC by producing force to match a ramp-force template as described in
Jochumsen et al. (2013). They were cued by a computer program (Knud Larsen,
SMI, Aalborg University) where the force from the dynamometer was used as
input, and visual feedback was provided during the experiment. The subjects were
seated 1.5 meters from the screen and asked to focus their gaze on the center of the
screen to minimize eye movement artifacts.
The movements were performed in blocks which were randomized for each
subject. Before each block, the subjects spend ~5 minutes familiarizing to the task.

2.3 Signal Acquisition


One channel of monopolar EEG (EEG amplifiers, Nuamps Express, Neuroscan)
was recorded continuously from a Ag/AgCl ring electrode with a sampling
frequency of 500 Hz and digitized with 32 bits accuracy. The electrode was located
at C3 according to the International 10-20 system. The signals were referenced to
the right earlobe and grounded at nasion. Electrooculography (EOG) was recorded
above the left eye. The impedance of the electrodes was below 5 kΩ throughout the
experiment.

2.4 Movement Detection


The EEG signal was digitally bandpass filtered in the range 0.05-10 Hz with a 2nd
order Butterworth filter.
468 M. Jochumsen et al.

The movements were detected from the continuous recordings using a template
matching approach that is similar to the one that was proposed by Niazi et al.
(2011) and used by Jochumsen et al. (2013).
The continuous recordings for the four tasks (see Fig. 1) were randomly divided
into four data sets, three for training and one for testing (4-fold cross-validation).
From the training data a template was extracted when averaging the movements
from the task onset to two seconds prior to this point. The detection threshold was
selected using a receiver operating characteristics (ROC) curve which was obtained
through cross-validation on the training data. The threshold was selected at the
upward convex part of the ROC curve corresponding to a tradeoff between
the number of false positive detections (FPs) and the true positive rate (TPR). The
likelihood ratio was (Neyman Pearson lemma) computed between the EEG
recordings in the testing set and the template (the template was shifted with 200
milliseconds). When two out of three consecutive ratios were above the detection
threshold and below the EOG threshold (125 µV) the detection was registered.
The performance of the detector was evaluated through the TPR (%), the
number of FPs per minute and the detection latency (the time between the point of
detection and the task onset).

Fig. 1 Averaged MRCPs across subjects for each movement type (ME: motor execution).
‘Fast’ indicates 0.5 seconds to reach the desired level of MVC, and ‘Slow’ indicates 3
seconds to reach that level. ‘n’ is the number of trials that was used to make the average.

3 Results
The detection performance is shown in table 1 where the averaged TPR (across
subjects) is presented for each task. 76-83 % of the movements were detected with
an average detection latency of -152±72 milliseconds (mean ± standard deviation
(SD)). The number of FPs per minute was on average 1.5±0.7 for the four task. Six
movements were performed per minute, and the duration of the experiment was on
average 30±1 minutes. The highest TPR was obtained for the slow movements
(83±8 %) performed at 20 % MVC.
Detection of Movement Intentions through a Single Channel 469

Table 1 Movement detection

Movement detection
Task TPR

Fast 20 % MVC 76±8


Fast 60 % MVC 77±10
Slow 20 % MVC 83±8
Slow 60 % MVC 77±7
Mean±
The averaged TPR (%) is shown for each task. The movements were detected ~150 milliseconds
before the task onset with 1.5 FPs/minute.

4 Discussion

Four types of palmar grasps were detected from the continuous EEG recordings
approximately 150 milliseconds before the task onset with an averaged TPR of 78
% and 1.5 FPs/min. A single channel was used to test the feasibility of a fast BCI
setup that may be applicable in neurorehabilitation.

4.1 Detection Performance


The performance of the detector was slightly lower compared to what has been
found in previous studies where a similar methodology has been applied for
movement detection of the lower extremities even though only a single channel has
been used [15, 17]. This may be explained by the cortical representation of the
hand which is closer to the recording site compared to that of the lower extremities
leading to a greater signal-to-noise ratio. It is a bit surprising that the highest TPR
was obtained for slow movements performed at 20 % MVC since it was this
movement type that showed the lowest TPR for dorsiflexions of the ankle joint
[17]. Also, the signal-to-noise ratio of the slow movement type was lower
compared to that of fast movements (see Fig. 1). This picture could be a bit
misleading due to a low number of subjects (n=7).
Even though the performance is relatively high, it may be further improved by
looking into different signal processing techniques that can enhance the signal-to-
noise ratio and feature extraction techniques to improve the discrimination between
movement intentions and noise. Different techniques have been outlined for
movement detection (using the MRCP) such as: blind source separation [19],
locality preserving projection [18], principal component analysis [20], power
spectral density estimation [21] and a comparison of several processing techniques
have been performed for classification of movement intentions [22]. A common
processing technique utilized in these studies, to correct for the blurring of the
electrical activity due to volume conduction and improve the signal-to-noise ratio,
470 M. Jochumsen et al.

is spatial filtering [23]. It should be investigated in a future study how the detection
performance is affected using only one channel compared to e.g. spatial filtered
data from nine channels.
The results obtained with a single channel could indicate that a fast setup of a
BCI for use in e.g. a clinical setting is possible. The detection performance, when
varying the levels of force and speed, is similar suggesting that a task specific
template may not be needed to obtain good performance even though the
movements are performed in different ways (see also Fig. 1) [17]. This is in line
with a previous study where the training time to individualize the detector to each
user has been eliminated by using a global subject independent detector [24].

4.2 Detection Performance Needed to Induce Plasticity


The estimated detection performance reached 76-83 % correctly detected
movements. This performance may be good enough for inducing plasticity when it
is combined with electrical stimulation since it is in the range of what has been
reported in other studies [7, 25]. In one of those, it was also found that the system
performance was positively correlated with the change in excitability of the
cortical projections to the target muscle [7]. However, the lowest limit of system
performance needed to induce plasticity is not known [1].

4.3 Limitations
The subjects in this study were healthy volunteers, on the contrary to the intended
user group which consists of stroke patients suffering from motor impairments.
The detection performance has not been thoroughly investigated in this patient
population, and it is a question that should be addressed in future studies. The
number of subjects was rather low; however, it seems feasible to use only one
channel to control a BCI for inducing plasticity. The data was analyzed offline;
this should be translated into an online system and tested in a future study. It is
feasible that a single channel EEG can be used in an online BCI since the same
detection technique for nine channels has been implemented and tested online [7].

5 Conclusion

The findings of this study showed it may be possible to detect the movement
intention of palmar grasps. This can be used as a control signal for assistive
devices in patient-driven neurorehabilitation where artificially produced
movements should be timely correlated to the intention of the user.

Acknowledgment. This work was supported by the Danish Technical Research Council.
Detection of Movement Intentions through a Single Channel 471

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A Standard Low-Cost Worldwide Accessible
Nintendo Wii Balance Test Can Differentiate
Older Fallers from Non-fallers

Martin G. Jorgensen1, Nicolas B. Hansen2,


Alberto L.R. Perez3, and Erika Geraldina Spaich4
1
Aalborg University Hospital, Aalborg, Denmark
mgj@rn.dk
2
Aalborg University, Aalborg, Denmark
3
Bispebjerg Hospital, Copenhagen, Denmark
alberto.luis.rodriguez.perez.01@regionh.dk
4
Center for Sensory-Motor Interaction, Aalborg University, Denmark
espaich@hst.aau.dk

Abstract. The purpose of this study was to explore if the Nintendo Wii Stillness
test could differentiate between age and gender matched fallers and non-fallers. 20
older fallers and 23 older non-fallers performed three trials of the Stillness balance
test. Results showed a ~23% difference in the scores of the two groups (p=0.007).
The Stillness test therefore appears to be able to differentiate age- and gender
matched fallers and non-fallers. In addition, the test is low-cost, time-efficient, and
widely available across the world and could therefore become a good alternative
to existing tools/scales for assessment of standing balance.

1 Introduction

Fall accidents within the older population are a major concern worldwide, as they
are associated with elevated morbidity, mortality, poorer overall functioning, and
early admission to long-term care facilities [1]–[3]. In Denmark a growth of
approximately 80% is expected in older adults (+65 years) through the next 30
years [4]. A similar growth is projected in USA as the population of older adults is
estimated to go from 45.1 million in 2014 to 92.0 million in 2060 [5]. More than
400 risk factors for falls have been identified [2], [6], and impaired balance
control is one of the most important factors.
A common way of measuring balance performance in older adults is through
objective force plate- or gait analysis. However, objective balance tools such as
these are expensive and technically difficult to operate in a clinical environment.
Thus, a need exists to find or develop low-cost, objective, quantitative balance
assessment tools directed towards a clinical setting.
In 2008, Nintendo Corporation (Kyoto, Japan) launched the Nintendo Wii
Balance Board (NWBB) primarily intended as a toy for kids. However, not long

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 473
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_70, © Springer International Publishing Switzerland 2014
474 M.G. Jorgensen et al.

after the launch, researchers worldwide started exploring the NWBB for additional
purposes than solely entertainment, and found that the NWBB could be used as a
training device [7]–[9], a physical examination tool [10], [11] and a prediction
tool [12]. A recent study reported that the Nintendo Wii Stillness test was highly
reproducible in community-dwelling older adults when assessing standing balance
[10]. However, the study did not explore the ability of the Stillness test to
discriminate between different populations (i.e. fallers vs. non-fallers). The
purpose of this study was therefore to explore if the Wii Stillness test could
discriminate between fallers and non-fallers.

2 Methods

2.1 Participants
This case-control study compared 20 older adults with a history of fall accidents
within the last 12 months with 23 age and gender matched older adults with no
history of falls (Tab.1). The recruitment of fallers took place between May 2013
and July 2013 at the geriatric fall clinic of Bispebjerg Hospital, Copenhagen,
Denmark and the non-fallers were recruited at senior society organizations in
Copenhagen, Denmark. Participants in both groups had to be at least 65 years or
older and with a minimum score of 27 in the mini-mental state examination,
ability to ambulate independently with or without use of a cane, and with no
severe hearing and vision impairments. In this study, a fall was defined as “an
unexpected event in which the participant came to rest on the ground, floor, or
lower level“ [13].

Table 1 Characteristics of the participants

Characteristics All Fallers Non-fallers


(n=43) (n=20) (n=23)

Age (yr.) 74.2±6.1 75.9±6.5 72.8±5.5


Weight (kg) 69.5±14.7 69.7±13.7 69.3±15.8
Height (cm) 167.4±8.0 165.1±6.5 169.4±8.8
Women (men) 33 (10) 16 (4) 17 (6)

2.2 Design
The study was a case-control study with age and gender matched cases and controls
(Fig. 1). To ensure transparency the study followed the STROBE statement
‘STrengthening the Reporting of OBservational studies in Epidemiology’ [14]. In
addition, the study was conducted according to the Declaration of Helsinki and all
participants gave their written informed consent prior to enrollment. Finally, the
local ethics committee of the North Denmark Region and the Danish Data Agency
approved the study.
A Standard Low-Cost Worldwide Accessible Nintendo Wii Balance Test 475

Fig. 1 Illustration of the design of the study

2.3 Wii Stillness Protocol


The Stillness test is a 30-second bilateral undisturbed balance test and is most
likely an approximation of the movement of the Centre of Pressure (COP) in the
anterior-posterior and medial-lateral plane. The outcome from the test is a stability
score (between 0 and 100%) where a higher degree of stability or steadiness is
given as a high percentage and vice versa (Fig. 2). The original Stillness test was
intended to have people look at a TV with visual feedback from a red dot, which
indicates movements in the anterior-posterior and medial-lateral plane. However,
in this study, to avoid a learning effect the TV was turned off, participants did not
receive visual feedback, and instead were instructed to focus on a visual focal
point positioned in eye height on a wall three meters away [10]. In addition,
participants were asked to remain as still as possible in a barefooted-bilateral (hip-
width) standing position with arms hanging relaxed at both sides. Participants
performed three successive trials of the Stillness test, separated by 30 seconds of
rest between trials as this previously has been shown to be highly reproducible in
older adults[10].

Fig. 2 Screenshoot of the Stillness test with outcome score in percent

2.4 Statistical Analysis


Statistical analysis was performed using SPSS (version 20, IBM, New York,
USA). The Shapiro-Wilk test was used to evaluate normality of distributions in
the Stillness test for the two groups. Differences in characteristics and Stillness
scores between fallers and non-fallers were assessed by an independent t-test
(two-tailed) and Levene´s test was used to assess equality of variances. A p-value
of <0.05 was considered statistically significant.
476 M.G. Jorgensen et al.

3 Results

The mean Stillness score in the Faller group was 46% (95%CI: 37.3% to 54.7%)
while in the non-faller group it was 59.6% (95%CI: 54.1% to 65.0%). The
independent t test revealed a significant difference between the two aged and
gender matched groups (P=0.007). This difference in scores between groups
corresponds to approximately 23% percent (calculated relative to the non-fallers
mean score).

Fig. 3 Mean and SE of the Stillness Score for the faller and non-faller group

4 Discussion

This is the first study to compare age and gender matched fallers and non-fallers
using standard Nintendo Wii software (Stillness test). The results showed that
non-fallers performed significantly better than fallers in the Stillness test.
A recent meta-analysis of the discriminative ability of the Timed Up and Go
test showed an 8.7% relative difference between healthy fallers and non-faller[15].
This discriminative ability is clearly lower when compared to the results of the
present study where a ~23% difference was seen between groups.
Previously we have demonstrated that the Stillness test is a highly reproducible
test of static balance in community-dwelling older adults, and that a strong
correlation was seen between the COP ellipse (mm2) recorded on a force plate and
the Stillness test [10]. In addition, the test is low-cost as the whole system can be
purchased for ~100 euro compared to the average price of a force plate (~8000
euro). Also, the Stillness test is widely available across the world and many
physiotherapy clinics already have invested in a complete Nintendo Wii system.
We therefore believe that the Stillness test could potential serve as a good
A Standard Low-Cost Worldwide Accessible Nintendo Wii Balance Test 477

alternative to existing tools/scales for assessment of standing balance and predict


falls. However, for the Stillness test to be adapted into clinical practice with the
purpose of predicting fall accidents, future prospective cohort studies should
explore sensitivity and specificity of the test.

5 Conclusion

The Study showed that the Stillness test can differentiate between age- and gender
matched fallers and non-fallers. Moreover, the test is low-cost, time-efficient, and
easily accessible around the world and could therefore become a good alternative
to existing tools/scales for assessment of standing balance.

Acknowledgment. We would like thank Lone Schaadt, Physiotherapist at department of


geriatrics Bispebjerg Hospital, Copenhagen, Denmark for helping recruit the fall patients
for the study.

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in Community-Dwelling Older Adults: A Randomized Controlled Trial. J. Gerontol.
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Home-based balance training using the Wii balance board: a randomized, crossover
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[9] Agmon, M., Perry, C.K., Phelan, E., Demiris, G., Nguyen, H.Q.: A pilot study of Wii
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[10] Jørgensen, M.G., Laessoe, U., Hendriksen, C., Nielsen, B.F., Aagaard, P.: Intra-Rater
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478 M.G. Jorgensen et al.

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Preliminary Validity of Game-Based Fall Risk Assessment in Community-Dwelling
Older &nbsp Adults. Geriatr. Nurs. 32(3), 188–194 (2011)
[13] Gillespie, L., Mc, R., Wj, G., Sherrington, C., Gates, S., Lm, C., Se, L.: Interventions
for preventing falls in older people living in the community (Review) (11) (2012)
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J.P.: The Strengthening the Reporting of Observational Studies in Epidemiology
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[15] Schoene, D., Wu, S.M.-S., Mikolaizak, A.S., Menant, J.C., Smith, S.T., Delbaere, K.,
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Geriatr. Soc. 61(2), 202–208 (2013)
Reliability of Multiple Baseline Measures
for Locomotor Retraining after Stroke

Taryn Klarner, Trevor S. Barss, Yao Sun, Chelsea Kaupp,


Simone Beattie, and E. Paul Zehr

University of Victoria, Rehabilitation Neuroscience Laboratory, Victoria, BC, Canada


The Centre for Biomedical Research, University of Victoria, Victoria, BC, Canada
and
The International Collaboration on Repair Discoveries,
British Columbia, Canada
pzehr@uvic.ca
www.rehabneurolab.ca

Abstract. The present work investigated the reliability of locomotion-related


physiological measures taken using a repeated test-retest protocol in stroke
participants. Data were collected across 3 testing sessions. Measurements of
muscle activity and force during maximum isometric dorsiflexion, plantarflexion
and hand grip contractions were taken for both the less and more affected limbs.
Cardiovascular measures and stretch reflex amplitudes in soleus muscle were
evaluated at rest. Background EMG activity and amplitudes of cutaneous reflexes
(following stimulation of the superficial peroneal and superficial radial nerves)
were evaluated during walking. Intraclass correlation coefficients (ICC) and
results from repeated measures ANOVA revealed no significant differences across
and between testing sessions and high absolute agreement (ICC = 0.665 to 0.998)
of measures within a participant. Our data support the suggestion that multiple
baseline measures obtained from the same participants should be considered a
valid alternative to the concept of a control group in intervention studies.

1 Introduction

Training and rehabilitative interventions require valid assessment of outcomes that


can be ascribed to the intervention. In turn, the assessment itself must have low
method error and good reliability if it is to be usefully applied. Additionally,
intervention studies have often used reference untrained “control” groups to
compare against the intervention or treatment groups. In clinical studies, this can
mean relegating committed volunteer participants to the role of control
participants. Accordingly, some researchers have instead opted for the “multiple
baseline” model where the participants who will be trained serve as their own
control [1].
The purpose of the present work was to investigate the reliability of multiple
baseline measures using a repeated test protocol in stroke participants. Previous

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 479
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_71, © Springer International Publishing Switzerland 2014
480 T. Klarner et al.

researchers have found high reliability in other baseline measures [1-4] and we
predict high association across test sessions. Results of this study have potential
implications for any future studies evaluating plasticity arising from training or
rehabilitative interventions.

2 Materials and Methods

2.1 Participants
Twelve chronic stroke subjects (at least 6 months post infarct), between 58 and 80
y old, participated with written informed consent in a protocol approved by the
Human Research Ethics Board at the University of Victoria.

2.2 Experimental Protocol


Repeated measurements were obtained from participants in three experimental
sessions over a period of three to four weeks, with at least six days between
sessions. At these sessions, the same tests were performed in the same order and
environmental conditions (i.e. temperature, noise, lighting, subject position) and
session time of day were kept as constant as possible [5,6].
For strength measures, stretch reflex testing, and resting cardiovascular
measures, participants were assessed while seated in a custom-fit chair designed to
minimize movement. Locomotor parameters and cutaneous reflex amplitudes were
evaluated while participants performed level walking on a motorized treadmill belt
with 0% body weight support (Woodway Desmo M, Waukesha, WI, USA).
Electromyographic (EMG) data from the soleus (SOL), tibialis anterior (TA),
flexor carpi radialis (FCR), and posterior deltoid (PD), from the more (MA) and
less (LA) limbs, were collected with surface electrodes placed in bipolar
configuration over the muscle bellies of interest. To control for variation in
positioning of electrodes across days, we used anatomical landmarks,
measurements, and pictures taken at the first session, and the electrodes were
placed by the same experimenter each time.

2.2.1 Recordings of MVIC’s


Maximal voluntary isometric contractions (MVIC’s) were performed for ankle
dorsiflexion, plantarflexion and hand grip for both the LA and MA limbs.
Following a brief warm-up, participants were given two attempts for achieving a
maximum contraction. In 10 second trials, following a silence period of 5 s,
contractions were held for each limb separately. Maximum values were taken as the
greatest reading generated over two trials.
Maximum forces produced during dorsiflexion and plantarflexion contractions
were established via strain gauge (Omegadyne Ltd. Model 101-500) and converted
to torque using a moment arm length of 0.15 m (measured from the heel block to
Reliability of Multiple Baseline Measures for Locomotor Retraining after Stroke 481

the center of the strain gauge). Hand grip was performed with a hand grip
dynamometer (Takei Scientific Instruments Company Ltd., Niigata, Japan). EMG
signals were amplified (GRASS P511, AstroMed) and band pass filtered from 100
to 300 Hz and all signals were sampled at 2000 Hz using custom built continuous
acquisition software (LABVIEW, National Instruments, TX, USA). Using custom-
written software programs (Matlab, The Mathworks, Inc., MA, USA) maximum
contractions were quantified offline by obtaining the mean value over 500 ms when
force and EMG signals were highest. EMG data were rectified and low pass filtered
at 100 Hz using a 4th order Butterworth filter. Values are reported as maximum
torque in Newton-meters (Nm) for ankle dorsi- and plantarflexion, kilograms (kg)
for hand grip and EMG in microvolts (µV).

2.2.2 Soleus Stretch Reflex


Soleus stretch reflexes were evoked using an electrodynamic shaker (ET-1126B;
Labworks Inc), placed over the more and less affected triceps surae tendons, in
separate trials [7]. Constant pressure was applied against the tendon and the shaker
was programmed to deliver a single sinusoidal pulse at a frequency of 100Hz. A
total of 30 pulses were delivered pseudo-randomly between 3 and 5 seconds.
Maximum soleus stretch reflexes were determined as the average of the three
largest peak to peak amplitude values of the reflex sweep, measured and reported in
millivolts (mV).

2.2.3 Cardiovascular Measures


These values were obtained with a digital blood pressure cuff placed over the less
affected arm. Values are reported in beats per minute (bpm) and millimeters of
mercury (mmHg).

2.2.4 Nerve Stimulation

During treadmill walking, cutaneous reflexes were evoked via combined surface
stimulation of the nerves innervating the dorsum of the hand (superficial radial;
SR) and foot (superficial peroneal; SP). Electrodes for SR and SP nerve stimulation
were placed just proximal to the radial head and on the crease of the ankle,
respectively, on the LA limbs. A Grass S88 stimulator with SIU5 stimulus isolation
and a CCU1 constant current unit (AstroMed-Grass Inc., Canada) was used to
deliver stimulation in trains of 5 x 1.0 ms pulses at 300Hz. Perceptual and radiating
thresholds (RT) were determined and non-noxious intensities were found for each
participant. Stimulation intensities were set to 2.2 x RT for the SR nerve, and 2.0 x
RT for the SP nerve. During treadmill walking, 120 stimulations were delivered
pseudo-randomly with an interstimulus interval of 1-5 seconds.
EMG data were sampled at 1000 Hz and analyzed offline for background
amplitudes and cutaneous reflexes. Background amplitudes were obtained from
steps without stimulation and quantified as the average peak response within a step.
A step was identified with custom-made force sensing resistors and determined as
482 T. Klarner et al.

the time between ipsilateral heel-strikes of the LA leg. Peak amplitudes are
reported in microvolts (µV).
To analyze cutaneous reflexes, stimuli were aligned to delivery and averaged
together. The average trace from the non-stimulated data was subtracted from the
stimulated average trace to produce a subtracted EMG ‘reflex’ trace. The stimulus
artifact was removed from the subtracted reflex trace and data were then low-pass
filtered at 30 Hz using a dual-pass, fourth order Butterworth filter. Cutaneous
reflexes were quantified as the average cumulative reflex over 150 ms following
stimulation.

2.3 Statistics
Using commercially available software (SPSS 18.0, Chicago, IL) reliability of
measures was determined with intraclass correlation coefficients to examine
absolute agreement in measures across time. A repeated measures ANOVA was
also used to examine differences across testing sessions. Statistical significance was
set at p ≤ 0.05.

3 Results

Data averaged across all participants from the three testing sessions are shown in
Table 1.

Table 1 Group data of baseline measures

Measure Test 1 Test 2 Test 3 ICC p


EMG During MVC (µV, standard deviation (sd))
LA SOL 27.7, 14.6 23.3, 8.3 29.9, 12.0 0.864* 0.417
MA SOL 15.2, 11.7 11.5, 5.7 12.9, 8.1 0.886* 0.318
LA TA 81.2 ,33.0 82.4, 39.4 91.1, 47.2 0.930* 0.459
MA TA 36.2, 31.9 27.0, 13.0 27.4, 17.9 0.665* 0.511
LA FCR 31.1, 12.9 30.3, 7.4 28.9, 9.6 0.869* 0.756
MAFCR 10.4, 9.4 12.9, 10.2 10.9, 8.1 0.950* 0.316
Maximum Plantarflexion and Dorsiflexion Torque (Nm, sd)
LA DF 10.6, 8.6 12.5, 9.1 11.4, 9.5 0.968* 0.343
LA PF 15.3, 11.0 18.6, 8.7 17.4, 10.2 0.875* 0.484
MA DF 6.5, 3.9 5.1, 4.3 6.3, 4.9 0.714* 0.401
MA PF 10.2, 5.7 9.9, 10.0 10.6, 5.4 0.736* 0.973
Maximum Hand Grip (kg, sd)
LA GRIP 32.3, 7.9 33.2, 8.1 32.6, 8.7 0.970* 0.753
MA GRIP 11.3, 14.7 11.0, 15.2 10.7, 14.7 0.998* 0.634
Stretch Reflex Amplitude (mV, sd)
LA 0.64, 0.37 0.55, 0.47 0.51, 0.25 0.932* 0.183
MA 0.59, 0.35 0.56, 0.32 0.67, 0.22 0.714* 0.567
Reliability of Multiple Baseline Measures for Locomotor Retraining after Stroke 483

Table 1 (continued)

Cardiovascular Measures (beats/min & mmHG, sd)


HR 74.2, 8.9 73.1, 5.9 74.1, 9.9 0.949* 0.757
Systolic BP 132.5, 10.7 134.6, 11.5 126.3, 14.6 0.775* 0.136
DiastolicBP 85.0, 8.8 81.7, 7.5 80.2,12.1 0.704* 0.115
Locomotor Background EMG Value (µV, sd)
LA SOL 18.9, 6.8 22.6, 11.9 18.7, 9.2 0.819* 0.144
LA TA 17.8, 9.5 20.3, 11.6 21.9, 13.2 0.904* 0.219
LA FCR 16.1, 7.7 16.7, 6.1 15.6, 4.3 0.813* 0.702
LA PD 17.7, 7.2 20.2, 21.2 19.3, 17.1 0.852* 0.825
MA SOL 13.3, 18.5 9.2, 2.5 11.9, 6.7 0.525* 0.595
MA TA 16.4, 14.0 14.0, 10.7 11.9, 7.6 0.581* 0.975
MA FCR 5.8, 2.6 5.4, 1.7 5.2, 1.6 0.840* 0.578
MA PD 5.9, 1.4 5.5, 2.0 5.6, 2.6 0.865* 0.561
Subtracted Cutaneous Reflex Amplitude (µV, sd)
LA SOL -0.15, 3.3 -0.22, 3.4 0.71, 1.9 0.626* 0.617
LA TA -1.4, 4.8 0.80, 7.5 0.88, 4.0 0.691* 0.342
LA FCR 7.3, 8.4 5.8, 7.3 4.1, 7.4 0.874* 0.287
LA PD 1.8, 3.6 3.4, 5.2 3.2, 4.5 0.873* 0.223
MA SOL 0.63, 1.2 0.30, 1.2 0.82, 0.9 0.700* 0.351
MA TA 0.04, 1.7 0.92, 1.9 -0.29, 1.9 0.680* 0.109
MA FCR 0.05, 0.5 0.34, 0.4 0.00, 0.2 0.792* 0.214
MA PD 0.08, 0.2 0.26, 0.4 0.23, 0.2 0.413* 0.233
* indicates significant intraclass correlation (p≤0.05). p-values from RM ANOVA are also reported.
Values are means for the less (LA) and more (MA) affected limbs for the soleus (SOL), tibialis anterior
(TA), flexor carpi radialis (FCR) and posterior deltoid (PD).

For within-subject comparison across testing sessions, values remain un-


normalized. To assess reliability, intraclass correlation coefficients and p-values
from RM ANOVA were calculated and are reported in Table 1. Asterisks indicate
significant correlations.
Figure 1 shows background EMG and cutaneous reflexes for muscles of the LA
and MA sides. Quantified levels of background EMG and reflex activity averaged
across all participants are reported in the bottom half of Table 1. In general,
moderate to high correlations were observed for all variables with a range of 0.665
to 0.998 for significant intraclass correlation coefficients. Although some variables
(e.g. cutaneous reflexes from LA Sol and MA PD) do not have significant
correlation across testing sessions, no significant differences were observed
for any variable following RM ANOVA and overall reliability of measures was
supported.
484 T. Klarner et al.

Fig. 1 Background EMG and cutaneous reflexes during treadmill walking for three testing
sessions averaged across all stroke participants. Test session 1 is in black, test session 2 is
in light grey and test session 3 is dark grey. Plots on the left show averaged EMG acivity
plotted as a function of the less affected locomotor cycle. Plots on the right show the
average cutaneous reflexes following combined stimulation of the SP and SR nerves during
walking. Data are plotted as a function of time with 100 ms before stimulation and 200 ms
post.

4 Discussion
Here we investigated the reliability of multiple baseline measures using a repeated
test protocol in stroke participants. Reliability analysis revealed strong correlation
Reliability of Multiple Baseline Measures for Locomotor Retraining after Stroke 485

amongst most variables and no significant differences were found when comparing
across multiple time points.
Multiple baseline measures should be considered a valid alternative or
replacement to the concept of a control group, given high internal consistency of
measures. In this way individual participant data contributes to a meaningful set of
baseline data with which to compare measures following an intervention, allowing
each participant to act as their own control. Indeed, several previous investigators
have successfully used a multiple baseline design to show improvement in motor
function for stroke participants. Butefisch and colleagues showed an improvement
in hand function following training [1] and more recently Dragert and Zehr showed
that unilateral dorsiflexion training can increase strength compared to a
participants’ baseline control values [8].
The robust nature of these baseline measures in stroke participants highlights
their value as assessment tools for intervention studies. These results were expected
as others have also found high association between baseline measures in stroke
participants. For example, high intraclass correlation coefficients (ICC) were found
for the amount of time taken during five repetitions of the sit-to-stand test [2], time
taken on the 10-m walk test [3], and in other temporal gait measures [4].
Here we expand current literature on multiple test reliability of baseline values
in stroke participants. Measures of strength and cardiovascular resting state test
physiological baselines and are often directly targeted by training interventions.
While reflex measures may not be the target of training itself, these measures can
be used to test underlying changes in overall nervous system plasticity. For
example, the strength of transmission between the arms and the legs can be tested
by remote movement conditioning of reflex amplitudes. In addition, the soleus
stretch reflex can be used as a clinical evaluation tool and for the assessment of
changes in spasticity [9].
Differences in absolute values between the more and less affected sides
observed here corroborate previous findings of asymmetry following stroke.
However, the general presence of interlimb cutaneous reflexes confirms that
neuronal pathways linking the arms and the legs remain at least partially conserved
[10] providing a substrate for training induced plasticity to improve function after
stroke.

5 Conclusion

Reliability of measures was supported with observations of high consistency in


values obtained across multiple baseline time points in stroke participants. These
results support the idea that multiple measures could provide valid, reliable and
meaningful baseline data useful for comparing results of an intervention study
where participants act as their own control.
486 T. Klarner et al.

Acknowledgment. The main support for this research was provided by a Grant-in-aid of
Research (EPZ) and doctoral fellowships (TK, TSB) from the Heart and Stroke Foundation
of Canada (BC & Yukon). Additional funding was provided by the Natural Sciences and
Engineering Research Council of Canada (EPZ).

References
[1] Butefisch, C., Hummelsheim, H., Denzler, P., Mauritz, K.H.: Repetitive training of
isolated movements improves the outcome of motor rehabilitation of the centrally
paretic hand. J. Neurol. Sci. 130(1), 59–68 (1995)
[2] Mong, Y., Teo, T.W., Ng, S.S.: 5-repetition sit-to-stand test in subjects with chronic
stroke: reliability and validity. Archives of Physical Medicine and Rehabilitation
91(3), 407–413 (2010)
[3] Collen, F.M., Wade, D.T., Bradshaw, C.M.: Mobility after stroke: reliability of
measures of impairment and disability. Int. Disabil. Stud. 12, 6–9 (1990)
[4] Holden, M.K., Gill, K.M., Magliozzi, M.R., Nathan, J., Piehl-Baker, L.: Clinical gait
assessment in the neurologically impaired. Reliability and meaningfulness. Phys.
Ther. 64, 35–40 (1984)
[5] Lagerquist, O., Zehr, E.P., Baldwin, E.R., Klakowicz, P.M., Collins, D.F.: Diurnal
changes in the amplitude of the Hoffmann reflex in the human soleus but not in the
flexor carpi radialis muscle. Exp. Brain Res. 170, 1–6 (2006)
[6] Zehr, E.P.: Considerations for use of the Hoffmann reflex in exercise studies. Eur. J.
Appl. Physiol. 86, 455–468 (2002)
[7] Palomino, A.F., Hundza, S.R., Zehr, E.P.: Rhythmic arm cycling differentially
modulates stretch and H-reflex amplitudes in soleus muscle. Experimental Brain
Research 214(4), 529–537 (2011)
[8] Dragert, K., Zehr, E.P.: High-intensity unilateral dorsiflexor resistance training results
in bilateral neuromuscular plasticity after stroke. Experimental Brain Research 225(1),
93–104 (2013)
[9] Voerman, G.E., Gregoric, M., Hermens, H.J.: Neurophysiological methods for the
assessment of spasticity: the Hoffmann reflex, the tendon reflex, and the stretch
reflex. Disability & Rehabilitation 27(1-2), 33–68 (2005)
[10] Zehr, E.P., Loadman, P.M.: Persistence of locomotor-related interlimb reflex
networks during walking. Clinical Neurophysiology 123, 796–807 (2012)
Continuous Monitoring of Respiration during
Rehabilitation

Marketa Kotova1, Ludek Zalud2,3, Jana Kolarova1,3, and Petr Dobsak3,4


1
Biomedical Engineering, Brno University of Technology, Brno, Czech Republic
xkotov01@stud.feec.vutbr.cz, kolarova@feec.vutbr.cz
2
Department of Control and Instrumentation,
Brno University of Technology, Brno, Czech Republic
zalud@feec.vutbr.cz
3
Center of Biomedical Engineering, St. Ann's University Hospital Brno,
Brno, Czech Republic
4
Department of Sports Medicine and Rehabilitation,
St. Ann's University Hospital Brno, Brno, Czech Republic

Abstract. Continuous monitoring of respiratory rehabilitation is important for


evaluation of the respiratory function and its improvement. Respiratory
rehabilitation can be applied in many of neuromuscular diseases or after chest
surgery. We have proposed a simple method for monitoring breathing in the chest
and in the abdomen by measuring with two pressure cuffs placed in the chest and
abdomen area. The measurement is relative, but sufficient for the purposes of
respiration exercises or for on-line therapeutic games based on breath control.
Another proposed method uses Time-of-Flight camera. This type of measurement
is absolute and suitable for both diagnosis and continuous monitoring of therapy.

1 Introduction
The proper way of breathing is important for everyone. Healthy people often do not
follow respiration until breathing problems start - during stress or during sport
activity in physiological cases. More serious cases are stroke, injury or surgery of
the chest and others. So, learning to breathe correctly is considerable for many
reasons.
Spirometry is a basic method of respiratory examination. A standard breathing
test measures forced vital capacity, which represents an amount of air, which can
be expelled after a deep breath. But this method is unacceptable for continuous
respiratory monitoring during long term rehabilitation. A disadvantage is the use
of mouthpiece or mask, which is not comfortable for anyone during exercises.
Some research teams have dealt with respiratory inductive plethysmography
(RIP) [1], [2], impedance plethysmography [3] and optoelectronic plethysmography
(OEP) [5]. All mentioned methods are contact (all mentioned methods require skin
contact), rarely available and expensive. Other research groups have dealt with the
detection of breathing by using camera and projection of the light pattern on the
patient - structured light plethysmography (SLP) [4].

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 487
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_72, © Springer International Publishing Switzerland 2014
488 M. Kotova et al.

We decided to measure respiration by two different ways. The first method is


based on measurement of the pressure associated with the expansion and
contraction of patient’s chest and abdomen during breathing with pressure cuffs
(Vernier with custom modification). The second method uses Time-of-Flight
(TOF) Camera SwissRanger SR-4000, which is non-contact and more suitable for
monitoring of long-term changes in the rehabilitation of patients.

2 Methods

2.1 Method Based on Pressure Measurement


The pressure cuffs are strapped around the chest and abdomen and pump air into
the belt with the hand bulb. They monitor the pressure associated with the
expansion and contraction of the chest during breathing. The positions of cuffs are
shown in Figure 1.
The measurement outputs are time dependent curves describing the changes of
chest and abdomen volumes. This measurement is relative and is used mainly for
correct breathing training and momentary monitoring during the therapy and used
for biofeedback - therapeutic games based on respiration control.
The patient usually sits for better handling cuffs on his body, but it is not
necessary.

Fig. 1 Principle of measuremnt by pressure cuffs

2.2 Method Based on Time-of-Flight measurement


SwissRanger SR-4000 TOF scanner is used to acquire data. Principle of
measurement by TOF camera is shown in Figure 2. The distance between camera
and patient surface is equal:
s = (t ⋅ c) / 2 , (1)
Continuous Monitoring of Respiration during Rehabilitation 489

where s is the distance between camera and patient body surface, t is the time
traversal of light emitted from light source placed in TOF camera and reflected
light from body surface, and c is the speed of light.
The camera uses near-infrared light (850nm) and image resolution is 176x144
pixels. The acquisition process is fast and distance error is in the order of
centimeters for 5m distance and single measurement without filtration [6].
The measurement output is a time sequence of 2D images showing a map of
distances between the camera and each point on the body surface. Therefore, this
method enables localization of regions (in spatial and temporal domain) of
pathological and incorrect movements of chest and abdomen. Thus, an
appropriately selected color map will help to visualize this important information
content of the acquired measurements. This measurement is absolute and also
suitable for biofeedback applications.
The measurement is performed with the patient lying down because of better
fixation of the upper-body, thereby reducing measurement errors in the method
with TOF camera.

Fig. 2 Principle of measuremnt by TOF camera

3 Measurement

The experiment is designed to demonstrate the applicability of the two novel


methods for continuous monitoring of respiration. The measurement results are
shown for basic measurements on two people. The measurement was carried out
as follows.
The measurement devices and the pressure cuffs are fixed on patient’s body.
Both described measurement methods are used independently – with pressure
cuffs or TOF camera. When all instruments are prepared and the patient is ready,
measurement can start.
490 M. Kotova et al.

First, the person breaths normally and then, maximum inhalation and
exhalation is measured to check actual respiratory capacity. Then, person breathes
differently during three experimental parts (marked as number of experimental
part in graph): 3 times in the abdomen (1), then 3 times in the chest (2), and finally
3 times into both areas (3). During the whole experiment, the relative changes of
chest and abdominal volumes were continuously measured by method with
pressure cuffs. In next whole experiment, the distances between chest and
abdominal surfaces and camera were continuously measured by TOF camera also
for 3 breaths into the abdomen, into the chest and into both areas. After that, the
average values of relative changes of volumes and absolute distances between
surfaces and camera in each experimental parts measured for chest and abdominal
(marked as chest (1-3) and abdominal (1-3) in graph) were calculated for both
methods and plotted into one graph.

Fig. 3 Comparison of respiratory activity of woman vs. woman plays a musical wind
instrument
Continuous Monitoring of Respiration during Rehabilitation 491

4 Results and Discusion

Comparison of respiratory activity of two woman measured by both methods is


shown in Figure 3. The x axis is divided into three sections corresponding to the
experimental parts: 1- patient breaths into the abdomen, 2- patient breaths to chest
and 3- patient breaths in both areas. The y axis on left side corresponds to relative
changes of chest and abdominal volumes measured by method with pressure cuffs.
The y axis on the right side corresponds to the distances between chest and
abdominal surfaces and TOF camera.
In Figure 3, we see that the woman was breathing in all areas as expected. It
means, during the first experimental part the average values should be higher for
abdominal: abdominal (1) > chest (1). The average values for second experimental
part should be higher for the chest: chest (2) > abdominal (2). Finally, during the
last experimental part measurement, relationship between the average values
cannot be predicted, because this strongly depends on the individual. In this case,
the first women prefers chest breathing (women use more thoracic breathing).
Looking at the results of the woman who plays a musical wind instrument, the
women breathes in the abdominal during each experimental part. This difference
can be binged about long experience on playing a wind musical instrument. The
main finding is that measurement results done by both methods are in correlation
during the whole experiment.
Two new methods for monitoring breath were introduced. The first method uses
pressure cuffs and measurement is relative. The second method uses TOF camera
and the measurement is absolute.
Both proposed methods are suitable for continuous monitoring of respiration
during rehabilitation. The method based on pressure measurement is simple, cheep
and suitable for self-depended home therapy. The second method, based on Time-
of-Flight measurement, is more suitable for diagnosis and rehabilitation in medical
facilities. The device itself (i.e. the TOF camera) is much more expensive and
needs more qualified operating staff, but on the other hand it provides absolute data
in terms of physical movements in distances and has the ability to show more
spatial measurements.

Acknowledgment. This work was supported by the European Regional Development Fund
- Project FNUSA-ICRC (No. CZ.1.05/1.1.00/02.0123).

References
[1] Wolf, G.K., Arnold, J.H.: Noninvasive assessment of lung volume: respiratory
inductance plethysmography and electrical impedance tomography. Critical Care
Medicine 33(suppl. 3), S163–S169 (2005)
[2] Strömberg, N.O., Dahlbäck, G.O., Gustafsson, P.M.: Evaluation of various models for
respiratory inductance plethysmography calibration. Journal of Applied Physiology
74(3), 1206–1211 (1993)
492 M. Kotova et al.

[3] Ansari, S., et al.: Impedance plethysmography on the arms: Respiration monitoring.
IEEE International Conference on Bioinformatics and Biomedicine Workshops
BIBMW, pp. 471–472 (2010)
[4] Wareham, R.J., et al.: Structured light plethysmography (SLP) compared to spirometry:
a pilot study. European Respiratory Journal (350) (2009)
[5] Aliverti, A., et al.: Optoelectronic plethysmography in intensive care patients.
American Journal of Respiratory and Critical Care Medicine 161(5), 1546–1552 (2000)
[6] Ringbeck, T., Systems, B.U.: A 3d Time of flight camera for object detection.
Measurement 9(2), 636–642 (2007)
The Effects of Neuromuscular Electrical
Stimulation on Corticomuscular Coherence
in Patients with Stroke

Meei-I Lai1, Li-Ling Pan1, Chung-Lan Kao2, Mei-Wun Tsai1,


Shun-Hwa Wei1, and Li-Wei Chou1
1
Department of Physical Therapy and Assistive Technology,
National Yang-Ming University, Taipei, Taiwan
{unicorn30916,hope881212}@hotmail.com,
mwtsai1@gmail.com, {shunhwa,lwchou}@ym.edu.tw
2
Department of Physical Medicine and Rehabilitation,
Taipei Veterans General Hospital, Taipei, Taiwan
chunglankao@gmail.com

Abstract. Neuromuscular electrical stimulation (NMES) applied in the periphery


can elicit strong sensory input that could modulate the excitability of contralateral
primary sensorimotor cortex. Here we want to understand the immediate effects of
1-session NMES on the coherence between brain and muscles and motor
performance in patients with stroke. EEG (16 channels) of bilateral sensorimotor
cortical area and surface EMG of the stroke-affected flexor pollicis brevis were
recorded while the subjects performed a 20-second steady hold contraction at 50%
maximal voluntary before and after a 40-minute electrical stimulation session on
median nerve. The stimulation (1-ms rectangular pulse, 100 Hz) was delivered with
a 20 s-on-20 s-off cycle. The intensity was set at the subjects’ highest tolerable level
without causing pain. Our preliminary results from 8 stroke subjects (3 in sham-ES
group) showed that coherence between contralateral primary motor cortex (hand
area) and flexor pollicis brevis muscle increased in lower gamma-band after using
NMES. Subjects performed better in force-maintenance task after receiving NMES.
Based on our preliminary results, NMES appears to increase corticomuscular
coherence and motor performance. Greater gamma-band coherence after repetitive
electrical stimulation might indicate enhanced cortical activity level and
sensorimotor integration during voluntary motor task.

1 Introduction

Stroke is one of the major contributors for loss of functional abilities and
independence in adults [1]. Previous studies have demonstrated that central
nervous system damages caused by stroke would change cortical excitability [2,
3], which is a key factor inducing abnormal motor patterns observed clinically.
Because of a direct pathway between somatosensory area and motor cortex [4, 5],

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 493
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_73, © Springer International Publishing Switzerland 2014
494 M.-I. Lai et al.

somatosensory input influences the reorganization of motor cortex. Using


neuromuscular electrical stimulation (NMES) on peripheral nerve in healthy
subjects, previous studies found that electrically-elicited sensory input could
modulate the excitability of contralateral primary sensory and motor cortex [6-10],
and it may enhance the hand functions in patients with stroke [11, 12].
The level of synchronization between EEG and EMG (corticomuscular
coherence), can be used to assess neural connectivity between cortex and muscles
[13]. Higher coherence values indicate a more synchronized pattern in order to
create consistent oscillation [14]. In addition, coherence is task dependent and
different frequency bands represent unique brain function [13-16]. By collecting
real-time EEG and EMG during movements, we can better understand the effects
of NMES on the functional connectivity between our brain and muscles, and
especially during dynamic tasks and functional voluntary movements.
Here we want to better understand the effects of NMES on the functional
connectivity between brain and muscles during voluntary movements in patients
with stroke, which were determined by the level of synchronization between EEG
and EMG (corticomuscular coherence). Once NMES is proved to be able to
enhance corticomuscular functional connectivity during voluntary movements, it
can be applied clinically to help regain motor function.

2 Methods

2.1 Subjects
Eight stroke subjects (2 female, 59.6 ± 10.2 yrs. old, range 48 to 79 years) were
recruited. Subjects were randomly assigned to ES or sham-ES group before the
experiment began. At the time of this report, 5 subjects (1 female) were in ES
group, and 3 subjects were in sham-ES group. Two subjects were suffered from left
hemiparesis in each group. All the patients were first-time stroke victims. The
mean time after stroke onset was 39.2 months (range 2.5 to 72 months) in ES
group, and 15.5 months (range 7.5 to 26 months) in sham-ES group. All the
subjects, except one male in ES group, were right-handed according to their
self-report. At the time of the experiment, all patients showed partial voluntary
movement of their thumbs and muscle power of thumb flexion was at least 2/5.
Individuals with history of neurological disorders, or limitation in range of motion
for thumb flexion, or unable to tolerate repetitive electrical stimulation (or severe
paresthesia) were excluded. Subjects were given their informed consent prior to
participation in the experiment. All the experimental procedures were performed
with the oversight of the Institutional Review Board of Shin Kong Wu Ho-Su
Memorial Hospital, and in accordance with the Declaration of Helsinki.
The Effects of Neuromuscular Electrical Stimulation 495

2.2 Experimental Procedure and Analysis


Subjects were seated comfortably in a chair with arm and back support. The
forearm was position in full supination and elbow in 90-degree flexion and
supported on the table. The stroke-affected thumb was secured in a ring attached to
a torque measurement device and the forearm was gently fixed with Velcro straps.
Before electrical stimulation, 16-channel EEG of bilateral sensorimotor cortical
area (fig. 1) and surface EMG of the affected flexor pollicis brevis were recorded
while the subjects performed a 20-second steady-hold contraction at 50% maximal
voluntary contraction (MVC). Subjects were instructed to maintain force as steady
as possible with real-time visual feedback of the thumb flexion force and targeted
force level (50% of MVC) on a screen in front of him/her. Two practice sessions
were given to each subject prior to the actual experiments.. Next, median nerve of
the affected hand was stimulated with 1-ms rectangular pulses at100 Hz, with a 20
s-on-20 s-off cycle [17]. The intensity was set at the subjects’ highest tolerable
level without causing motor response and pain. Electrodes were placed on the same
place without electrical stimulation in sham-ES group. After the NMES session,
EEG and EMG were collected again while the subjects performed the same
20-second steady-hold contraction of their stroke-affected thumb.

2.3 Data Analysis and Statistics


Sampling rate of both EEG and EMG were at 1000 Hz, and the recordings were
segmented into artifact-free epochs of 512 sample points with 256-sample overlap
(ranging from 80 to 100 epochs) to generate linear correlation between EEG and
EMG. Coherence from 0 to 60 Hz was calculated between the EEG of each of the
16 channels and the EMG of the flexor pollicis brevis muscle by customized
programs written in MATLAB. Coherence was calculated using the following
equation with a frequency resolution of 0.98 Hz.

|P |
|C |
P ·P

In this equation, Pxx(f) and Pyy(f) are auto-power spectral density of the EEG
and EMG signals (represented as x and y) throughout the segments for a given
frequency f, and the Pxy(f) is the cross- power spectral density between them.
Coherence is a measure of linear correlation between two signals on a scale from 0
to1, where 1 indicates a perfect correlation [18]. EEG electrodes with changes in
coherence greater than one standard deviation after NMES session were selected
for further comparison.
496 M.-I. Lai et al.

Fig. 1 16-channel EEG of bilateral sensorimotor cortical area

Fig. 2 Coherence value between contralateral primary motor cortex (Cz, C2, C4) and flexor
pollicis brevis muscle before (a) and after (b) NMES. Note the increased coherence in
gamma band in C4 after NMES. Other 4 subjects in ES groupshowed similar trend.

Motor performance was evaluated by the deviation of force trajectory from the
targeted 50% MVC level. By using cumulative sum procedure, force deviation
from the value of 50% MVC in each bin of the timeline for 20 seconds was
calculated. The result then divided by the amount of data points for normalization.
Mann-Whitney U test was used to compare peak value of coherence and force
deviation between ES group and sham-ES group. Correction of multiple
comparisons was made by using Bonferroni method.

3 Results

Our preliminary results from 8 stroke subjects showed that coherence between
contralateral primary motor cortex (hand area, C3 or C4) and flexor pollicis brevis
muscle increased in lower gamma-band after using NMES (p=0.025). The
The Effects of Neuromuscular Electrical Stimulation 497

non-affected side of brain showed no consistent change between 2 groups. Fig. 2


showed change of coherence before and after using NMES of one of the subjects in
ES group. Theoretical threshold of coherence was calculated (at the significance
level of 0.05) [18], which showed in red dotted line. Peak value of
gamma-coherence increased in the 40-to-50 Hz frequency band after 40-minute
NMES session. In motor performance comparison, subjects in ES group
demonstrated better control in maintaining steady force output after receiving
NMES (p=0.025) (Fig. 3).

Fig. 3 Force deviation of all the subjects before and after NMES. Subjects who recevied
true-ES controlled better on maintaining steady force output after 40-minute NMES session.

4 Discussion

After a 40-min NMES session, the main changes were in gamma band coherence of
the affected hemisphere. It is demonstrated that beta band coherence is associated
with mild to moderate isometric contractions [15, 16, 19]. In contrast, gamma band
coherence is related to stronger muscle contraction and hypothesized to serve visual
and somatosensory information encoding [14, 20-22]. Also, gamma oscillations
play an important role in sensorimotor integration when executing of motor task
[23-25]. Previous studies have revealed that corticospinal excitability of the motor
cortex and cortical activation increased significantly after subjects (stroke and
healthy adults) receiving peripheral electrical stimulation [9-12], which suggest that
these stimulation signals may induce plasticity in central nervous system and
influence motor functions [26, 27]. Since gamma band coherence is related to
process and integrate afferent input information with motor output, we believe that
the increase in gamma band coherence after using NMES is from the increase of
sensory feedbacks and by sensorimotor integration.
498 M.-I. Lai et al.

Changes in corticomuscular coherence reveal functional status of neuromuscular


control during voluntary movements. Corticomuscular coherence is weakened
during isometric visuomotor tasks in patients with stroke [28-30], and increased
beta band coherence with improved motor performance during 20%MVC was
observed in patients with stroke after robotic assistant rehabilitation training [31].
In the current study, by providing abundant peripheral stimulation signals, NMES
appears to enhance the functional connectivity of motor cortex and muscles,
resulting in enhance lower gamma band coherence and motor performance under
50%MVC isometric contraction condition. Our preliminary work demonstrates that
peripheral repetitive electrical stimulation is effective in changing brain plasticity
and improving motor performance in patients with stroke.

5 Conclusion

Based on our preliminary results, NMES appears to increase corticomuscular


coherence and motor performance. Gamma band coherence has been demonstrated
that it is correlated with performing stronger isometric contraction. In addition,
gamma oscillations played an important role in afferent inputs encoding, and
increase afferent inputs may have contributed to enhancing gamma-band
coherence. Increased in gamma band coherence after repetitive electrical
stimulation might indicate enhanced cortical activity level and sensorimotor
integration during voluntary motor task.

Acknowledgment. This work was supported by a grant from Ministry of Education, Aim for
the Top University Plan and National Science Council of Taiwan. The authors also thank Dr.
Chia-Feng Lu for his assistance in coherence analysis.

References
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[2] Traversa, R., Cicinelli, P., Bassi, A., Rossini, P.M., Bernardi, G.: Mapping of motor
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The Effects of Neuromuscular Electrical Stimulation 499

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Exercising the Tibialis Anterior Muscle of
Children with Cerebral Palsy for Improved
Neuroplasticity Using an Electrical Guitar

Jeppe V. Larsen, Thomas B. Moeslund, and Dan Overholt

Institute of Architecture, Design and Media Technology


at Aalborg University,
Frederik Bajers Vej 5, 9200 Aalborg Ø, Denmark
{jvl,tbm,dano}@create.aau.dk

Abstract. This paper is a suggestion on how to improve or extend a known


method of exercising the tibialis anterior muscle for improved mobility for
children with cerebral palsy through neuroplasticity. We suggest that by using
slightly altered existing devices, in this case the Actuated Guitar, it is possible to
motivate children to do functional activities as regular exercises and that it will
provide better results when compared to traditional exercises.

Keywords: Rehabilitation, Musical Instrument, Neuroplasticity, Motivation,


Cerebral Palsy.

1 Introduction

People with Cerebral Palsy often have lowered functionality of the tibialis anterior
muscle, which is the front facing muscle on the lower leg covering the length of
the shin. Having problems to activate the tibialis anterior muscle results in
difficulty doing dorsiflexion of the foot, that is, lifting the tip of the foot upwards.
Normally dorsiflexion is working in tandem with plantarflexion, that is stretching
the foot away from the knee. This is for example used when walking, and help
positioning the foot in the right angle producing a smooth and normal gait cycle.
Lack of control or strength in the tibialis anterior muscle can results in the
characteristic tiptoe gait often seen on children with cerebral palsy. What happens
is that following a planterflexion the tibialis anterior muscle is not strong enough
or not activated properly and a full dorsiflexion is not executed causing the toe to
touch the ground first when walking. This makes it difficult to walk and even
more difficult to walk in rough or non flat terrain. This uneven gait makes it extra
tiring for children with cerebral palsy to follow along in the tempo of normal
children. Therefor rehabilitation of children with cerebral palsy has often focus on
training the tibialis muscle to improve gait and mobility.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 501
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_74, © Springer International Publishing Switzerland 2014
502 J.V. Larsen, T.B. Moeslund, and D. Overholt

2 Methods

2.1 Traditional Training of the Tibialis Anterior Muscle


A common technique used to strengthen the tibialis anterior muscle is a simple
repetitive exercise of the isolated muscle using a device designed for the purpose,
see figure 1. You simply put weight on the front of the foot and the user lifts the
foot as high and as many times he or she can. The device is often used in
combination with other exercises such as long walks or walking in different and
difficult terrains.

Fig. 1 An example of a device used to train the tibialis anterior muscle. The heel is placed
in the cutout and the tip of the foot under the strap. Weight and size can be customized. -
Image provided by Jakob Lorentzen from the Helena Elsass Centret.

2.2 Rehabilitation and Neuroplasticity


Neuroplasticity refers to the brain’s remarkable ability to rearrange areas in the
brain previously used for other specific tasks. The idea is that if an area of the brain
has been damaged that information or functionality can relocate to an undamaged
area of the brain. Advances within this area will be extremely important and helpful
for people with brain injuries like cerebral palsy or stroke victims. Studies show
that by doing 400 – 600 repetitions a day exercise can lead to structural
neurological changes [1][2][3]. There is still a lot to discover regarding
neuroplasticity and how to optimize and target specific areas and functionality of
the brain.
Exercising the Tibialis Anterior Muscle of Children with Cerebral Palsy 503

The type of repetition used in rehabilitation is also important. Passive exercise is


where a therapist is performing or aids the patient in moving a limb opposed to an
active exercise where the patient performs a conscious action himself. When
talking neuroplasticity active exercise is the only type that have showed any results.
[1].

2.3 Motivation through Functional Activity


For children repetition without any apparent goal is quickly becoming a boring
task. The best rehabilitation is the exercises that the child will do by itself in his or
her own context and by own free will. As stated in the section above a high number
of repetitions every day is needed to achieve the desired results and therefor
motivation is the key for a positive result. An indirect way to accomplish this is by
functional activity exercise [1]. A functional activity is an exercise that has a
purpose e.g. picking up a glass. If the active exercises can be either replaced or
supported by functional activities in their everyday lives and interests or hobbies of
the child the chances for self supported continuous rehabilitation will be a lot
higher.

2.4 The Actuated Guitar


Musicians’ brains have often been used as models for neuroplasticity because the
plasticity is rather extreme in the brains of musicians [5]. One of the reasons why the
changes are more pronounced can be because music performance requires, that a
high number of areas of the brain are working simultaneous to coordinate the body
and on the same time interpreting what it is hearing and reacting accordingly [5].
An example of a device that can be used to do functional exercise in a musical
context is the Actuated guitar [4], see figure 2. The actuated guitar was developed
to give people with hemiplegia cerebral palsy, stroke victims or similar disabilities
the ability to play on a real electrical guitar. User studies were conducted during the
2013 Summer Camp at the Helena Elsass Center[6] and showed that children with
no prior musical training were able to produce rhythmic strumming patterns using
their non affected foot and thereby over time be able to operate and play the
instrument.
The system allows for a wide variety of input devices that make an expandable
and divers rehabilitation tool that can be used in many different areas.

2.5 Functional Activity-Based Training of the Tibialis Anterior


Muscle
Our hypothesis is that, using a foot pedal as input to control the Actuated Guitar,
see figure 3, it is possible to setup at functional activity that will facilitate the same
movement patterns as the traditional exercise. The goal is to compare if the
504 J.V. Larsen, T.B. Moeslund, and D. Overholt

Fig. 2 The Actuated Guitar. The actuator pulling the pick across the strings is a motorised
fader from a mixing console. The motor is controlled via a Arduino microcontroller and a
2Motor motor controller mounted inside the guitar’s body.

Fig. 3 The pedal used for strumming the guitar. The height of the pedal will increase or
decrease the angle X and thereby alter the difficulty and the intensity of the exercise.

functional activity’s effect on neuroplasticity is greater than the traditional exercise,


not the muscle building capabilities.
The studies should be longitudinal when dealing with neuroplasticity networks
because it is time consuming, probably 3 – 6 months. First part of the evaluation
will be a qualitative evaluation focusing on how the different exercises motivate the
children. Are the guitar and its possibilities more motivating over time compared to
the traditional exercise? The second part will be a series of test to determine if the
children’s has gained better control of the tibialis anterior muscle.
Exercising the Tibialis Anterior Muscle of Children with Cerebral Palsy 505

3 Discussion

The idea of using existing or slightly altered technologies to replace or improve


existing rehabilitation has numerous benefits. First of all, making people able to
rehabilitate through existing devises and initiatives can significantly cut down
costs. Enabling people with e.g. CP to play a real guitar opens up a world of
opportunities they would otherwise not be able to explore. If they got a one of a
kind custom made instrument, there will be no one to teach them how to play the
custom made instrument. They will not be able to identify with artists playing that
instrument, they will not be able to identify their instrument in popular music, they
will not be able to find inspiration, sheet music or watch videos of performances
the internet. It will be more or less impossible to keep up a long-term motivation.
With a solution like the Actuated Guitar, people can use all the initiatives like every
normal child. By doing just enough scaffolding long-term motivation is possible
and will be fed by the children’s own desire for learning and through that
continuous exercise with a high number of repetitions which will increase the
benefits of neuroplasticity.

Acknowledgment. Funding for this work was provided in part by a grant from Ludvig og
Sara Elsass Foundation.

References
[1] Kimberley, T.J., Samargia, S., Moore, L.G., Shakya, J.K., Lang, C.E.: Comparison of
amounts and types of practice during rehabilitation for traumatic brain injury and
stroke. JRRD 47(9), 851 (2010)
[2] Kleim, J.A., Barbay, S., Nudo, R.J.: Functional Reorganization of the Rat Motor Cortex
Following Motor Skill Learning. Journal of Neurophysiology 80(6), 3321–3325 (1998)
[3] Classen, J., et al.: Rapid plasticity of human cortical movement representation induced
by practice. Journal of Neurophysiology 79(2), 1117–1123 (1998)
[4] Larsen, J.V., Overholt, D., Moeslund, T.B.: The Actuated Guitar: A Platform Enabling
Alternative Interaction Methods. In: Presented at the SMC Proceedings of the Sound
and Music Computing Conference, pp. 235–238. Logos Verlag Berlin (2013)
[5] Munte, T.F., Altenmuller, E., Jancke, L.: “The musician’s brain as a model of
neuroplasticity,”. Nature Reviews Neuroscience 3(6), 473–478 (2002)
[6] http://www.elsasscenter.dk
Feedback Strategies for BCI
Based Stroke Rehabilitation:
Evaluation of Different Approaches

Alexander Lechner, Rupert Ortner, and Christoph Guger

g.tec Medical Engineering, Schiedlberg, Austria


lechner@gtec.at

Abstract. Brain-computer interfaces (BCIs) allow human communication without


using the brain’s normal output pathways. A BCI is a tool that converts signals
recorded from the user’s brain into control signals for different applications. Most
BCI systems are based on one of the following methods: P300; steady-state
visually evoked potentials (SSVEP); and event-related desynchronization (ERD).
Electroencephalog-ram (EEG) activity is recorded non-invasively using active or
passive electrodes mounted on the human scalp. In recent years, a variety of
different BCI applications for communication and control were developed. A
promising new idea is to utilize BCI systems as tools for brain rehabilitation. The
BCI can detect the user's movement intention and provide online feedback for
rehabilitation sessions. In many cases, stroke patients can re-train their brains to
restore effective movement. Previous work has continued to show that higher
density electrode systems can reveal subtleties of brain dynamics that are not
obvious with only few electrodes. This paper tries to optimize current BCI
strategies for stroke rehabilitation by comparing conventional bar feedback (bFD)
to immersive 3-D virtual reality feedback (VRFB).

1 Introduction

Brain - Computer Interfaces (BCI) allow new communication channels using


different mental states. In a typical BCI, a user performs voluntary mental tasks.
Each task produces distinct patterns of electrical activity in the
electroencephalogram (EEG). Using monitoring systems and on-line signal
processing software, automatic tools can identify which mental tasks a user
performed at specific times. Most modern BCI applications rely on one of three
types of mental tasks, which are associated with different types of brain activity:
Imagined movement, which produces event-related desynchronization (ERD)
dominant over central electrode sites [1, 2]; Attention to oscillating visual stimuli,
which produces steady-state visual evoked potentials (SSVEPs) dominant over
occipital sites [3]; Attention to transient stimuli, which produces the P300 event-
related potential dominant over parietal and occipital sites [1, 4]. In the last
few years, several publications suggested that using motor imagery based

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 507
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_75, © Springer International Publishing Switzerland 2014
508 A. Lechner, R. Ortner, and C. Guger

Brain-Computer Interface systems (MI-based BCI) can induce neural plasticity


and thus serve as important tools to enhance motor rehabilitation for stroke
patients [5 - 8] . Ang et al. [5] reported higher 2-month post-rehabilitation gain on
Fugl-Meyer (FM) assessment scale for patients using a BCI-driven robotic
rehabilitation tool compared to a control group (6.0 versus 4.0), but without
significant results. However, among subjects with positive gain, the initial
difference of 2.8 between the two groups was increased to a significant 6.5 after
adjustment for age and gender. Recently, Shindo et al. [6] tested the effectiveness
of neurorehabilitation training when using a BCI for controlling online feedback
from a hand orthosis. The motor-driven orthosis was hypothesized to help the
patient extend his paralyzed fingers from 90 to 50 degrees. That article also
concluded that the therapy improved rehabilitation. Grosse-Wentrup et al.
summarize the state of the art in this research field [9].
Neurofeedback is a process that uses real-time displays of EEG or functional
magnetic resonance imagining (fMRI) to illustrate brain activity, usually with the
goal to control central nervous system activity. In MI-based BCIs, neurofeedback
is critical to optimize the user’s performance. As the user practices the skill,
sensory and proprioceptive (awareness of body position) input initiates feedback
regulation through the relevant motor circuits. Over time, the skill becomes more
and more automatic. The learning mechanism in this case is similar to learning to
ride a bicycle [2]. Hence, the feedback must reflect the user’s task in an
appropriate way. For example, when using the BCI for motor rehabilitation, the
feedback should be similar to the motor activity.
In [8], Ramos-Murguialday et al. investigated an online proprioceptive BCI
system linking hand movements and brain oscillations, eliciting implicit learning
effects and producing an increase in sensory-motor rhythms (SMR) related neural
network excitation during motor imagery, passive and active movement. Their
results demonstrated that the use of contingent positive proprioceptive feedback
BCI enhanced SMR desynchronization during motor tasks.

2 Methods
In this study, two different feedback strategies that can be used for a rehabilitation
task are evaluated. During two sessions, the participants were asked to perform MI
of either the right or left hand (in random order) as dictated by a visual paradigm.
The first feedback strategy shows the hands of an avatar in a 3-D Virtual Reality
Feedback environment (VRFB; see section 2). Either the left or the right hand of
the avatar moves according to the MI. For comparison, a popular strategy (bFB,
e.g., in [1]) was used. Here the feedback entails the movement of a bar on the
computer screen. This bar always starts in the middle of the screen and extends
either to the left or right side of the screen, according to the detected motor
imagination. Seven persons were tested using both feedback strategies. EEG was
measured with 63 EEG channels, distributed over the whole cortex. Recently,
Neuper and colleagues compared different BCI feedback strategies [10].
Feedback Strategies for BCI Based Stroke Rehabilitation 509

Fig. 1 Workflow of the model

There, the realistic feedback consisted of a hand grasping a target, and the bar
feedback was similar to the present study. While Neuper used only three bipolar
channels for the classification, the present study used a common spatial patterns
(CSP) approach. The higher number of channels, combined with the method of
CSPs, yields better classification results [11].

2.1 Paradigms and Sessions


The method of CSP creates a set of spatial filter that are optimized for each user
separately and hence increase classification accuracy in comparison to fixed filter
setups [11 - 12]. The whole online classification workflow can be seen in Fig. 1.
Data were bandpass filtered between 8Hz and 30 before the four most important
spatial filters were applied, resulting in four feature channels. For further
processing, the variance of these four channels was calculated within a moving
window of 1.5 seconds. These values were then normalized and log transformed
before using them for a Linear Discriminant Analysis (LDA) classification. The
LDA output finally controls the feedback device.
Before the tests started, the healthy users (all male right handed persons between
25 and 30 years old) were trained on motor imagery tasks until they reached
significant control accuracy (p<0.05). After that, the two sessions with different
feedback were executed. The workflow can be seen in the middle of Fig 1. Each
session consisted of seven runs; each run included 20 trials for left-hand movement
and 20 trials for right-hand movement in a randomized order. The first run (run1)
was performed without providing any feedback. The resulting data were visually
inspected, and trials containing artifacts were manually rejected. These data were
used to compute a first set of spatial filters (CSP1) and a classifier (WV1).
With this first set of spatial filters and classifier, another four runs (run2, run3,
run4, run5) were performed while giving online feedback to the user. The merged
data of these four runs (run 2, 3, 4 and 5) were used again to set up a second set of
spatial filters (CSP2) and a classifier (WV2) that used a higher number of trials and
was more accurate. Finally, to test the online error rate during the feedback
sessions, two more runs (run 6, run 7; merged data: run 6 and 7) were done.
510 A. Lechner, R. Ortner, and C. Guger

Each trial lasted eight seconds; between each trial there was a random trial to
trial interval between 0.5s and 1.5s to avoid adaptation. After two seconds, a beep
directed the user to the upcoming cue. The cue-phase, during which the subject was
told to imagine moving either the left or right hand, started at 3s and stopped at
4.25s.
The end of the cue-phase was marked by a second beep. The feedback-phase
started at 4.25s and lasted until the end of the trial (8s). The user was asked to
perform the MI from the beginning of the cue-phase until the end of the feedback-
phase. The feedback was updated every sample, classification was done on a
sliding window.
The error rate can be calculated by comparing the presented cue and the
classified movement. The error rate, as displayed in Table 1, was calculated by
applying CSP2 and WV2 onto the merged datasets run 6 and 7. The classifier and
the errors were calculated every 500 ms. For every such calculation, the classifier
was applied to the features and the classification result compared to the cue,
resulting in the error rate that was averaged over all trials. The “accuracy” term
used in this paper refers to the difference between 100% and the calculated error
rate. For each session two values of error rate were calculated: the minimum error,
which is the lowest value within the feedback phase. Second, we calculated the
mean error rate, which is the mean of the single error values during the feedback
phase (4.5s – 8s).

2.2 Feedback Strategies


Feedback strategy number one (bar feedback; bFB, see Fig. 1) is quite common for
motor imagery tasks. A bar begins in the middle of the computer screen and
extends either to the left or the right of the screen. If a left-hand movement is
detected, the bar grows to the left; for a right-hand movement, it extends to the
right side. The length of the bar is proportional to the classified LDA-distance.
During the cue phase, in addition to the bFB, a red arrow points to the left or to the
right side of the screen, indicating to the user which MI he or she should perform.
The virtual reality feedback (VRFB) strategy instead uses a virtual reality
research system (g.VRsys, g.tec medical engineering GmbH, Austria). The user sits
in front of a 3D-PowerWall wearing shutter glasses. The size of the PowerWall is
3.2m x 2.45m, and the distance between PowerWall and user is about 1.5m. The
user sees the left and right hands of an avatar from a first-person point of view (see
Fig. 1). The only movement the avatar performs is the continuous opening and
closing of either the left or the right hand. No modulation of the speed of the
movement is done. During the cue-phase (from second 3 until second 4.25 of the
experiment), the user needs to know which MI has to be performed. In the VRFB
task, the opening/closing of one of the hands provides this information. After
second 4.25, a second beep appears, and the observed movement of the avatar is the
feedback to the performed MI.
Feedback Strategies for BCI Based Stroke Rehabilitation 511

Table 1 Error rate of 7 subjects using both feedback strategies

bFB VRFB

Subject Mean Err. Min. Err. Mean Err. Min Err.


(%) (%) (%) (%)

S1 42.30 33.80 37.30 31.30

S2 5.50 0.00 3.20 0.00

S3 35.50 20.00 37 25.00

S4 45.70 37.50 30.70 25.00

S5 5.20 2.50 14.10 5.00

S6 17.00 11.30 5 1.30

S7 3.90 1.30 4.60 0.00

mean 22.16 15.20 18.84 12.51

3 Results

For each session, the averaged error rate over all trials and over the single time-
steps starting from 4.5s until 8s is shown. Table 1 summarizes the results from
these seven subjects. The first number shows the mean error rate and the second
number shows the minimum error rate.
These values reflect the error rate resulting from applying CSP2 and WV2 to the
data of runs 6 and 7, and show the online error rate that the users experienced
during these runs. The first number in each cell shows the mean error rate, the
number in parentheses shows the minimum error for the single time-steps. The
results show a significant performance variance between subjects.
In three out of seven subjects, the error rate increased with the VRFB, but
overall, the bFB yielded worse results compared to the virtual reality (S1, S2, S4
and S6). This shows also the mean error rates or all subjects.

4 Conclusions

This study compared two different feedback strategies for performing MI for stroke
rehabilitation. The VRFB provided realistic feedback that was similar to the
imagined movements. Hence, we expected this strategy would lead to better
classification. This hypothesis was only true with the mean error rate of all seven
subjects. Data of some single users though shows different results. After the
sessions, subjects said that it was quite disturbing when the classifier erred, and
hence the “wrong” hand moved during the VRFB session. We propose that this
512 A. Lechner, R. Ortner, and C. Guger

mismatch between expected and actual feedback was primarily responsible for both
this cognitive dissonance and worse performance. In future studies, we will only
feedback when the correct hand is classified.
Acknowledgment. This work was funded by the EC project Better.

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A System for Real-Time Estimation
of Joint Torque with Evoked EMG
under Electrical Stimulation

Zhan Li, Mitsuhiro Hayashibe, David Andreu, and David Guiraud

INRIA DEMAR Team


and
LIRMM, CNRS/University of Montpellier II,
Montpellier, France
{zli,hayashibe,andreu,guiraud}@lirmm.fr

Abstract. Functional electrical stimulation (FES) is a useful rehabilitation


technique for restoring motor capability of spinal cord injured (SCI) patients
by artificially driving muscle contractions. Real-time FES systems with online
modulation ability are in great need for clinical applications. In this work, a
system for real-time estimation of joint torque with evoked electromyography
(eEMG) is presented. Kalman filter (KF) is adopted and embedded into the
system as the online torque estimator. The real-time estimation system would
be promising toward FES control with consideration of torque changes caused
by muscle fatigue.

1 Introduction
Functional electrical stimulation (FES) is able to restore injured subjects’
motor ability by delivering electrical current pulses to their paralyzed mus-
cles. Muscle contraction can be artificially driven through the recruitment of
motor units by electrical stimulus. The elicited muscle contraction transfers
muscle-tendon force to the limb segment and finally results in joint move-
ment. The resultant joint force/torque was found to be highly correlated
to evoked electromyography (eEMG) [1][2]. Explicit consideration of eEMG
which represents evoked muscle electrical activities for joint torque estima-
tion and control, could distinguish the actual moment elicited by stimulus
and that by external forces. In our previous works [3][4][5], eEMG was em-
ployed for muscle fatigue tracking with surface and implanted stimulation
electrodes placed on patients, and we analyzed and evaluated the estimating
performance in a off-line way with the recorded data. From such off-line anal-
ysis and evaluation we see that the eEMG based estimation approach can be
considered for torque prediction, implying its potential online usage for FES.

This work is partly supported by FP7 European EPIONE project.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 513
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_76,  c Springer International Publishing Switzerland 2014
514 Z. Li et al.

In realistic clinical environments for personalized neuroprosthetics


[6][7][10], the FES executions divided in loops should be completed adaptively
within a reasonable time duration (few ms). The closed loop modeling in-
volving the acquired bio-feedback information (e.g., eEMG and joint torque)
has to be established and identified in real-time to facilitate the stimulus
modulation. In addition to evaluating and verifying the eEMG based torque
estimation approaches with the recorded data in a off-line way, developing
the real-time eEMG based torque estimation system is one of the key pre-
liminary steps before implementing real-time closed loop torque control. If
the real-time eEMG-based torque estimation/prediction works well, one may
consider to perform further real-time predictive torque control by FES.
Here we list some major issues which should be considered as follows.
1) Acquisition and processing of raw eEMG and human kinetics/kinematics
data should be performed synchronously to determine the true correlation
between them;
2) estimation should be computed every stimulation loop;
3) stimulation sampling time should be maintained regardless of additional
torque estimation process.
One key and challenging point can be that the computational identification
time should be constrained to the time intervals between adjacent stimula-
tion loop executions. Theoretically a Mwave appears once per stimulation
loop post stimulus delivered to motor units, and the instant identification
should be done before the next Mwave appears. Therefore, model parame-
ters updating for every stimulation loop has to be achieved no more than
the period of the loop. Otherwise, there will be largely-accumulated time
lags between the real torque and estimated torque, making the estimation
corrupted.
In this paper, we present a real-time eEMG based joint torque estimation
system. In such system, raw eEMG (M-wave) and joint torque data are ac-
quired synchronously and afterwards mean absolute value (MAV) of the raw
eEMG is calculated per stimulation loop. Recursive Kalman filter (KF) is
used as the online estimator for identifying MAV-to-torque relationship. Pre-
diction results show promising performance of real-time eEMG based joint
torque estimation system.

2 Protocol and Data Processing


The system tests were conducted on one able-bodied volunteer subject upon
his consent, as a pilot study before entering a wide protocol on spinal cord in-
jured patients (approved by Nı̂mes Ethics Committee, France, 2013).
The system setup for the torque estimation experiment is shown in Fig. 1.
The system consists of the wireless stimulator [9] (Vivaltis Inc., Montpellier,
France) as shown in Fig. 2, eEMG (Biopac MP100, Biopac Systems Inc.,
A System for Real-Time Estimation of Joint Torque 515

Fig. 1 Experimental setup for real-time FES-induced torque estimation

Santa Barbara, CA, USA) and torque acquisition devices (Biodex 3, Shirley
Corp., NY, USA), and a laptop computer with the MATLAB interface for
data processing and torque estimation. The subject is seated on the chair
with the ankle at 90 degrees, while the joint center was aligned with the axis
of a calibrated dynamometer. The shank was adjusted to be horizontal to
the ground with the knee joint at 40 degrees. The foot was strapped to the
pedal to transmit ankle torque to the dynamometer and to allow the optimal
recording of isometric ankle torque. The bipolar AgCl EMG electrodes were
positioned over the muscle belly in the direction of muscle fiber with 20mm
interelectrode spacing. The reference electrode was placed on the patella of
another leg. Electrical current pulses generated through the wireless stimula-
tor were delivered to the right Tibialis (TA) muscle group with surface elec-
trodes placed. Raw eEMG of TA muscle group and ankle joint torque were
recorded, amplified (gain 1000) and sampled at a frequency fsamp = 4096Hz
by an acquisition system with a 16-bit A/D card.
The stimulation frequency was set at fstim = 40Hz leading to the loop
execution time 25ms. The maximum pulse width (PW) of the stimulator was
limited to 350μs. The suitable stimulation intensities were found to be 25mA.
The test session included two phases: identification and prediction phases.
Each sequence contained trapezoidal trains consisting of 2s stimulation (0.5s
ramp-up, 1s plateau and 0.5s ramp-down) and 2s rest. During identification
phase, the plateau stimulation PW of each trapezoidal train was increased
516 Z. Li et al.

Fig. 2 Wireless stimulator (Left) with its control unit (Right)

gradually with step size of from 10% to 90% of the maximum PW. After
identification, the plateau stimulation PW was randomly determined within
40% to 100% of maximum PW in the prediction phase. The real-time PW
series were predefined and dispatched through MATLAB Timer object and
then sent to the wireless stimulation unit. The stimulation artifacts existing
in the raw eEMG were removed by blanking with additionally involving the
following steps: 1) Calculate differences between adjacent raw eEMG samples
recorded in one loop (around fsamp /fstim ≈ 103 samplings); 2) Compare
these differences with a threshold value, if the differences are larger than
it, set the corresponding adjacent raw eEMG samples as zero. During every
loop the mean absolute value (MAV) of eEMG and mean value of torque
were computed based on the fsamp /fstim ≈ 103 raw eEMG and raw torque
sampling respectively. Next, when there was no stimulus, the corresponding
MAV value was set to zero. Since detection of the whole area of Mwave needs
exact detecting of the M-wave lasting duration in real time, which could be
rather difficult to detect, the MAVs of eEMG were averaged to be smoother
(with a 0.8s time length moving window).

3 Online Kalman Filter Estimator


In a previous work, a polynomial Hammerstein model (PHM) was used as the
estimator model which could represent muscle contraction. Wwe defined con-
traction dynamics as the relationship between muscle activation and torque
production [3][8]:


l 
m 
n
y(k) = ai y(k − i) + bi cj uj (k − i) + w(k) (1)
i=1 i=1 j=0

where y(k) denotes model response output and u(k) denotes model input, ai ,
bi , and cj denote the model parameters to be identified, w(k) is the zero mean
A System for Real-Time Estimation of Joint Torque 517

0.35

0.3

0.25
MAV of eEMG (V)

0.2

0.15

0.1

0.05

0
0 5 10 15 20 25 30 35 40 45 50
Time (s)

10
Measured
Identification Phase
Estimated
8
Prediction Phase

6
Torque (Nm)

−2
0 5 10 15 20 25 30 35 40 45 50
Time (s)

Fig. 3 Plotting of real-time online eEMG based torque estimation results. Up-
per: MAV of the measured eEMG; Lower: corresponding estimated and measured
torque containing identification and prediction phases, from t = 20s identification
is switched off.

Gaussian white noise. In case of identifying relationship between stimulus


and eEMG, u(k) denotes normalized stimulus PW and y(k) denotes MAV of
eEMG; In case of identifying relationship between eEMG and torque, u(k)
denotes MAV of eEMG and y(k) can denote analog voltage signal (with the
baseline-value effect eliminated) scaling real torque.
The state space form of such PHM is described as follows:

x(k) = A(k)x(k − 1) + B(k)Φ(u(k − 1)) + w(k) (2)

y(k) = x1 (k) (3)


where w(k) is Gaussian white noise vector and Φ(u(k−1)) = [u(k−1) u2 (k−
1) · · · un (k−1)]T . Matrix A(k) transforms the previous state vector x(k−1)
into the current state vector x(k). Coefficient B(k) denotes coupled linear and
nonlinear parameter matrix associated with input u(k − 1).
Recursive KF with a forgetting factor λ ∈ [0.9 1] [3] is adopted as the
online estimator in the real-time environment. Since eEMG is involved as the
bio-feedback in the closed loop, dual estimators can exist. One is estimator
between stimulus and eEMG, and the other is between eEMG and torque [8].
518 Z. Li et al.

Here, the recursive KF contains two parts, first one is a priori estimate phase
and the second one is a posteriori update phase.
1) a priori estimate:

x̂(k) = F(x(k − 1), u(k − 1)) (4)

P̂(k) = A(k − 1)P(k − 1)AT (k − 1)/λ (5)

ŷ(k) = x̂1 (k) (6)


where x̂(k) and P̂(k) are the priori estimated state vector and plant covari-
ance matrix respectively, and ŷ(k) is the predicted muscle output.
2) a posteriori update:

S(k) = H(k)P̂(k)HT (k) + λI (7)

K(k) = P̂(k)HT (k)S−1 (k) (8)


State vector and covariance matrix are respectively updated by

x(k) ← x̂(k) + K(k)(y(k) − ŷ(k)) (9)

P(k) ← (I − K(k)H(k))P̂(k) (10)


Such recursive KF can be implemented with the real-time measurement
and acquisition system. It is worth noting that the actual obtained torque
τ (k) = Sy(k) (Nm) is scaled according to its linear relationship to the mea-
sured analog voltage y(k) (V) exported from the analog port of the Biodex
chair, where S = 43.2/5 (Nm/V) is the scaling parameter.

4 Results
We present online identification and prediction results obtained by the es-
tablished real-time system. During the whole estimation process, the prede-
fined stimulation pattern is of trapezoidal type. Fig. 3 shows the plotting of
eEMG-based torque estimation results. In the first 20 seconds the model is
undergoing identification, after time instant 20s, measured torque informa-
tion is not used any more and we predict the torque purely based on eEMG
with the identified model.
One motivation of utilizing eEMG-based rather than PW-based estimator
for torque predication is originated from the fact that eEMG-based can be
of higher stability for closed-loop torque control [8]. Utilization of eEMG
may improve potential muscle fatigue tracking. To evaluate the prediction
performance of estimation, we introduce two indexes, root mean square error
(RMSE) and variance accounted for (VAF):
A System for Real-Time Estimation of Joint Torque 519

Table 1 Real-time torque prediction performance evaluation


Trial # RMSE (Nm) VAF (%)
1 1.09 89.10
2 0.63 87.61
3 0.52 87.82
4 0.75 74.13
5 0.66 67.26


N 2
k (τm (k) − τ̂ (k))
RMSE =
N

and
var(τm − τ̂ )
VAF = (1 − )×%
var(τm )
where τm is the actual measured torque vector and τ̂ is the predicted torque
vector. Tab. 1 shows the aforementioned performance indexes for the predic-
tion of the able-bodied subject with five trials. The overall average RMSE
and VAF are respectively 0.73±0.21 Nm and 81.14%±9.86%. The system’s
loop execution time of the every instant estimation was between 18ms and
20ms for all loops, which was not exceeding 25ms. The measure maximum
torque of the subject was around 15Nm, so the RMSEs of the five trials are
below 1Nm indicating accurate predictions achieved by the system.

5 Conclusion and Future Work


In this work, a real-time system for online estimation of joint torque with
evoked electromyography (eEMG) is presented. The whole estimation sys-
tem consists of eEMG/torque acquisition and predefined-pattern stimulus
delivery. Kalman filter (KF) is adopted and embedded into the system as the
online estimator. Such real-time online torque estimating system produces
promising prediction results. If the computational time of every stimulation
loop is less than 1/fstim , the real-time estimation system can hold the stimu-
lation frequency fstim fixed. Additional functionalities of real-time FES-based
torque control into the system should not much increase the executive time of
each computation loop and the system operation has to be restricted within
the stimulation loop duration 1/fstim . Thus, in order to deal with this time
constraint,development of efficient online computational estimation/control
algorithms is important and the online torque control function is under de-
veloping based on the method as in [8]. Additionally, in order to further eval-
uate feasibility of the real-time torque control with eEMG as bio-feedback,
520 Z. Li et al.

the next step needs to perform the experiment with SCI patients. We will
demonstrate the feasibility of restoring complex movement using closed loop
FES on SCI patients.

References
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force sensor of isometric electrically stimulated muscle. IEEE Trans. Biomed.
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3. Zhang, Q., Hayashibe, M., Fraisse, P., Guiraud, D.: FES-induced torque predic-
tion with evoked emg sensing for muscle fatigue tracking. IEEE/ASME Trans.
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prediction under muscle fatigue in implanted neural stimulation. J. Neural
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prediction with evoked EMG synthesized by NARX-type recurrent neural net-
work. In: Proc. IEEE/RSJ Int. Conf. Intell. Robots Syst., Vilamoura, Portugal,
pp. 2198–2203 (2012)
6. Waltz, E.: An electrifying awakening electrical stimulation of the spinal cord
could let paralyzed people move again. IEEE Spectr. 50(11), 46–52 (2013)
7. Borton, D., Micera, S., del Millán, J.R., Courtine, G.: Personalized neuropros-
thetics. Sci. Transl. Med. 5(210), 210rv2 (2013)
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closed-loop torque control in functional electrical stimulation. IEEE Trans.
Biomed. Eng. 60(8), 2299–2307 (2013)
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tecture for therapeutic functional electrical stimulation: a technology to design
network-based muscle control. In: Proc. IEEE EMBS Conf., Buenos Aires, Ar-
gentina, pp. 6218–6221 (2010)
10. Li, Z., Hayashibe, M., Fattal, C., Guiraud, D.: Muscle fatigue tracking with
evoked EMG via recurrent neural network: toward personalized neuroprosthet-
ics. IEEE Comput. Intell. M. 9(2), 38–46 (2014)
Wheelchair Control with the Tip of the Tongue

Eugen Romulus Lontis1, Bo Bentsen1, Michael Gaihede2,


and Lotte N.S Andreasen Struijk1
1
Center for Sensory Motor Interaction, Dept. of Health Science and Technology,
Faculty of Medicine, Aalborg University, Fredrik Bajers Vej 7, D3,
9220 Aalborg East, Denmark
{lontis,brasse,naja}@hst.aau.dk
2
Department of Otolaryngology, Head & Neck Surgery,
Aalborg University Hospital, DK-9000 Aalborg, Denmark
mlg@rn.dk

Abstract. A tongue controlled oral interface for control of assistive devices has
been developed for disabled persons at Aalborg University. The interface consists
of a mouthpiece attached to the palate of the oral cavity of the user with dental
retainers, an activation unit attached to the tongue as the upper ball of a piercing
and a central unit for signal processing. The central unit has been interfaced to a
Permobil C500 wheelchair. One healthy subject performed driving tests on two
triangular tracks of 7.2 m (two sides of 2 m length at 900) and on a linear track of
8.34 m (4.17 m forward and 4.17 m backwards) to evaluate maneuverability of the
wheelchair controlled by the tip of the tongue. Mean maximal velocities of 0.31,
0.28, 0.26, 0.3, and 0.61 m/sec were obtained on the two triangular tracks on both
directions and on the linear track respectively, after 3 to 4 repetitions of the driving
test on each track. These results suggest that good control of the wheelchair may
be obtained using the oral interface in a short period of training.

1 Introduction
Dramatic change of the quality of life of a person results after an injury of the
sensory-motor system at the cervical level of the spine. A high degree of disability
confines the person in a wheelchair and requires daily assistance of a helper.
Several research teams have aimed to partially restore or compensate the lost
functionality of the disabled person in the last decades. Interfaces using the intact
functionality of the voice, brain, eyes, head, and tongue have been developed to
provide control of assistive devices to increase mobility and communication
ability of the disabled person [1], [2], [3], [4].
A tongue controlled oral interface has been developed at Aalborg University
based on inductive sensors [5], [6]. The printed circuit board technology (PCB)
has been used to manufacture inductive sensors due to the ability to consistently
provide sensors with low tolerance electrical parameters, to design multivariate
geometry of an assembly of sensors, and to facilitate an easy integration process
with driving electronics. The inductive sensor consists of an air-cored coil
designed as a sandwich structure formed by wire windings in interconnected

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 521
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_77, © Springer International Publishing Switzerland 2014
522 E.R. Lontis et al.

A C activation unit
magnetic flux
coil

Vemf

Fig. 1 Tongue controlled oral interface. A Placement of inductive sensors on the palate of
the oral cavity and the activation unit. B Activation unit, glued or pierced to the tongue. C
Principle of activation. Modified from [5] with permission, © 2006 IEEE.

parallel planes [6]. A small cylindrical piece of soft ferromagnetic or conductive


material (i.e. the activation unit) perturbs the magnetic field generated by the
sensor when gliding at the sensor’s surface, inducing a voltage change back into
the sensor (Fig. 1). The sensor’s inductance L changes as a result of the
perturbation of the flux Φ of the magnetic field generated by an electric current i
flowing through the coil according to equation (1). The induced voltage Uemf in the
coil changes with inductance according to Faraday’s law (2).
Φ
L= (1)
i
di
U emf = − L (2)
dt

Sensor’s geometry plays a major role in relation to the size and electrical
properties of the activation unit, extending the functionality of the sensor from an
on-off switch type for text input to a proportional type for movement or position
detection in real-time [6]. A full alphabet keyboard based on a PCB pad having 10
sensors, similar to a mobile phone keypad, and a proportional mouse based on a
PCB pad having 8 sensors with real-time control of both direction and speed,
similar to a joystick, have been implemented. Previous experimental results have
been reported [6], [7]. [8], [9].
The paper reports evaluation of maneuverability of a wheelchair controlled by a
healthy subject using the tongue controlled oral interface when driving on
triangular and linear tracks. The oral interface fully replaced the original joystick
control of a Permobil wheelchair for settings control (chair positions, lights,
access of external auxiliary devices) and driving (real-time proportional control of
both direction and speed).
Wheelchair Control with the Tip of the Tongue 523

2 Methods

2.1 Subjects
One healthy subject gave written consent to participate in the experiment.
Experimental protocol was approved by the Local Ethics Committee (N-
20120039).

2.2 Tongue Controlled Oral Interface


The mouthpiece of the tongue control oral interface consisted of a set of inductive
sensors, driving electronics and a rechargeable battery encapsulated in epoxy
together with dental retainer to optimally fit the palate of the user’s oral cavity (Fig.
2A and 2B). The inductive sensors consisted of interconnected planar coils
manufactured on ten layers in the printed circuit board technology on two pads
connected through a flex print to driving electronics. The upper sensor pad
consisted of ten round coils that had an on-off switch type of functionality similar
to that of a keypad of a mobile phone when the activation unit was placed at or
glided on the surface of the sensor. The lower sensor pad consisted of eight round
or oval sensors. Gliding the activation unit at the surface of these sensors provided
variable signals. Two dimensional track of the activation unit at the surface of the
pad was obtained from combined and processed signals from adjacent sensors
using fuzzy logic, providing a pointing device. The functionality of the pointing
device was similar to that of a wheelchair’s joystick. Placing the activation unit in
the middle of the pad generated no signal, whereas placing the activation unit away
from the pad center in a radial direction provided a vector that made possible
driving the wheelchair along that radial direction having a speed proportional to the
distance between position of the activation unit and the pad center (Fig. 2B).

2.3 Wheelchair Setup and Data Recording


A Permobil C500 wheelchair was used during the test. The central unit of the
tongue controlled oral interface was mounted on the arm support holding the
original control system of the wheelchair (joystick and display, Fig. 2C).
The central unit was wired to the wheelchair’s interface for power and signal
control. An auxiliary master control system of the wheelchair was placed at the
back of the wheelchair so that an assisting person could take over the control of the
wheelchair if needed. A video camera was mounted at the back of the wheelchair
with a 900 view (relative to the floor) of the back wheels as they drove along the
test track. Video recording was performed at VGA resolution at 15 frames per
second.
524 E.R. Lontis et al.

  
tŝƌĞůĞƐƐ
Ϯ͘ϰ',njZĂĚŝŽ

Central Unit

ĂďůĞ Suport arm for


video camera

Fig. 2 A Tongue control oral interface for wheelchair. The mouthpiece placed on the palate
of the oral cavity of the subject transmits data through radio to the central unit (black box).
The central unit processes data and sends the data further through a cable to the interface of
the wheelchair, replacing the original control system of the wheelchair (joystick and two
control buttons, red and white). B Mouthpiece of the tongue control system showing
sensors that replace the two control buttons (upper sensor pad) and the joystick (lower
sensor pad) of the original control system of the wheelchair. C Wheelchair setup,
illustrating attachment of the central unit of the tongue control system, the auxiliary
wheelchair control system, the wheelchair interface, and the arm support for the video
camera for tracking position and speed of the wheelchair.

2 C 4

Fig. 3 Track setup, illustrating the path used for evaluation of wheelchair’s maneuverability
when driving the wheelchair using the oral interface. Two triangular tracks 1-C-2-1 and 1-
C-4-1 (and reverse 1-2-C-1 and 1-4-C-1), and one linear track 1-C-3-C-1 (forward-
backward) were used. The segments 1-C, 2-C, 3-C, and 4-C were of 2 m length. Projection
of the wheelchair’s front wheels was aligned with the starting point 1, giving a 0.17 m start
segment between point 1 and the equivalent center of the wheelchair (i.e. middle point of
the front wheels axis). Circles of 1 m radius as area for maneuver evaluation.
Wheelchair Control with the Tip of the Tongue 525

Table 1 Track with types of maneuvers and the associated total time, track length and mean
velocity
a
Track / length [m] Total time [sec] / mean velocity [m/sec]

1-C-2-1 / 7.2 54.3 S3 25.3 S4 25.8 S4 23.2 S4


/ 0.13 / 0.28 / 0.28 / 0.31
Type of maneuver b
900left 8.9 6.4 7.2 4.3
1350left 10.4 7.8 6.8 7.1
1350left 29.3 10.3 9.3 12.4
1-2-C-1 / 7.2 75.7 S4 25.3 S4 24.6 S4 18.7 S4
/ 0.09 / 0.28 / 0.29 / 0.38
Type of maneuver b
450right 6.7 2.2 5.1 2.9
1350right 24.8 12.6 5.8 4.2
900right 29.1 4.7 5.7 3.4
1800right 13.1 5.2 6.2 7.8
1-C-4-1 / 7.2 48.3 S3 28.7 S4 28.1 S4
/0.15 /0.26 /0.25
Type of maneuver b
900left 11.2 7.4 4.2
1350left 17.4 7.2 6.7
1350left 18.7 12.6 14.1
1-4-C-1 / 7.2 92.3 S3 27.5 S4 23.1 S4
/ 0.08 / 0.25 / 0.3
Type of maneuver b
450right 9.7 6.8 3.2
1350right 9.2 7.6 4.7
900right 9.9 4.9 5.3
1800right 62.3 7.3 9.3
1-C-3-C-1 / 8.34 28.2 S3 17.8 S4 13.8 S4 14.7 S4
/ 0.3 / 0.47 / 0.61 / 0.57
forward c 16.8 6.2 7.7 6.1
backward c 11.3 11.6 5.1 8.6
a
Total time as defined in methods section for the track and type of maneuver, for a given speed level
of the wheelchair, S3 or S4. Mean velocity expressed for the total track only.
b
Type of maneuver executed when driving along the track.
c
Forward and backward correspond to the total time for driving between points 1 to 3 and 3 to 1
respectively.

The central unit was set to send raw and processed data from the mouthpiece to
a PC through Bluetooth. A PC running software provided on-line visual feedback
for sensor activation to an experimenter for quality check of data transmission.
526 E.R. Lontis et al.

2.4 Test Track


Two triangular tracks 1-C-2-1 and 1-C-4-1 (driving on both directions), and a linear
track 1-C-3-C-1 (1-C-3 forward and 3-C-1 backward driving) have been used to
test maneuverability of the wheelchair controlled by the oral interface (Fig. 3).
Each of the two triangular tracks had two equal sides of 2 m (1-C, C-2, C-4) length
at 900. The total length of the track was of 7.2 m, including the triangle perimeter of
6.86 m length plus a start segment of 2 x 0.17 m length at point 1. The linear track
had a length of 8 m plus the start segment of 2 x 0.17 m length at point 1. The start
segment was added to the track so that projection of the front wheels fitted the start
point 1. The subject was instructed to follow the track between the points defined.
Maneuvers at the 450, 900, 1350, and 1800 were defined as driving the wheelchair in
an area represented by a circle of 1 m radius having the center in each of the points
2, 3, 4, and C (Fig. 3). At point 1 the used had to stop in the same position as at the
start of the test. Each track was performed 3 to 4 times.

3 Results

The time and mean velocity for each track and maneuver are shown in Table 1.
Mean velocities decreased with repetition of the test.

4 Discussion

The subject obtained good control of the wheelchair in a relative short time (i.e. 3
to 4 repetitions of each track). The subject has already performed an experiment
controlling a computer (keyboard and mouse) with a previous version of the oral
interface at Aalborg University. A constant visual feedback of sensor activation
was provided at that time helping reducing false activations. Control of the
wheelchair resembles control of the PC mouse, however, the lack of the visual
feedback may increase the time for performing the test, at least for the first trials.
Technique of sensor activation plays a major role in false activation. Continuous
gliding of the activation unit at the sensors’ surface reduces considerably the false
activation due to feedback provided by the wheelchair when moving.
Acknowledgment. The support and the enthusiasm of the subject participating in this study
are greatly acknowledged.

References
[1] Craig, A., Tran, Y., McIsaac, P., Boord, P.: The efficacy and benefits of
environmental control systems for the severely disabled. Med. Sci. Monit. 11(1),
ra32–ra39 (2004)
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[2] Ding, D., Cooper, R.A., Kaminski, B.A., Kanaly, J.R., Allegretti, A., Chaves, E.,
Hubbard, S.: Integrated control and related technology of assistive devices. Asst.
Technol. 15, 89–97 (2003)
[3] Huo, X., Ghovanloo, M.: Evaluation of a wireless wearable tongue-computer interface
by individuals with high-level spinal cord injuries. J. of Neural Eng. 7(2) (2010)
[4] Raya, R., Roa, J., Rocon, E., Ceres, R., Pons, J.L.: Wearable inertial mouse for
children with physical and cognitive impairments. Sensors and Actuators A:
Physical 162(2), 248–259 (2010)
[5] Andreasen Struijk, L.N.S.: An Inductive Tongue Computer Interface for Control of
Computers and Assistive Devices. IEEE Trans. on BME 53(12), 2594–2597 (2006)
[6] Lontis, R., Andreasen Struijk, L.N.S.: Design of inductive sensors for tongue control
system for computers and assistive devices. Disabil. Rehabil. Assist. Technol. 5(4),
266–271 (2010)
[7] Andreasen Struijk, L.N.S., Lontis, E.R., Bentsen, B., Christensen, H.V., Caltenco,
H.A., Lund, M.E.: Fully Integrated Wireless Inductive Tongue Computer Interface for
Disabled People. In: EMBC 2009, Minneapolis, USA, pp. 548–550 (2009)
[8] Lontis, R., Lund, M.E., Christensen, H.V., Bentsen, B., Gaihede, M., Caltenco, H.,
Andreasen Struijk, L.N.S.: Clinical evaluation of wireless inductive tongue computer
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Aires, Argentina, vol. 34, pp. 3365–3368 (2010)
[9] Lontis, R., Caltenco, H.A., Bentsen, B., Christensen, H.V., Lund, M.E., Andreasen
Struijk, L.N.S.: Inductive Pointing Device for Tongue Control System for Computers
and Assistive Devices. In: EMBC 2009, Minneapolis, USA, pp. 2380–2383 (2009)
[10] Kim, J., Park, H., Bruce, J., Sutton, E., Rowles, D., Pucci, D., Holbrook, J., Minocha,
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M.: The Tongue Enables Computer and Wheelchair Control for People with Spinal
Cord Injury. Sci. Transl. Med. 213(5), 213ra166 (2013)
Information on Ankle Angle from
Intramuscular EMG Signals during
Development of Muscle Fatigue in an
Open-Loop Functional Electrical Stimulation
System in Rats

Line E. Lykholt1, Sahana Ganeswarathas1, Anil K. Thota2,


Kristian Rauhe Harreby1, and Ranu Jung2
1
Center for Sensory-Motor Interaction (SMI),
Department of Health Science and Technology (HST),
Aalborg University (AAU), Denmark
{llykho09,sganes09}@student.aau.dk,
krauhe@hst.aau.dk
2
Adaptive Neural Systems Laboratory,
Department of Biomedical Engineering,
Florida International University, USA
{rjung,athota}@fiu.edu

Abstract. Functional Electrical Stimulation (FES) is one method available for


rehabilitation of spinal cord injured subjects. Although FES is used in the clinic
today, reliable and robust feedback for a closed-loop system is limited.
The objective was to examine if intramuscular electromyographic (iEMG) re-
cordings (of tibialis anterior and gastrocnemius medialis) can provide reliable
information of functional movement (i.e. ankle angle) during development of
fatigue.
Four longitudinal intrafascicular electrodes (LIFEs) were implanted in two fas-
cicles of the sciatic nerve in three adult Sprague-Dawley rats. Open-loop FES was
applied to produce rhythmic ankle movement. The FES stimulation pulse widths
and amplitudes were determined for the individual rats based on the strength dura-
tion curve. Each frequency (30, 40, 50, 60 and 70 Hz) was applied to perform 100
step cycles followed by a 15 min rest period. Kinematic information on the ankle
angle and iEMG were recorded simultaneously.
The results showed that the ankle angle and the iEMG amplitude decreased
when the muscles fatigued. A correlation between the ankle angle and iEMG was
present, which indicates that iEMG information can be used as feedback for a
closed-loop system. The correlation was higher at higher stimulation frequencies
(>0.76 at stimulation frequencies above 40 Hz).

1 Introduction
Injury to the spinal cord may cause permanent loss of voluntary motor function
and sensation below the level of the lesion. Functional electrical stimulation (FES)

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 529
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_78, © Springer International Publishing Switzerland 2014
530 L.E. Lykholt et al.

is a technique that has been used for many years for the rehabilitation of subjects
with spinal cord injury. [1], [2], [3]
The aim of the FES is to electrically activate the paralyzed muscles in a con-
trolled way to restore motor function. FES can be applied to the subject using an
open-loop (feedforward) or a closed-loop (feedback) control strategy. [1], [2], [3]
FES is commonly applied in the clinic in an open-loop mode that operates with
fixed stimulation parameters. A clear advantage is that the paradigm is simple and
easy to use. However, prolonged stimulation leads to muscle fatigue. An appropri-
ate closed-loop stimulation strategy could alleviate this problem. However,
closed-loop FES systems are dependent on feedback from the part of the body that
is controlled, and the availability of sensors and signals to provide a reliable feed-
back signal from the controlled limb or organ is therefore essential. [1], [2], [3]
One source of feedback can be achieved by recording kinematic data that pro-
vides information on the joint angles. Kinematics would reveal when fatigue oc-
curs. [1], [4] However, the recording of kinematic information requires specialized
equipment and is a highly time consuming procedure, which is not suitable for
daily use in the clinic or at home. Therefore it will be important to have access to
another source of information. Information on movement and muscle fatigue can
also be obtained through electromyography (EMG) recordings. The use of EMG
recordings would be relatively easy to implement in the clinic or in a portable
system since it is cheap, quick to setup and is used routinely today. Surface EMG
has the advantage of being easy to record but suffers from cross talk and the daily
need to don and doff the electrodes. An alternative signal source is the use of
intramuscular EMG (iEMG), which is a more invasive technique. This may help
overcome some of the drawback associated with surface EMG. Previous studies
show that it is possible to extract information from the iEMG related to the force
during movement [5].
There is today limited knowledge on whether information on joint angles may
be extracted from iEMG during normal movement and how muscle fatigue may
influence this.
The objective of this study was therefore to examine if information extracted
from iEMG recordings can provide reliable information on a functional movement
and during development of muscle fatigue in a rat model.
To investigate the objective, FES using longitudinal intrafascicular electrodes
(LIFEs) was used to produce a cyclic movement of the hindlimb of the rat while
recording iEMG. The FES was applied in an open-loop mode to induce muscle
fatigue over time. Kinematic data was also recorded as a reliable measure of the
movement.

2 Methods

Data was obtained from three adult healthy male Sprague-Dawley rats (294-615
g). The experimental procedures were approved by Florida International Universi-
ty Institutional Animal Care and Use Committee.
Information on Ankle Angle from Intramuscular EMG Signals 531

2.1 Animal Preparation


After induction of anesthesia with isoflurane gas (5 %), a single injection of So-
dium Pentobarbital (40 mg/kg ip) was given. Anesthesia was maintained with
isoflurane (0.5-2.0 %), throughout the experiment. The level of anesthesia was
assessed with toe pinch, and observation of eye blink and the respiration rate. To
prevent dehydration regular subcutaneous injections of isotonic saline in the dorsal
cavity were administered.
The left sciatic nerve was exposed and four single channel LIFEs were inserted
into the fascicles innervating the Tibialis Anterior (TA) and Gastrocnemius Me-
dialis (GM) muscles. The TA and GM are the main muscles involved in the
movement of the ankle and can be activated from one nerve. To verify that the
electrodes were placed correctly inside the fascicles, electrical stimulation was
applied while observing TA and GM muscle twitch. The LIFEs were sutured to
the epineurium and the incision was closed.

Table 1 Applied LIFE stimulation parameters

Amplitude ( ) Pulse width ( )


Rat 1: GM 50 30
Rat 1: TA 30 30
Rat 2: GM 50 60
Rat 2: TA 250 100
Rat 3: GM 30 40
Rat 3: TA 20 30

2.2 Experimental Setup and Data Acquisition


The rat was placed in a prone position on an elevated platform so that the hin-
dlimbs were hanging freely.
3-D kinematic data was recorded by a Peak Motus System (Peak Performance
Technologies, Inc. Centennial, CO) by placing cone shaped three-dimensional
reflective markers on the hip, knee, ankle and toe. The system included two infra-
red cameras focused on the rat at an oblique angle of approximately 45° each. The
kinematic data was sampled at 60 Hz.
To record differential iEMG, two stainless steel fine wire electrodes were in-
serted with an average interelectrode distance of 3.5 mm in the TA and GM mus-
cles. The reference electrode was placed under the skin at the back of the rat. The
iEMG data was amplified (A-M systems Model 1700, gain = 100) filtered (band
pass: filter 100 Hz -10 kHz, notch filter at 60 Hz), sampled (10 kHz, NI USB-
6259, National Instruments, USA) and saved in a PC using a custom LabView
routine.
To determine the stimulation pulse width and amplitude a strength duration curve
was first established by consecutively stimulating the four implanted LIFEs with
different pulse widths (30, 40, 50, 60, 70, 80, 90, 100, 150, 200, 250 and 300 µs)
532 L.E. Lykholt et al.

while increasing the stimulation pulse amplitudes until a muscle twitch was seen. A
pulse width and 1.5 times the amplitude at rheobase were selected for stimulating
the fascicles (see Table 1).
To determine the stimulation frequencies the muscle contraction was visually
observed. The stimulation frequency was chosen such that it provided a fused
contraction, which was later confirmed from kinematic data.
The open-loop stimulation was applied to the fascicles innervating TA and GM
muscles alternately to produce a rhythmic movement. One hundred step cycles
were performed at each stimulation frequency (30, 40, 50, 60 and 70 Hz) followed
by a 15 min period of rest. Kinematic data from ankle movement and correspond-
ing iEMG were recorded simultaneously.

Fig. 1 Shows the range of movement of the ankle angle and iEMG amplitude envelope over
time for the GM muscle. The maximal range of ankle angle and iEMG amplitude envelope
was normalized to 100 %. A gradual decrease in the ankle angle and iEMG was observed
for the GM over time.

2.3 Data Analysis


The kinematic markers were identified using the Peak Motus software. The data
were digitized and filtered with a fourth-order band-pass Butterworth filter [6]. To
find the range of movement for both the GM and TA individually the maximum
range of the movement (maximal extension to maximal flexion) was calculated for
each cycle.
To obtain the iEMG amplitude envelope to investigate when the amplitude de-
creased, the iEMG amplitude was full wave rectified and low-pass filtered (3rd
order low-pass Butterworth filter with 0.5 Hz cut off frequency). The maximal
range of ankle angle and the iEMG amplitude envelope were normalized to 100 %
and an average of the normalized data obtained for the three rats. These averaged
data were used for the rest of the data analysis. Fatigue was defined as a decrease
Information on Ankle Angle from Intramuscular EMG Signals 533

Fig. 2 Shows the range of movement of the ankle angle and the iEMG amplitude envelope
over time for the TA. The maximum range for ankle angle and the iEMG amplitude
envelope were normalized to 100 %. A correlation between the two signals can be ob-
served. The decrease in the iEMG and ankle angle can be observed for the TA after 10-15 s
indicating presence of fatigue.

in the ankle angle and the iEMG amplitude envelope. A correlation coefficient
was calculated between the iEMG and ankle angle for both muscles for each fre-
quency.

3 Results
The movement produced by the GM muscle for all the stimulation frequencies
was in the range of 5-100 % of the maximum ankle angle, see Fig 1. The ankle
angle increased during the first step cycles (approximately 10 s). After this it de-
creased during the rest of the step cycles. The response after 60 Hz decreased
more rapidly than the other frequencies. The iEMG amplitude decreased conti-
nuously and rapidly for approximately the first 25 s (40-60 %). After this the rate
of the decrease was less for the rest of stimulation (30-40 %).
Table 2 Correlations coefficients between ankle angle and iEMG for GM and TA for the
different LIFE stimulations

GM TA
30 Hz 0.36 0.22
40 Hz 0.63 0.95
50 Hz 0.77 0.96
60 Hz 0.85 0.96
70 Hz 0.85 0.96
534 L.E. Lykholt et al.

The movement produced by the TA muscle for all the stimulation frequencies
was in the range of 65-100 % of the maximum ankle angle, see Fig 2. The ankle
angle increased for the first 10 s. After this there was a decrease from 10-25 s
thereafter a plateau was reached for the rest of the step cycles (65-85 %). The
iEMG amplitude was found to be stable for the first 10 s. After this the 50, 60 and
70 Hz response rapidly decreased from 10-30 s (30-60 %), while the 30 Hz re-
sponse produced no changes for the rest of the step cycles (80 %). The 40 Hz
response also had a different tendency where it decreased less compared to 50, 60
and 70 Hz response (85 %). After this a plateau was reached for the 50, 60 and 70
Hz response (30-50 %). Here the 40 Hz response still decreased and did not reach
a plateau (60 %). The ankle angle and the iEMG amplitude demonstrated similar
response.
To quantify the degree of correlation between the ankle angle and the iEMG,
the correlation coefficient between the ankle angle and the iEMG data were calcu-
lated (see Table 2). In the case of the GM muscle, it was observed that the higher
the stimulation frequency that was applied, the higher the correlation observed
(mean and standard deviation of 0.76 +/- 0.1 for 40 HZ – 70 Hz frequencies). In
the case of the TA muscle the same tendency was observed, i.e. coefficients for
the TA was high for the 40, 50, 60 and 70 Hz (0.95 +/- 0.1). This indicated that
there was a good correlation between the ankle angle and the iEMG amplitude
except when applying 30 Hz stimulation.

4 Discussion
In the current study the ankle angle was measured with kinematic data. This was
compared to the iEMG amplitude to examine the correlation between these. The
results showed that there was a correlation between the ankle angle and the iEMG.
The correlation was higher for the TA than the GM.

4.1 Comparison of results with Other Studies


Previous studies from E. A. T. De Laat et al., S. G. Boe et al., J. R. Potvin et al.
revealed that the relation between muscle force and amplitude is present and that
the variable used for this was root mean square amplitude. Here they were looking
at the linear force and root mean square amplitude using surface electrodes. [7],
[8], [9]

4.2 Methodological Considerations


With the use of an animal model instead of a human model the physiological in-
fluences are not the same. When a human walks normally there is a force applied
to the leg due to maintaining balance and standing upright. In this experiment, this
was not taken into account since the leg of the rats was hanging freely and no
external force was applied.
Information on Ankle Angle from Intramuscular EMG Signals 535

The markers were placed by visual inspection of the animal’s anatomical struc-
ture. Placement of the markers may therefore have varied slightly from animal to
animal. During the offline digitization of the kinematic video data it was possible
that some degree of error was present in the marker identification because of in-
distinct images. Especially the toe marker was difficult to distinguish in the video
during the extension phase of the movement.
During the stimulation the frequency was changed from 30-70 Hz. The stimula-
tion was done in that same order during all of the experiments. It is not possible to
judge if a particular stimulation frequency caused some cumulative influence on
the next stimulation sequence. This could be solved by randomization.
A factor that may have had an influence on the results is potentiation. This oc-
curs during continuous stimulation and also has a tendency to happen in fast
twitch fibers, and causes a positive staircase phenomenon [10]. This could likely
explain that some of the kinematic data had a tendency to not reach a maximum of
100 % just after the stimulation onset. Here the maximum movement range was
not reached until approximately 10 s after the onset of the stimulation.

5 Conclusion

In the present study it was investigated if information extracted from iEMG could
provide reliable information on a functional movement (i.e. the ankle angle) dur-
ing development of muscle fatigue. A higher degree of correlation was found
between iEMG and ankle angle when stimulation frequencies above 40 Hz were
applied to produce muscle contractions. Also, the results indicate that TA may be
a more reliable source of feedback than the GM since the TA had higher correla-
tion coefficient than the GM (GM: average of 0.76 +/- 0.01, TA: 0.96 +/- 0.01).
Further research should focus on developing an animal model where the corre-
lation coefficient would be higher. In a future perspective the improvement would
be beneficial for the clinical rehabilitation with the FES for subjects with spinal
cord injury.

Acknowledgment. We would like to thank Ph.D. student Ricardo Siu for manufacturing
the LIFEs. Supported in part by R01-EB008578 to Ranu Jung.

References
[1] Fairchild, M.D., Kim, S., Iarkov, A., Abbas, J.J., Jung, R.: Repetitive hindlimb
movement using intermittent adaptive neuromuscular electrical stimulation in an in-
complete spinal cord injury rodent model. Experimental Neurology 223, 623–633
(2010)
[2] Abbas, J.J., Triolo, R.J.: Experimental Evaluation of an Adaptive Feedforward Con-
troller for Use in Functional Neuromuscular Stimulation System. IEEE Transl. J. 5,
12–22 (1997)
536 L.E. Lykholt et al.

[3] Kim, S., Fairchild, M.D., Iarkov (Yarkov), A., Abbas, J.J., Jung, R.: Adaptive Control
of movement for Neuromuscular Stimulation-Assisted Therapy in a Rodents Model.
IEEE Transl. J 56, 452–461 (2009)
[4] Rose, J., Gamble, J.G.: Human Walking, 3rd edn., ch. 3. Lipincott Willams & Wil-
kins, Philadelphia (2006)
[5] Kamavuakoa, E.N., Rosenvanga, J.C., Bøga, M.F., Smidstrupa, A., Erkocevica, E.,
Niemeiera, M.J., Jensen, W., Farinaa, D.: Influence of the feature space on the estima-
tion of hand grasping force from intramuscular EMG. Biomedical Signal Processing
and Control 8, 1–5 (2013)
[6] Thota, A.K., Carlson, S., Knapp, E., Thompson, B., Jung, R.: Neuromechanical Con-
trol of Locomotion. Journal of Neurotrauma 24(2), 442–465 (2005)
[7] De Laat, E.A.T., Visser, C.P.J., Coene, L.N.J.E.M., Pahlplatz, P.V.M., Tavy, D.L.J.:
Nerve Lesion in Primary Shoulder Dislocation and Humeral Neck Fractures. J. Bone
Joint Surg. 76, 381–383 (1994)
[8] Boe, S.G., Rice, C.L., Doherty, T.J.: Estimation Contraction Level Using Root Mean
Square Amplitude in Control Subjects and Patients With Neuromuscular Disorders.
Arch. Phys. Med. Rehabil., 711–718 (2008)
[9] Potvin, J.R.: Effects of muscle kinematics in surface EMG amplitude and frequency
dur-ing fatiguing dynamic contractions. Department of Human Biology and Nutri-
tional Sciences, 144–151 (1997)
[10] Krarup, C.: Enhancement and Diminution of Mechanical Tension Evoked by Stair-
case and by the Teanus in Rat Muscle. J. Physiol. 311, 355–372 (1981)
Frailty Assessment Based on Trunk
Accelerometry during Walking

Ion Martinikorena, Alicia Martínez-Ramírez, Pablo Lecumberri,


Nora Millor, Marisol Gómez, and Mikel Izquierdo

Public University of Navarre Pamplona, CP 31006 Spain


jon.martinikorena@gmail.com

Abstract. The interest in ageing has been notably increased in the last decade
because of the continue increment of life expectancy. Some of its consequences
like imparity or frailty have become the center of attention of basic, clinic and
poblational investigations due to the incidence level and gravity of the adverse
outcomes derived from the age. It is estimated that the frailty syndrome affects to
the 20% of the population older than 75 years. It is found that the functional
decline derived from this syndrome brings to dependency, institutionalization,
hospitalizing and death. Thus, one of the greatest actual challenges in this field is
to found parameters that can discriminate between vulnerably and healthy
subjects. Frailty causes an accelerated motor impairment. Gait analysis has been
widely used to predict frailty. Characteristics like velocity or spatio-temporal
parameters obtained with walking force platforms have been significantly
considered in the literature. Recently, various studies have revealed that one
inertial measurement unit provides relevant information about human movements
with a minimum part of the cost and complexity of traditional force platforms. In
this way, the aim of the present study is to investigate the applicability of trunk
accelerometry for the assessment of spatio-temporal and frequential gait
parameters allowing clinicians to perform measurements outside the laboratory
environment that could improve the prediction of frailty.

1 Introduction

Frailty syndrome is an age-associated disease that is characterized by decreases in


the functional reserve and resistance to stressors related to different physiological
systems. Though the term, frail, has been widely used to describe the oldest old in
the population, it has become increasingly recognized that, although, frailty is age-
related, it is not caused by old age itself and is not a normal part of aging [1],
therefore the onset of frailty may be possibly preventable, avoided, or delayed [2].
Based on recent estimates, almost 20% of people over age 75 are frail [3]. This
syndrome is strongly associated with sarcopenia and places older individuals at
special risk for disability, hospitalization, and death induced by falls. Along with
sarcopenia, skeletal muscle fat infiltration, which is assessed through muscle

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 537
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_79, © Springer International Publishing Switzerland 2014
538 I. Martinikorena et al.

tissue attenuation, is associated with an increased risk of mobility loss in older


men and women. As a consequence of impaired muscle function, the diagnosis of
frailty includes physical impairments, such as low gait speed, fatigue, and low grip
strength [4]. Although there is a lack of consensus in the definition of frailty, an is
still point of controversy, the most accepted operational definition is the proposed
by Fried et al. using five criteria: slow gait velocity, low physical activity,
unintentional weight loss, exhaustion, and muscle weakness [3] . An individual
with three or more of these criteria is characterized as “frail”, with one or two
items is identified as “pre-frail”, and those with no frailty criteria were categorized
as “not-frail” [4]. Also, the presence of three or more of these criteria has been
independently associated with worsening mobility, disability, incident falls,
hospitalizations, and mortality [4]. Of the five criteria, gait velocity has been
shown to be the best parameter to predict adverse outcomes and the most
successful marker for the identification of physical frailty [4, 5]. In this way, it has
been lot of effort in gait analysis to obtain new characteristics, which could help to
improve the assessment of frailty. The most accepted method in gait analysis is the
ground reaction platforms, which measures three dimensional reaction force
vectors. Although parameters obtained by those methods have been related to
adverse outcomes like physical impairments, falls and other pathologies, their cost
and complexity restricts the use to a laboratory environment, making them
impractical in ambulatory assessments. Recently, various studies have revealed
that one inertial measurement unit provides relevant information about human
movements with a minimum part of the cost and complexity of traditional force
platforms. In this way, the aim of the present study is to investigate the
applicability of trunk accelerometry for assessment of spatio-temporal and
frequential gait parameters allowing clinicians to perform measurements outside
the laboratory environment that could improve the prediction of frailty.

2 Metodologhy
718 subjects from an elderly population (319 males, 399 females age: 75.4±6.1 yr,
mass: 71.8±12.4 Kg, height: 157.5 ± 5.9 cm) volunteered to participate in this
study. All of them were required to complete 3-m walk test at their own pace.
Kinematic and dynamic data were acquired from a tri-axial inertial Orientation
Tracker MTx (WSENS, Xsens Technologies B.V. Enschede, Netherlands)
attached over the L3 region of the subject’s lumbar spine. Output signals and
statistical analysis were computed with Matlab© software..
Measured spatio-temporal parameters, related in the literature with gait
disorders [3, 6-10] were step and stride regularity, gait symmetry, Coefficient of
Variation (CoV) of step time, signal Root Mean Square value (RMS) and
approximate entropy (AE), while frequential parameters were the harmonic ratio
(HR) and total harmonic distortion (THD). All these parameters were obtained for
three directions, vertical (VT), medio-lateral (ML) and antero-posterior (AP).
Frailty Assessment Based on Trunk Accelerometry during Walking 539

Step and stride regularity and gait symmetry were obtained from the
autocorrelation function of the acceleration signal “x”. The autocorrelation
function is represented by a sequence of autocorrelation coefficients A over
increasing time lags “m”:
| |
1
| |
The autocorrelation coefficients were divided by the number of samples in the
time series to be analyzed to obtain unbiased coefficients. The estimation of step
and stride regularity is made measuring the prominence of first Ad1 and second
peak Ad2 after the central (cero lag) peak, respectively. Gait symmetry is
considered as the difference between both peaks and normalized with their
maximum.
| 1 2|
max 1, 2
Gait variability can also be estimated calculating the CoV of step time where
is the mean and σ the standard deviation.

σ
Each step period for one signal is obtained with single peak detection in the
vertical acceleration signal. The RMS value is defined by this equation:

In statistics, approximate entropy (ApEn) is a technique used to quantify the


amount of regularity and the unpredictability of fluctuations over time-series data.
The algorithm used to calculate ApEn for each signal is the proposed by Ho Kalon
et al. [11]. The frequential parameter Harmonic Ratio (HR) is calculated dividing
the sum of odd harmonics by even harmonics and the Total Harmonic Distortion
is the ratio between the sum of amplitudes of all harmonics and the fundamental
frequency amplitude.


In both cases the first 20 harmonics have been considered.


The significance level of the differences in the mean obtained in the three
groups has been calculated using Student’s t-test. Before that all data sets have
passed a Shapiro–Wilk normality test.
540 I. Martinikorena et al.

3 Results

For all parameters, measured in VT direction, we obtain significance differences


(p<0.01) between the three groups. However, no significance differences were
obtained in the AP and ML directions. Results are shown in Table 1.

Table 1 Parameters mean and standar deviations in VT directions and p-value between
groups

Healthy Pre-Frail Frail p-value

mean (std) mean (std) mean (std) H-PF PF-F H-F

Step
0,68 0,16 0,58 0,19 0,42 0,21 * * *
Reg.

Stride
0,64 0,17 0,58 0,19 0,44 0,21 * * *
Reg.

Sym. 0,14 0,11 0,18 0,15 0,25 0,21 * * *

RMS 1,29 0,44 1,04 0,41 0,69 0,29 * * *

step time
0,10 0,07 0,12 0,08 0,15 0,08 * * *
CV

HR 2,33 0,55 2,15 0,46 1,96 0,57 * * *

THD 2,68 1,11 3,35 1,64 4,43 2,34 * * *

AE 0,01 0,02 0,02 0,03 0,05 0,04 * * *

* p<0.01

Figure 1 shows the mean and standard deviation of the vertical acceleration
throughout the steps for one subject of each group (Frail, Pre-Frail and
Healthy).

4 Discussion
These results provide evidence that trunk accelerometry obtained with a unique
inertial measurement unit is a reliable method for detecting gait impairments and it
can provide helpful information to identify frailty populations.
Frailty Assessment Based on Trunk Accelerometry during Walking 541

Fig. 1 Vertical acceleration patterns

Acknowledgment. The authors are indebted to the Spanish Ministry of Health, Insitute
Carlos III, Department of Health of the Government of Navarra and Government of Spain,
Consejo Superior de Deportes for financing this research.

References
1. Fried, L.P., et al.: From Bedside to Bench: Research Agenda for Frailty. Sci. Aging
Knowl. Environ., pe24 (2005)
2. Morley, J.E.: Diabetes, Sarcopenia, and Frailty. Clin. Geriatr. Med. 24, 455–469
(2008)
3. Montero-Odasso, M., et al.: Gait Variability Is Associated With Frailty in Community-
dwelling Older Adults. The Journals of Gerontology Series A: Biological Sciences and
Medical Sciences 66A, 568–576 (2011)
4. Fried, L.P., et al.: Frailty in Older Adults: Evidence for a Phenotype. The Journals of
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(2001)
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Increasing Voltage Transients Using Implanted
Titanium Nitride Neural Stimulation Electrodes

Suzan Meijs1, Morten Fjorback2, Søren Sørensen3,


Kristian Rechendorff3, and Nico J.M. Rijkhoff1
1
Center for Sensory-Motor Interaction (SMI),
Aalborg University, Aalborg, Denmark
smeijs@hst.aau.dk
2
Neurodan A/S, Aalborg, Denmark
3
Danish Technological Institute, Århus, Denmark

Abstract. The electrochemical properties of porous titanium nitride (TiN) stimula-


tion electrode coatings were investigated in vivo in the chronic setting. Four tita-
nium pins were coated with porous TiN and implanted in the pelvic region of two
minipigs. Electrochemical impedance spectroscopy (EIS) was performed daily,
while voltage transient measurements (VTM), electrical stimulation and cyclic
voltammetry (CV) were performed every other week. Electrical stimulation was
applied successfully during the course of the study. Voltage transients and tissue
impedance increased, while charge storage decreased during the first 3-4 weeks
after implantation. This is most likely related to encapsulation of the electrode.

1 Introduction

Neural stimulation is applied to treat many different types of conditions, including


incontinence. The electrode investigated in this study is intended to restore conti-
nence by reflexively inhibiting the bladder muscle [1, 2]. The electrode is
implanted in the pelvic region near the genital nerve, using a minimal invasive
procedure. This has the advantage that the surgical procedure is short and causes
very little damage to the area. However, the position of the electrode with respect
to the genital nerve is not precisely known and is likely to vary from implantation
to implantation. Therefore, a monopolar electrode design is chosen, as shown in
Fig. 1.
As the electrode is implanted using a minimal invasive procedure, it is likely to
be situated at a distance of several millimeters from the genital nerve. This means
that a relatively large current is required to activate the nerve and obtain the de-
sired response. Therefore a porous electrode coating could be advantageous, as
this increases the charge injection limit [3]. Another reason for applying an elec-
trode coating is that the substrate could be made of an inexpensive material, such
as titanium or stainless steel, rather than using platinum, for example. In this
study, we investigate a porous TiN coating.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 543
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_80, © Springer International Publishing Switzerland 2014
544 S. Meijs et al.

The purpose of this study was to investigate the electrochemical properties of


the porous TiN electrode coating in vivo in the chronic setting. The focus of this
paper is on the VTM, as these are a measure for the electrodes’ performance in
terms of electrical stimulation.

Fig. 1 Monopolar electrode in the implantation tool (ø: 3 mm)

2 Methods

Ethical approval was obtained for all parts of the experiments involving animals
(2012-15-2934-00177).

2.1 Electrode Fabrication


Four titanium pins (6 mm2) and two titanium disks (1000 mm2) were coated with a
14 µm thin film of porous TiN using a CC 800/9 industrial-scale DC magnetron
sputtering system (CemeCon AG). This increased the electrochemical surface
area of the electrodes to more than 500 times its geometrical surface area. An eTFE
coated MP35N wire (Heraeus, Switzerland) was crimped onto each electrode pin,
after which a PEEK body was attached to it using silicon adhesive. An eTFE coated
MP35N wire was laser welded onto each titanium disk. The connection was
insulated using silicone to strengthen it.

2.2 Surgical Procedure


Four electrodes were implanted in two Göttingen minipigs using a single step
procedure. An incision was made in the skin next to the vagina. The electrodes
were pushed medially to the implantation site, few centimeters below the skin,
while applying electrical stimulation. A pulse train consisting of five biphasic
pulses with a phase width of 200 µs and an inter-pulse interval of 4 ms was used.
The electrode was released when the threshold for eliciting a contraction of the anal
sphincter was less than 5 mA. One TiN disk counter electrode was implanted at the
back of each pig. The electrodes had a percutaneous exit site at the back of the pigs.

2.3 Electrochemical Measurements


All measurements were made using a 2-electrode setup, with the TiN coated pins as
working electrodes and the TiN disks as counter and pseudo-reference electrodes.
Increasing Voltage Transients 545

Electrochemical impedance spectroscopy (EIS) was performed daily while the


animals were awake and constrained using a custom built sling. The impedance
spectrum was measured from 0.1 Hz – 10 kHz, using Solartron, Model 1294 in
conjunction with 1260 Impedance/gain-phase Analyzer (Solartron Analytical, UK),
run by the accompanying SMaRT software. Using the RC electrode model of Wei
and Grill [4], the series tissue resistance, Rtissue, was assumed to equal the impedance
magnitude at 10 kHz, as the electrode’s double layer capacitance is shunted at high
frequencies. This assumption is valid if the phase angle approaches 0 [4].
CV was performed by cycling the electrode potential between the water
reduction and oxidation limits. These limits were established directly after
implantation. The electrode potential was in- and decreased until an exponentially
increasing current was observed using a sweep rate of 0.05 V/s. CV was performed
every other week while the pigs were anesthetized. 10 CV cycles were recorded at
0.05, 0.1, 0.5 and 1.0 V/s. The surface area under and over the 0 A axis were
calculated to obtain the cathodic and anodic charge storage capacity (CSC) of the
electrodes, respectively.
VTM were made using a cathodic-first bipolar symmetric current pulse with a
200 µs phase duration and a 40 µs inter-phase, during which no current was
applied. The access resistance was subtracted from the VTM to determine Qinj. The
access resistance was calculated as the potential difference between the last data
point of the anodic phase and 20 µs after pulse cessation (Fig. 2). Qinj was reached
when the maximal cathodic and anodic potentials, Emc and Ema, respectively,
reached the water window limits [3]. For analysis of the voltage transients, the open
circuit potentials (OCP) were set to 0 V; this is called normalization (Fig. 2). The
OCP and the potential drop during the inter-phase were used for additional
analyses. The latter was calculated as the difference between the potential 20 µs
after cessation of the cathodic phase and the potential at onset of the anodic phase.
VTM were made every other week, while the pigs were anesthetized. CV and VTM
were performed using a VersaSTAT 3 potentio- galvanostat (Princeton applied
research, USA).

Fig. 2 The access resistance was subtrancted from the original data and the OCP was set to
0V to facilitate comparison of voltage transients
546 S. Meijs et al.

Electrical stimulation was performed every other week using a Teca Synergy T-
EP - EMG/EP Monitoring System (Oxford Instruments Medical, UK). The pigs
were restrained using a sling while stimulation was performed. The lowest current
at which an anal sphincter contraction was observed visually was considered the
threshold. The stimulation current was then increased to determine whether the
sphincter contractions became stronger. Each session took approximately 5 minutes
per electrode.

3 Results

The lead of electrode 2 was missing on the last measurement and it was thus
impossible to make measurements; this data is therefore lacking. As the emphasis
of this paper is on the VTM, these are reported first. Afterwards, a summary of the
other measurements follows.

3.1 Voltage Transient Measurements


The average normalized voltage transients (Fig. 3), increased in amplitude during
the first 26 days. The shape of the voltage transients was curved and did not change
during the implanted period, apart from the amplitude change.
The Qinj could not be determined for any of the electrodes, due to the large
access resistance (~1 kΩ). Therefore, the Ema and Emc at 5 mA (Fig. 4 and 5), were
analyzed. Ema was constant throughout the study, while Emc decreased during the
first 26 days. The difference between the trends in Ema and Emc was partly due to
decreasing OCP during the first 2 weeks (Fig. 6). Directly after implantation, the
average OCP was 156 mV, which decreased to 83 mV and stabilized at
approximately 0 V from day 13.

0.3

0.2
Normalized potential (V)

0.1

0
day 0
-0.1
day 8
-0.2 day 13
day 26
-0.3 day 42
day 53
-0.4
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1
Time (ms)

Fig. 3 Average normalized voltage transients usin a 5 mA current


Increasing Voltage Transients 547

Fig. 4 Emc as a function of time after implantation

Fig. 5 Ema as a function of time after implantation

Fig. 6 OCP as a function of time after implantation


548 S. Meijs et al.

Fig. 7 Tissue drop during the inter-phase as a function of time after implantation

7
Day 0
6 Day 8
Day 26
5 Day 42
Day 53
CSC (mC)

0
0.05 0.1 0.5 1
Sweep rate (V/s)

Fig. 8 Average anodic (dashed) and cathodic (uninterrupted) CSC as a function of sweep
rate

The drop during the inter-phase, shown in Fig. 7, has also influenced the trend
observed for Emc and Ema. The potential difference during the inter-phase period
increased during the first 26 days, after which it stabilized.

3.2 Electrochemical Impedance Spectroscopy


The phase angle at the highest frequencies in the spectrum indeed approached 0.
The average Rtissue was 440 Ω on the day of implantation. It increased to ~800 Ω
after 3 weeks and remained at that level for the rest of the study. The impedance
magnitude at lower frequencies followed the same trend.
Increasing Voltage Transients 549

3.3 Cyclic Voltammetry


The limits for water reduction and oxidation were -0.9 V and 1.2 V, respectively.
The anodic and cathodic CSC, (Fig. 8) were nearly equal for all electrodes
throughout the study at all sweep rates. The CSC decreased from 6.1 mC at 0.05
V/s directly after implantation to 4.3 mC at 0.05 V/s at the end of the study. The
greatest decrease occurred during the first 26 days (1.2 mC at 0.05 V/s), after which
the decrease between the different measurements was comparable to the decrease
between each cycle during a single measurement.

3.4 Electrical Stimulation


Contractions of the anal sphincter were observed during every stimulation session
and for every electrode. The threshold currents were stable during the course of
the study with average currents between 1.5 and 2.5 mA.

4 Discussion

It was possible to activate the anal sphincter during a period of almost 2 months
using stable and safe currents. It was not possible to establish Qinj, but the currents
used for electrical stimulation were certainly below this limit. Although Qinj was
not established, we speculate what an Emc of -400 mV using a 5 mA current
means. In the ideal situation, using twice the current, a voltage transient twice the
size would be obtained. In that case, a maximum of 12.5 mA could be used in vi-
vo. Based on the results of this study, 12.5 mA is enough to achieve reflexive in-
hibition of the bladder, as average stimulation thresholds were between 1.5 and
2.5 mA. In humans, stimulation thresholds between 0.75 and 12.0 mA were found
using percutaneous needle electrodes and stimulation leads [1, 2].
An increasing trend and stabilization of the voltage transients was observed
from day 26. This corresponds well with the decreasing trend and the stabilization
of Emc and the inter-phase potential drop. Furthermore, the OCP showed an in-
crease during the first 2 weeks after implantation, Rtissue increased during the first
3 weeks after implantation and the CSC decreased most during the first 26 days.
After 3-4 weeks, all changes appeared to subside.
It has been established that the increasing Rtissue during the first weeks after
implantation is related to the encapsulation process [4]. It is likely that the stabili-
zation of the OCP is related to the same process, as the OCP depends on the
electrode material and the electrolyte with which it interfaces. The working and
counter electrode are made of the same material, though the tissue they interface
with is slightly different. The counter electrode is implanted directly below the
skin on top of a muscle fascia, while the working electrode is implanted in adipose
tissue. The OCP directly after implantation was therefore different from 0 V. As
the fibrous capsule began to form around the working and counter electrodes, the
550 S. Meijs et al.

OCP approached 0 V, which is expected as both the materials and the electrode-
tissue interface are similar.
The potential drop that occurs during the inter-phase continued to increase up
to 26 days after implantation, which compares well with the increase in the vol-
tage transients and the decrease of Emc. The reason for this is likely that the OCP
stabilizes as soon as the electrode-tissue interfaces at the working and counter
electrodes are similar, while the inter-phase potential drop, the voltage transients
and Emc continue to be influenced until the formation of the tissue capsule is com-
plete. The potential drop observed during the inter-phase is due to slow (> 20 µs)
relaxation processes in the tissue. Directly after implantation, blood accumulates
around the electrode [4], causing a relatively small potential drop during the inter-
phase. This corresponds well with the dielectric properties of both blood as well as
adipose tissue [5, 6], which shows changes in conductivity from 1 MHz. The po-
tential drop due to the tissue resistance as well as its relaxation properties is thus
captured mostly during the first 20 µs after pulse cessation. However, many of the
more fibrotic tissues show changes in conductivity from as low as 10 Hz [5, 6]. It
is likely that formation of a dense fibrotic capsule decreases the mobility of
charged molecules and thereby increases the relaxation time. This causes an in-
crease in the potential drop during the inter-phase, but it also cause an increase in
the voltage transients, as changes are seen from 10 Hz.
The CSC decreased most during the first 26 days of the study, after which the
decrease subsided. The decrease between the different measurements after 26 days
was comparable to the decrease between each cycle within a single measurement
and it is likely that the decrease in CSC is also related to the formation of a dense
fibrous capsule. It is unlikely, however, that the CSC is affected by the decreased
mobility of large charged molecules, as low sweep rates are employed. It is per-
haps more likely that the surface area within the pores cannot fully be utilized
even at low sweep rates, as the cells encapsulating the electrode block the narrow
(< 1 µm) pores.
It is possible, however, that the increasing voltage transients and decreasing Emc
are not only due to changes in the tissue surrounding the electrode, but also to
electrode degradation. In this study, the changes subsided after 3-4 weeks. How-
ever, a similar study has been performed in cats using iridium oxide electrodes [7],
where Emc continued to increase until explantation of the electrodes. The CSC,
however, showed no significant change over time for the one electrode array that
did not show signs of leakage [7]. The continued increase of Emc would indicate
that the observed changes were not due to tissue responses, but to changes of the
electrodes. However, measurements were not performed frequent enough to draw
any definitive conclusions regarding the observed trends [7]. In this study, mea-
surements were made more frequently, but it remains difficult to determine the
cause of the observed changes. They seem to be at least in part caused by changes
in the tissue surrounding the electrode, but this in turn is also influenced by the
implanted material.
Increasing Voltage Transients 551

5 Conclusion

Electrical stimulation was applied effectively during the course of the study, using
currents that were within safe limits. However, the potential excursions using a
stimulation current of 5 mA increased during the first 26 days of the study. It is
suggested that this is related to the encapsulation process, which took place during
the same period.

Acknowledgments. Research supported by the Danish National Advanced Technology


Foundation.
The authors wish to thank the technical staff at the laboratory animal facility of Aalborg
University hospital.

References
[1] Martens, F.M.J.: Diagnosis of neurogenic detrusor overactivity and treatment with
conditional electrical stimulation of the dorsal genital nerves. PhD dissertation, Fac.
Med. Sc., Radboud Univ., Nijmegen (2011)
[2] Goldman, H.B., et al.: Dorsal genital nerve stimulation for the treatment of overactive
bladder symptoms. Neurourol. Urodyn. 27, 499–503 (2008)
[3] Cogan, S.F.: Neural stimulation and recording electrodes. Annu. Rev. Biomed.
Eng. 10, 275–309 (2008)
[4] Grill, W.M., Mortimer, J.T.: Electrical properties of implant encapsulation tissue. Ann.
Bio-Med. Eng. 22, 23–33 (1994)
[5] Gabriel, C., Gabriel, S., Corthout, E.: The dielectric properties of biological tissues: I.
Literature survey. Phys. Med. Biol. 41, 2231–2249 (1996)
[6] Gabriel, S., Lau, W.M., Gabriel, C.: The dielectric properties of biological tissues: II.
Meas-urements in the frequency range 10 Hz to 20 GHz. Phys. Med. Biol. 41, 2251–
2269 (1996)
[7] Kane, S.R., Cogan, S.F., Ehrlich, J., Plante, T.D., McCreery, D.B., Troyk, P.R.: Elec-
trical performance of penetrating microelectrodes chronically implanted in cat cortex.
IEEE Trans. Biomed. Eng. 60, 2153–2160 (2013)
Frailty Detection Using the Instrumented
Version of the 30-s Chair Stand Test

Nora Millor1, Pablo Lecumberri1, Marisol Gómez1,


Alicia Martínez-Ramírez1, and Mikel Izquierdo2
1
Department of Mathematics at Public University of Navarra
Pamplona, C.P. 31006, Spain
nora.millor@gmail.com,
{marisol,pablo.lecumberri,alicia.martinez}@unavarra.es
2
Department of Health Sciences at Public University of Navarra
Tudela C.P. 31500, Spain
mikel.izquierdo@gmail.com

Abstract. Frailty syndrome is regarded as a major predictor of co-morbidities and


mortality in older populations. Performance test such as the 30-s chair stand one
(30-s CST) are a cornerstone for detecting early decline. However, predictions are
normally more qualitative than quantitative. Latest advances in body-fixed sensors
lead us to a new dimension of measurements, kinematic parameters that can
furnish clinicians by objective information to outperform their diagnostics. In the
case of the 30-s CST, it has been demonstrated that an instrumented version of the
test is able not only to directly provide the actual outcome, the number of
performed cycles, but also other kinematic parameters that can explain the
movement performance. This instrumented version involves including an inertial
unit which provides acceleration and angular velocity data. However, different
steps are necessary to extract meaningful information from those rough data. Here,
it is explained the full process to obtain kinematic parameters from the 30-s CST
and the ones able to differentiate different frailty levels (i.e. Z-acceleration and Z-
velocity peaks and positive and/or negative impulses). The main contribution is
that this new quantitative information could be of special help in clinical
diagnostics, home care services and/or in a fall risk prevention program.

1 Introduction

Frailty occurs in people older than 65 years (ranging from 7 to 16.3%), and its
prevalence increases with age [1;2]. Moreover, this geriatric syndrome embodies
an elevated risk of catastrophic declines in health and function among older adults
[2-6]. However, it is not easy to identify those patients who are more prone to
suffer this disability. Up until now, frailty is commonly established using the Fried
criteria according to the following components: slowness, weakness, weight loss,

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 553
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_81, © Springer International Publishing Switzerland 2014
554 N. Millor et al.

exhaustion, and low physical activity. Therefore, a patient was classified as frail if
he had more than three of this components; pre-frail if he had only two and
healthy if he had any of them. Nevertheless, the main problem is that the
identification of these items tends to be more qualitative than quantitative and
requires certain experience of the tester. It is needed to find an automatic tool that
could be able to furnish clinicians with objective parameters to improve their
diagnostics. The detection of a frail-risk status could make it possible to reduce
these syndrome consequences and improve the patient’s well-being.
One of the most used tests in geriatrics to determine one of the factors involved
in frailty (i.e. the lower-limbs forces) is the 30-s chair stand test [7;8]. The reasons
are that: (1) the only requirement to perform the test is a chair, (2) rising from a
chair is regarded as one of the most demanding tasks in our daily life [9] and a
prerequisite to talk [10]. While this test is in wide usage, only the total number of
visually counted full stands is used as a clinical predictor index. Recent
advantages of body-fixed sensors have demonstrated their ability to measure other
movement information, the kinematics [11-13].
Here, we tried to outperform the information about the 30-s CST using the
kinematic parameters which are able to explain how the movement has been
performed. Thereafter this paper explain the performed steps to instrument the 30-
s CST using a unique inertial sensor as well as the selected parameters able to
differentiate different frailty levels.

2 Procedure

2.1 Subjects and Protocol


Four hundred and thirty one subjects from an elderly population volunteered to
cooperate in this study by performing the 30-s CST at their own pace. The
exclusion criteria were disability to perform the test or any unstable medical
condition. Participants were classified according to the Fried criteria, [2].
Therefore, they were divided into a frail group of 31 subjects (aged 79 ± 6 years,
body mass 69.3 ± 11.9 kg, and height 1.54 ± 0.08 m), a pre-frail group of 206
subjects (aged 73 ± 5 years, body mass 75.6 ± 13.8 kg, and height 1.57 ± 0.09 m)
and a healthy group of 194 subjects (aged 74 ± 5 years, body mass 73.2 ± 11.3 kg,
and height 1.58 ± 0.07 m). All of them were thoroughly informed about the
experimental procedure; the purpose, nature, and possible risks associated with the
study; and their right to terminate participation at their discretion. Subsequently,
they provided their written informed consent to participate. These experimental
procedures were approved by the Institutional Review Committee of the Public
University of Navarra and the Department of Health Sciences of the Government
of Navarra, according to the Declaration of Helsinki.
Frailty Detection Using the Instrumented Version of the 30-s Chair Stand Test 555

The 30-s CST consists of standing up and sitting down from a chair as many
times as possible within 30 seconds. A standard chair (with a seat height of 40 cm)
without a backrest but with armrests was used. Initially, subjects were seated on
the chair with their back in an upright position. They were instructed to look
straight forward and to rise after the “1, 2, 3, go” command at their own preferred
speed with their arms folded across their chest. All trials were performed using the
same chair and with similar ambient conditions.

2.2 Instrumentation
An inertial MTx Orientation Tracker (WSENS, Xsens Technologies B.V.,
Enschede, Netherlands) was attached over the L3 region of the subject’s lumbar
spine to provide the kinematic data for each trial. It recorded at a sampling rate of
100 Hz. The L3 position was chosen because of its proximity to the body’s center
of mass (CoM) in the standing position. The nine individual MEMS sensors from
the MTx provided kinematic data such as the 3D acceleration and the 3D rate of
turn (rate gyro). Moreover, the drift-free 3D orientation was also provided by the
MTx using Kalman filters and the previously mentioned kinematic data.

2.3 Data Analysis


An automated data analysis procedure was implemented using Matlab 7.11
(MathWorks Inc., Natick, MA, USA) to improve the objectivity and simplicity of
the current 30-s CST evaluation. The automated analysis provides an accurate
count of the number of repetitions, removing failed attempts as determined by the
roll rotation angle (X-orientation) in combination with the Z-acceleration signal,
and the derived Z-velocity and Z-position, and the kinematic parameters. The
procedure was implemented as a three-step algorithm:

• First, the signals provided by the MTx were processed to obtain the drift-free
Z-velocity and Z-orientation signals. The “PB-algorithm” [14] was used to
remove the drift generated by the double integration. It consisted on a first
fourth-level polynomial curve adjustment to correct the dc-bias due to
assuming a gravity acceleration of 9.8m/s2; and a subsequent baseline
interpolation from local maxima and minima to eliminate the baseline
fluctuations still observed.
• Second, the corresponding sit-to-stand-to-sit cycles and their main phases
(impulse, stand-up and sit-down) [15] were defined using the X-orientation
as well as the Z-acceleration, Z-velocity and Z-position. The Z-position
signal was employed as an indicator of changes in the vertical position of the
MTx unit, making it possible to automatically obtain the number of
completed cycles (the current standard measurement from the 30-s CST).
Information about body sway movement from the X-orientation data, and
about up and down forces from the Z-acceleration signal provided enough
556 N. Millor et al.

markers to clearly detect stand-up and sit-down events and define the
mentioned phases, figure 1.
• Third, durations and temporal kinematic parameters were extracted from the
MTx data. In particular, X-orientation, Z-acceleration and Z-velocity were
selected as the main signals related to the movement performance. The first
one informs about the way the subjects manage their body (i.e. trunk’s
forward and backward tilt), the second one about the impulse required to
reach the upright position and the third one about the speed of the movement.
A selection of thirty three parameters related to durations and directly
obtained from the MTx signals (i.e. mean, standard deviation, maximum,
minimum and range) were analyzed in terms of means for the three phases of
each cycle. Furthermore, other parameters were extracted from the MTx
information: (1) X-orientation maximum ranges (4 parameters) ; (2) the area
under the curve of the Z-acceleration data for the duration of the
corresponding stand-up and sit-down movement (6 parameters), (equation
1); and maximum and minimum peaks of the drif-free Z-velocity signal (4
parameters). In total, 48 parameters were extracted to analyze their
relationship with frailty similar to [16].
tj
AUC Zacc =  ti
a Z (t ) dt (1)

• Finally, Z-velocity pattern were obtained for a mean sit-stand-sit cycle of


frail, pre-frail and healthy groups.

3 Results

3.1 Current Test Outcome


Healthy subjects performed a significantly (p≤0.0001) greater number of sit-to-
stand cycles (10.1±3.1) during the test duration than did either pre-frail (8.3±2.4)
or frail subjects (6.6±2.4).

3.2 Durations
Duration of the cycles as well as the corresponding impulse, stand-up and sit-down
phase were able to differentiate between all groups of frail, pre-frail and healthy
subjects. Indeed this parameters were significantly greater (p≤0.0001) for the
frailest groups, table 1.

3.3 MTx Parameters


Not one of the parameters obtained from the X-orientation data was able to
differentiate the three frailty groups.
Frailty Detection Using the Instrumented Version of the 30-s Chair Stand Test 557

Maximum and minimum values of the Z-acceleration signal for both stand-up
and sit-down phases were able to differentiate between all groups. In particular,
both maximum and minimum values were significantly greater for less frailty
groups, table 1.

3.4 MTx Derived Parameters


Not one of the X-orientation maximum range parameters was able to differentiate
the three frailty groups.

Fig. 1 X-orientation signal (blue line), Z-acceleration signal (green line), and Z-position
signal (red line) from a sit-stand-sit cycle. The principal events T1, T2, T3 are also included.

Fig. 2 Z-velocity pattern for the frail (red-line), frail (blue-line) and healthy (green-line)
subjects
558 N. Millor et al.

Within the AUC parameters only the AUC+,T for the stand-up phase and AUC+,-,T
for the sit-down one were significantly higher for the frailest groups (p≤0.0001),
table 1.
Finally, only the Z-velocity maximum for the stand-up phase and the minimum
for the sit-down phase were significantly higher (p ≤ 0.001) in relation with the
frailty level. In particular, less frail subjects were not able to perform the transitions
as fast as the other groups, Table 1.

3.5 Signal Patterns


Differences were found for the Z-velocity pattern. Greater values for the Z-
acceleration peaks were observer for the healthy groups than the corresponding for
pre-frail and frail ones, fig. 2.

4 Discussion

Our analysis revealed that movement-related parameters such as the phase’s


durations and power-related magnitudes such as Z-acceleration and Z-velocity
peaks as well as certain measures of the AUCZ-acc, are able to clearly differentiate
between people belonging to different frailty groups, Table 1.
Cycles and phases durations were significantly lower for less frailty level. This
result demonstrates that frailty makes subjects perform the sit-stand-sit cycle in a
slower manner but also the subsequent phases (i.e. impulse, stand-up and sit-
down) have a reduced duration as previously signaled in [3;17].
In relation to the parameters derived from the X-orientation signal, any
significant difference was found for the three groups. This result is in accordance
with Ganea et al. who either found any difference in trunk tilt or X-orientation
range between frail and healthy subjects [17].
Parameters obtained from the acceleration signal were the ones which
demonstrate more significant differences between subjects belonging to different
frailty groups. Stand-up and sit-down phases were the ones that showed more
importance in this case. In particular, Z-acceleration and Z-velocity peaks as well
as certain AUCZ-acc values were significantly lower for frailer groups. Therefore,
this frailty group has less physical capacity to perform the stand-up and sit-down
phases of the cycles during the 30-s CST. This finding might be explained by the
fact that frail subjects have reduced power in their lower extremities, leading to a
restricted and cautious strategy for transition performance [18;19].
In summary, differences in the frailty level of a subject can be found by
evaluating the specific way the 30-s CST cycles are carried out. In particular,
parameters derived from the Z-acceleration signal were highlighted in this study
as the more prone to differentiate different frailty levels. Until now, measurements
were based on the quantity of cycles, and there was no information about the
quality of the movement performance. This results leads to a new source of
Frailty Detection Using the Instrumented Version of the 30-s Chair Stand Test 559

Table 1 Significantly different kinematic parameters(p<0.0001)

Kinematic parameters
Frail Pre-frail Healthy
Parameter Mean Mean Mean
1 1
Durations (s)
Impulse phase 1.90 1.31 1.07
Stand-up phase 1.38 1.13 0.96
Sit-down phase 1.67 1.30 1.10
Cycle 4.94 3.76 3.12
Z-acceleration
2
Max. peak|Stand-up 1.91 2.62 3.10
Max. peak|Sit-down 2.47 3.62 4.43
Min. peak|Stand-up -1.74 -2.47 -3.23
Min. peak|Sit-down -1.25 -1.90 -2.44
2
AUC|Z-acc. (m/s )
AUC+|Stand-up 0.50 0.65 0.71
T
AUC |Stand-up 1.01 1.29 1.44
AUC+|Sit-down 0.45 0.62 0.69
AUC-|Sit-down 0.34 0.49 0.58
AUCTSit-down 0.80 1.11 1.27
Z-velocity (m/s)
Max. peak|Stand-up 0.48 0.61 0.68
Min. peak|Sit-down -0.37 -0.51 -0.59
1
Standard deviation

information to outperform current clinically used test such as the 30-s CST. The
present findings motivate future investigations into these topics. Therefore, other
disabilities (i.e. risk of falls and Parkinson) as well as rehabilitation process could
be evaluated.

5 Conclusion

Kinematic parameters extracted from a single sensor located on the lower back
make it possible to differentiate subjects with different frailty levels. These results
are a preliminary step toward the development of a user-friendly and automated
560 N. Millor et al.

tool to help clinicians in assessing the 30-s CST in an objective manner based on
movement-related parameters.

Acknowledgment. The authors are indebted to the Spanish Department of Health


and Institute Carlos III of the Government of Spain [Spanish Net on Aging and
frailty;(RETICEF)], Department of Health of the Government of Navarre and Economy and
Competitively Department of the Government of Spain, for financing this research with
grants numbered RD12/0043/0022, 87/2010, and DEP2011-24105 respectively.

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[11] Boonstra, M.C., van der Slikke, R.M.A., Keijsers, N.L.W., van Lummel, R.C.,
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Frailty Detection Using the Instrumented Version of the 30-s Chair Stand Test 561

[12] Dejnabadi, H., Jolles, B.M., Casanova, E., Fua, P., Aminian, K.: Estimation and
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[13] Fuschillo, V.L., Bagala, F., Chiari, L., Cappello, A.: Accelerometry-based prediction
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1513 (1996)
An EMG Pattern Comparison of Exoskeleton
vs. End-Effector Robotic Device for Assisted
Walking Training

Giovanni Morone1,*, Marco Iosa1, Federica Tamburella1, Luca Muzzioli1,


Iolanda Pisotta1, Juan C. Moreno2, José L. Pons2, Stefano Paolucci1,
Febo Cincotti1, and Marco Molinari1
1
IRCCS Santa Lucia Foundation, via Ardeatina, 30, 00179, Rome, Italy
g.morone@hsantalucia.it
2
Bioengineering Group, Spanish National Research Council,
CSIC, Carretera Campo Real, Madrid, Spain

Abstract. Gait Trainer (GT) and the Lokomat (Loko) are two commercial robotic
devices developed for assist task-oriented, intensive practice of walking in
neurological patients. Despite the many studies involving these devices, there are
not specific studies comparing electromyography (EMG) activity during sessions
of walking training performed using these devices. This study aimed to explore the
differences in the EMG patterns between these two devices and in respect over-
ground walking. EMG of eight lower limb muscles were bilaterally recorded and
analyzed in one healthy subject. Thigh muscles were more active during GT-
session, whereas shank muscles during Loko-session. Furthermore, decreasing the
guidance assistance of Loko (i.e. the percentage of force applied by the robot in
respect to that needed for following the predetermined trajectory, training), all the
muscles showed an increment of the EMG signal. These results showed clear
differences in muscle activation patterns between the two systems and, as
expected, quite different from the pattern observed in over-ground locomotion.
These results are of importance for the correct use of robotic devices in gait
rehabilitation and would represent the preliminary step to address their correct use
in neurologically impaired subjects.

1 Introduction

The Gait Trainer (GT) and the Lokomat (Loko), are the most popular and diffused
devices to assist task-oriented, intensive practice of walking. These devices are
based on two different approaches.: Lokomat is an exoskeleton actively moving
thigh and shank by motors and passively the foot by a spring; Gait Trainer is and
end-effector device, i.e. it directly moves the feet fixed to its platforms, and thighs
and shanks are hence passively moved following the feet movements [1,2]. Both

*
Corresponding author.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 563
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_82, © Springer International Publishing Switzerland 2014
564 G. Morone et al.

the devices have a similar body weight support system. Although these two
robotic devices have been commercially available for more than 10 years, a
comprehensive characterization of robotic induced gait muscular pattern
activations is not available yet. Although Loko and GT had been built with the
idea to assist non ambulant patients affected by distinct neurological conditions –
Lokomat for Paraparetic patients and GT for Hemiparetic patients with stroke – ,
both devices are used and commercially proposed in several neurological
conditions with different functional walking status [3-6]. Experiments reporting
characterization of EMG patterns during walking training regarding a single
device comparing treadmill and over-ground walking are available [7,8] but no
studies have directly compared EMG-patterns of the same subject on Loko and
GT. Only one study have reported a kinematic comparison based on
accelerometric measures in a healthy subject demonstrating the importance
to perform training at a walking speed similar to that of normal over-ground
walking [9].
The first aim of this study was to evaluate the EMG patterns in a subject tested
with both these devices set with similar training conditions. The second aim was
to explore the effects of different amount of guidance assistance in Loko on EMG
patterns.

2 Materials and Methods

A female healthy subject was enrolled (age: 21, height: 160cm; weight: 65kg).
Twelve EMG wireless sensors (Trigno system; Delsys , Boston, USA) [10] were
bilaterally applied to: Gastrocnemious Lateralis (GASTR), Soleus (SOLEO),
Tibialis Anterior (TA), Rectus Femoris (RF), Biceps Femoris (BF) and
Semitendinosus (SEMIT), in accordance with SENIAM recommendations. Every
sensor was also used for recording kinematic data having a triaxial accelerometer
included on board. Every session lasted 1 minute. Two sessions were performed
on the Loko with 30% of Body Weight Support (BWS) and a velocity of 1.5
Km/h; first one was performed at 50% of Guidance Assistance (GA) provided by
the Loko whereas in the second one GA was set at 100%. Patients with complete
or incomplete spinal cord injury require GA settings at 50 or 100% respectively.
Thus, to allow comparison with SCI performances in future studies, data were
collected with GA set at both 50 and 100% .
One session was performed on GT with the same conditions of Body Weight
Support (30%) and same velocity (1.5 Km/h). The values of BWS (30%) and WS
(1.5km/H) were selected in accordance with the handbooks of the two devices and
guidelines for using GT [11]. In order to confront the two devices Loko
parameters were set as GT. Also overground walking was tested on a 20 meter
walking path at 1.5 km/h (subject was helped by a metronome for keeping the
right velocity). EMG signals were recorded at 2000Hz and then filtered with a
An EMG Pattern Comparison of Exoskeleton vs. End-Effector Robotic Device 565

band-pass filter between 10 and 450Hz together with a Notch band-stop filter at
50Hz. Root Mean Square (RMS) of the filtered signal were then computed for
each muscle along each entire session.

3 Results

The RMS of EMG-signals are reported in Figure 1. The muscle activity was
higher during GT-sessions than during LOKO-sessions for RF, BF, and SEMIT,
i.e. the thigh muscles. The opposite was observed for TA, GASTR and SOLEO,
i.e. the shank muscles.
Regarding the comparison of the two different percentages of guidance
assistance in LOKO, the EMG-patterns were lower for all the muscles with the
assistance of 100% in respect of that of 50%. Figure 2 shows for these two
conditions on Loko the EMG-patterns of SOLEO.

Fig. 1 EMG-RMS for Loko with 50% of guidance assistance (blue), for Loko with 100% of
gait assistance (yellow), for GT (red) and overground walking (green)

Fig. 2 EMG-RMS EMG-RMS for SOLEO in respect of the gait cycle on Loko with the
guidance assistance of 50% (blue) and 100% (red)
566 G. Morone et al.

4 Discussion

The study explored the potential differences of EMG patterns during walking
training in two different robotic devices. In depth knowledge of neurophysiological
effects of training in different robotic devices is critical for identifying patients
and/or functional status of patients who might benefit more from a specific
training/device.
Results showed ankle muscles to be more active on Loko than on GT and thigh
muscles more active on GT than on Loko. Muscle activation differences might be
explained considering differences in imposed kinematics and in force application
sites between the two devices. Furthermore, in accordance with literature [12], the
reduction of Loko-guidance assistance implied an overall increment of muscle
activity being the task more demanding.
The main limit of this study is that only one healthy subject was enrolled, but we
defined a protocol and identified potential differences between the two devices that
could imply different motor training and thus different learning processes
associated with their use. Patients might benefit differently according to their
functional deficit from one or the other device. This hypothesis has to be verified in
patients with different functional walking status and/or different frame of recovery.
Further testing in healthy subjects and in patients with stroke or spinal cord injury
are at present on-going.

Acknowledgment. The work presented here was partially supported by Italian Ministry of
Health and by SYMBITRON project which is supported by EU research program FP7,
FET-Proactive initiative “Symbiotic human-machine interaction“ (ICT-2013-10) under
project contract #611626. The SYMBITRON project is coordinated by University of
Twente.

References
[1] Masiero, S., Poli, P., Rosati, G., Zanotto, D., Iosa, M., Paolucci, S., Morone, G.: The
value of robotic systems in stroke rehabilitation. Expert Rev. Med. Devices (January
30, 2014)
[2] Iosa, M., Morone, G., Fusco, A., Bragoni, M., Coiro, P., Multari, M., Venturiero, V.,
De Angelis, D., Pratesi, L., Paolucci, S.: Seven capital devices for the future of stroke
rehabilitation. Stroke Res. Treat. 2012, 187965 (2012)
[3] Mayr, A., Kofler, M., Quirbach, E., Matzak, H., Fröhlich, K., Saltuari, L.:
Prospective, blinded, randomized crossover study of gait rehabilitation in stroke
patients using the Lokomat gait orthosis. Neurorehabil. Neural Repair 21, 307–311
(2007)
[4] Wirz, M., Zemon, D.H., Rupp, R., et al.: Effectiveness of automated locomotor
training in patients with chronic incomplete spinal cord injury: a multicenter trial.
Arch. Phys. Med. Rehabil. 86, 672–680 (2005)
An EMG Pattern Comparison of Exoskeleton vs. End-Effector Robotic Device 567

[5] Hesse, S., Werner, C., Bardeleben, A.: Electromechanical gait training with functional
electrical stimulation: case studies in spinal cord injury. Spinal Cord 42, 346–352
(2004)
[6] Morone, G., Bragoni, M., Iosa, M., De Angelis, D., Venturiero, V., Coiro, P., Pratesi,
L., Paolucci, S.: Who benefit from robotic-assisted gait training? A randomized
clinical trial in patients with subacute stroke. Neurorehabil. Neural Repair 25(7), 636–
644 (2011)
[7] Hesse, S., Uhlenbrock, D., Sarkodie-Gyan, T.: Gait pattern of severely disabled
hemiparetic subjects on a new controlled gait trainer as compared to assisted treadmill
walking with partial body weight support. Clin. Rehabil. 13(5), 401–410 (1999)
[8] Gizzi, L., Nielsen, J.F., Felici, F., Moreno, J.C., Pons, J.L., Farina, D.: Motor modules in
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[9] Regnaux, J.P., Saremi, K., Marehbian, J., Bussel, B., Dobkin, B.H.: An
accelerometry-based comparison of 2 robotic assistive devices for treadmill training
of gait. Neurorehabil. Neural Repair 22(4), 348–354 (2008)
[10] Oliveira, A.S., Gizzi, L., Kersting, U.G., Farina, D.: Modular organization of balance
control following perturbations during walking. J. Neurophysiol. 108, 1895–1906
(2012)
[11] Iosa, M., Morone, G., Bragoni, M., De Angelis, D., Venturiero, V., Coiro, P., Pratesi,
L., Paolucci, S.: Driving electromechanically assisted Gait Trainer for people with
stroke. J. Rehabil. Res. Dev. 48, 135–146 (2011)
[12] Moreno, J.C., Barroso, F., Farina, D., Gizzi, L., Santos, C., Molinari, M., Pons, J.L.:
Effects of robotic guidance on the coordination of locomotion. J. Neuroeng.
Rehabil. 10, 79 (2013)
Effectiveness of Robotic Assisted Walking
Therapy: The Role of Age and Sex

Giovanni Morone1,*, Marco Iosa2, Franco Marinozzi3, Erika D’Antonio3,


Patrizia Poli4, Stefano Masiero4, Marco Molinari2, and Stefano Paolucci2
1
IRCCS Santa Lucia Foundation, via Ardeatina, 30, 00179, Rome, Italy
and
Doctoral School, Medical Clinical and Experimental Sciences,
Neurosciences, University of Padua, Italy
g.morone@hsantalucia.it
2
IRCCS Santa Lucia Foundation, via Ardeatina, 30, 00179, Rome, Italy
3
Faculty of Biomedical Engeneering, University of Rome Sapienza, Rome, Italy
4
Rehabilitation Unit, Department of Neurosciences,
University of Padua, via Giustiniani 3, 35128 Padova, Italy

Abstract. Robotic-assisted walking training has spread in recent years with


positive results regarding its efficacy. However there are few information
regarding the target people for a more effective robotic rehabilitation. The
present study is aimed to investigate if possible demographic factors can
influence robotic-assisted walking training. The study was performed in a
neurorehabilitation setting. A total of 74 patients were randomized in robotic-
assisted gait training abbreviated conventional therapy (RAGT) and floor-assisted
gait training abbreviated conventional therapy intervention (FAGT). Outcome
measure was the walking ability measured by Functional Ambulation
Classifications (FAC). Results show that in RAGT group walking recovery was
more effective for female than males (p=0.0048) and for patients over 65 years
(≥65 yrs, p=0.040). This combined gender/age effect was not observed in FAGT
group. Among demographic factors gender and age are critical for selecting stroke
patients with higher chance of gait robotic gait therapy efficacy.

1 Introduction

Indipendent walking after stroke is the most important goal of rehabilitation with
an high impact on survivors quality of life [1].
After the limited evidence achieved by treadmill training with Partial Body
Weight observed in patients with stroke, robotic devices were specifically built for
rehabilitation. [2,3]
Among available robotic gait machines for hemiparetic patients, Gait Trainer
(GT), which controls endpoint trajectories (GT II, Rehastim, Berlin,

*
Corresponding author.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 569
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_83, © Springer International Publishing Switzerland 2014
570 G. Morone et al.

Germany)[4,5] and the Lokomat, which integrates a robotic exoskeleton on a


treadmill (Hocoma Medical Engineering Inc, Zurich, Switzerland) [5,6] are the
most widely used in Europe.
Recent studies about robotic gait training have investigated the effectiveness of
these devices [7,8] in relationship with the patient’s stroke severity. Following the
same line, it was recently investigated by our group the influence of psychological
features [9] on robotic-assisted training efficacy. However, little attention has been
placed to the patient’s demographic features like gender and age.
The aim of this study was to investigate whether and how demographic
characteristics may affect the efficacy of robotic gait training.

2 Materials and Methods


We have screened consecutive patients with recent stroke admitted to our
rehabilitation unit during the period January 2010 to March 2013. Screening was
performed during the first week of hospitalization. Inclusion criteria were:
hemiparesis in the subacute phase with significant gait deficits (Functional
Ambulation Category < 3) [10] caused by a first-ever stroke; cerebral lesions
confirmed by computed tomography or magnetic resonance imaging; age between
18 and 80 years. Exclusion criteria were: sequelae of prior cerebrovascular
accidents or other chronic disabling pathologies; orthopedic injuries that could
impair locomotion; severe spasticity that limited lower extremity range of motion
to less than 80%; sacral skin lesions; Mini-Mental State Examination score < 24;
hemispatial neglect, as evaluated by a neuropsychologist. Selected patients were
enrolled and randomized in robotic-assisted abbreviated conventional therapy
(RAGT) and floor-assisted abbreviated conventional therapy intervention (FAGT)
groups.
Subjects in FAGT group performed 2 daily session (5 times/week for 30 days)
of 40 minutes kinesio-therapy one of conventional therapy and one of gait
oriented therapy.
Subjects in RAGT group performed 2 daily session (5 times/week for 30 days)
of 40’ kinesio-therapy one of conventional therapy and one of GT therapy (20’
were allocated for the patient’s preparation, parameter setting, and 20’ for GT
treatment).
Mean and standard deviation were used to summarize the values of FAC score
among groups, whereas median and quartiles were used in figure to show the data
distribution. Non parametric inferential statistics were used. Mann-Whitney u-test
was used to compare age, time onset and effectiveness in terms of FAC-score
between groups. Effectiveness was computed as the percentage improvement in
FAC-score in respect of the maximum achievable improvement, i.e. as follows:
(dismissal score – admission score) / (maximum of scale – admission score) * 100.
FAC is a six point ordinal scale categorizing patients according to basic motor
skills necessary for functional ambulation.[10]The protocol was approved by the
local independent ethics committee, and all participants provided written informed
consent.
Effectiveness of Robotic Assisted Walking Therapy: The Role of Age and Sex 571

Partial data from the first 48 patients have been already published focusing on
who might benefit from robotic assisted training in term of patients severity [7,8].

3 Results

Seventy-four patients were enrolled and randomized in two groups, RAGT, n=38
and FAGT, n=36. These groups resulted matched for age (RAGT: 61.47±12.38
years old, FAGT: 62.31±13.36 years old, p=0.766), gender (RAGT: 27 M; FAGT:
23M; p=0.511 and time onset at admission (20.00±15.63 vs. 17.33±12.39 days,
respectively, p=0.709). The mean FAC effectiveness at dismissal resulted
statistically higher in RAGT than in FAGT: (75.00±17.77% Vs. 60.93±23.58%
respectively; p=0.0048). This significance was lost considering only male subjects
(p=0.158), while maintained considering only females (p=0.007). By grouping
patients according to age (> or < 65 years), RAGT vs FAGT FAC effectiveness
significance was maintained for elderly subjects (>65 p=0.040) but not younger
ones (<66, p=0.080).
Figure 1 shows the box whiskers plot of distribution of FAC-effectiveness.

4 Discussion

The principal result of the study is that the outcome of robotic gait training was not
affected by older age and female gender, two negative prognostic factors of
walking recovery in conventional therapy.
Eelderly patients had a significantly higher relative risk of being low responders
to conventional therapy both on mobility and activities of daily living [11]. Further,
a study found that female sex was a mildly unfavourable prognostic factor in
rehabilitation results after stroke [12]. Neither gender nor age affected the outcomes
of robotic therapy. We previously reported that best stroke candidate for GT
therapy are the more severely affected patients [7,8]. In this line, patients that are
less likely to benefit from the conventional therapy are those that present the higher
efficacy of the robotic training.
However, two important elements in our study design must be carefully
considered. As observed in a previous study, psychological factors are important
determinant of rehabilitation outcome [9] and they might be differently represent
according to gender and age. This co-factors have to be taken into consideration in
subsequent studies . For instance, it has been reported that older women are less
incline to consent to be treated with robotic devices, essentially because of a fear of
these new technologies. [7] So the women and the elderly that accepted to be
treated with Gait Trainer can be those most motivated and compliant, this might
have influenced the results. The importance of an active participation during
rehabilitation has recently been affirmed by a clinical trial [13] and in a review on
top-down approach in stroke rehabilitation [14]. The other aspect is a possible
572 G. Morone et al.

Fig. 1 Box-plot of effectiviness in terms of FAC (Functional Ambulation Classification) for


robotic-assisted gait training abbreviated conventional therapy (RAGT) and floor-assisted
gait training abbreviated conventional therapy intervention (FAGT): the boxes show the
lower quartile, median (bold line), and upper quartile values, the whiskers represent the
most extreme values within 1.5 times the interquartile range from the ends of the box,
the circles represent the outliers (data with values beyond the ends of the whiskers), n
represent the number of subjects for each group, effectiveness is the improvements
expressed in percentage of the maximum achievable improvement. Above sex comparison
(males in blue, females in pink), below age comparison (in green subjects younger than 65
years old, in grey of 65 years old or older).

ceiling-effect: we analysed the effectiveness, id est the achieved improvement in


respect of the maximum achievable improvement, and this last one could be higher
in more severely affected patients.
In conclusion, in line with the overgrowing interest in defying protocol and
patient selection to correctly tailor robotic gait therapy, present findings indicate
demographic feature represent the first step of this endeavour.

Acknowledgment. The work presented here was supported by the Italian Ministry of
Health.
Effectiveness of Robotic Assisted Walking Therapy: The Role of Age and Sex 573

References
[1] Langhammer, B., Stanghelle, J.K., Lindmark, B.: Exercise and health-related quality
of life during the first year following acute stroke: a randomized controlled trial. Brain
Inj. 22, 135–145 (2008)
[2] Sullivan, K.J., Brown, D.A., Klassen, T., et al.: Physical Therapy Clinical Research
Network (PTClinResNet). Effects of taskspecific locomotor and strength training in
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(2011), doi:10.1186/1743-0003-8-66 (review)
Cortical Contribution to Crossed Reflexes
in Walking Humans

Natalie Mrachacz-Kersting1, Sabata Gervasio1,


Dario Farina2, and Thomas Sinkjær3
1
Department of Health Science and Technology at Aalborg University,
9220 Aalborg Ø, Denmark
{nm,saba}@hst.aau.dk
2
Department of Neurorehabilitation Engineering,
Bernstein Focus Neurotechnology Göttingen,
Bernstein Center for Computational Neuroscience,
University Medical Center Göttingen, Georg-August University, Göttingen, Germany
dario.farina@bccn.uni-goettingen.de
3
Danish National Research Foundation, Copenhagen, Denmark
ts@dg.dk

Abstract. In this pilot study we investigated whether a transcortical pathway


mediates the short-latency responses elicited in the contralateral gastrocnemius
lateralis (cGL) by ipsilateral posterior tibial nerve (iPTN) stimulation. For this
purpose, single pulse sub-threshold (90% active motor threshold) transcranial
magnetic stimulation (subTMS) was applied in combination with iPTN
stimulation at several interstimulus intervals (ISI) while the subjects (n=6) walked.
SubTMS has been shown to reduce cortical output to the target muscle, inducing a
suppression in the EMG signal of the voluntary activated muscle. While no
differences were observed for the first component to the response, a considerable
depression of the second part, referred to as long-latency component (LLC) was
observed when the subTMS was timed such that the induced suppression would
coincide with this component. These results strongly suggest the cortical control
of the LLC in the cGL response. This allows for an enhanced flexibility during
unexpected perturbations, ensuring that the appropriate output is produced in
accord with the functional demand.

1 Introduction

Recent studies have identified several short-latency responses in contralateral


muscles when the ipsilateral side is perturbed either by electrical nerve stimulation
or unexpected ankle and knee joint perturbations [1;2;3]. For example, electrical
stimulation to the ipsilateral posterior tibial nerve (iPTN) at an intensity of 85% of
the maximal M-wave (85% Mmax) elicits a short-latency suppression of the
ongoing activity of the contralateral soleus (cSOL) muscle [4] and a facilitation of
the contralateral lateral gastrocnemious muscle (cGL) [3]. During dynamic tasks,

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 575
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_84, © Springer International Publishing Switzerland 2014
576 N. Mrachacz-Kersting et al.

such as walking, the size of the responses is modulated in a phase specific manner
being largest during phase transitions. This supports a functional role for such
crossed effects.
In animal studies, commissural interneurons have been identified that directly
link afferent information arising from muscle receptors to motorneurons
innervating muscle fibers located on the opposite limb [5]. In human studies such
commissural interneurons are likely to exist for two reasons. First, the onset latency
of the short-latency responses is too short for any supraspinal input. Secondly,
selective blocking of specific muscle afferents either abolishes or significantly
alters the size of the response in the contralateral muscles [1].
While in the cSOL we have documented a short lasting depression following
iPTN stimulation, the cGL has a long duration facilitation that in most subjects is
characterized by several peaks [3]. The onset of the facilitation in cGL is on
average 69.6 ms, and thus at least the first component is spinally mediated; the
second component however, is likely to have supraspinal input. Indeed a
transcortical pathway would not only signify a higher cortical control of these
crossed responses but it would ensure greater flexibility. In our previous study we
have speculated that the cGL facilitation may act to increase dynamic stability,
accelerating the propulsion phase of the contralateral leg and thus preparing for a
faster step in the event that the stimulated leg is not able to sustain the body weight.
The objective of the current study is to investigate the possibility that the latter
burst of the cGL response is mediated by a transcortical pathway and thus under
cortical control.
We applied a transcranial magnetic stimulation (TMS) using a sub-threshold
stimulus for evoking a motor evoked potential (MEP) in the cGL. This has been
shown in previous studies to lead to a suppression in the activity of the target
muscle with an onset slightly later than that of the MEP [6]. This suppression is
thought to reflect an inhibition of the cortical contribution to the EMG activity of
the target muscle. As such, since we hypothesize a cortical contribution to the
crossed response in the cGL, we expected the latter part of the crossed response to
be affected (decreased) by the sub-threshold stimulus.

2 Procedures

2.1 Subjects
Six subjects (5 males, 1 female) aged 20-29 years provided written and informed
consent to participate in this study. Approval was given by the Ethics Committee of
Northern Jutland (Reference number: N-20110040). At the time of the study, all
subjects were free of any known physical or neurological disorders.

2.2 Apparatus and Instrumentation


Surface electrodes (20mm Blue Sensor Ag/AgCl, AMBU A/S, Denmark) were
used to record the electromyographic (EMG) activity of the ipsilateral soleus
Cortical Contribution to Crossed Reflexes in Walking Humans 577

(iSOL) and the contralateral gastrocnemius (cGL) for all aspects of the
experiments. The EMG signals were amplified and band pass filtered at 20 Hz - 2
kHz and rectified. A pressure-sensitive trigger was placed under the left heel of the
subject’s shoe and used to trigger the sampling to the computer. All data were
sampled at a frequency of 2 kHz.
A Magstim 200 (Magstim Company, Dyfed, UK) with a focal figure of eight
double cone coil (110 mm diameter) was used to apply single pulses (with a
posterior to anterior directed current) to elicit a MEP in the muscle of primary
interest which was the cGL muscle.
Monopolar stimulation of the left (ipsilateral) posterior tibial nerve (iPTN) was
applied using an isolated stimulator (Noxitest IES 230), with cathode (PALs
platinum round electrode, Model No. 879100, 3.2 cm diam, Axelgaard Man)
located in the popliteal fossa and anode (PALs platinum rectangular electrode,
Model No. 895340, 7.5  10 cm, Axelgaard Man) on the anterior aspect of the knee
at the level of the patella. The cathode was adjusted to minimize the movement
artifact in the iSOL and to optimize the observed M-wave.

2.3 Experimental Procedures


Subjects were asked to walk on an instrumented split belt treadmill (Woodway) at
a self-selected walking speed. Following an initial adaptation period of 2-3
minutes, data for 20 walking cycles were collected and the average stride time
extracted. As the crossed response in the cGL has been shown to be most
prominent at 80% of the gait cycle in relation to the stride time calculated for the
ipsilateral leg [3], this time was chosen for all remaining aspects of the
experiment.
Next, the iPTN was stimulated at 80% of the gait cycle using randomized
intensities of the stimulator output. The resulting M-wave in the iSOL was
monitored online to ensure that the entire input-output relation was attained. The
maximum M-wave (M-max) was subsequently extracted and the intensity that
evoked an M-wave of 85% M-max determined. Subjects then walked again at
their preferred speed while stimuli were applied at 80% of the gait cycle at an
intensity of 85% M-Max. Stimulated steps were randomly applied with a control
condition in which no stimulation occurred. The cGL was monitored online to
extract the exact onset of the facilitatory response following the iPTN stimuli.
Subjects were seated in a chair and their vertex marked for the initial placement
of the TMS coil. Initially the stimulation intensity for the magnetic simulation was
set at approximately 50% of stimulator output to find the optimal site for evoking
a MEP in the cGL. The best spot for stimulation (also termed the hot-spot) was
taken as the coordinate where the peak to peak amplitudes of the recorded
responses from the muscle, the MEP was greater in the target muscle than
amplitudes of adjacent coordinates for a given stimulus intensity. For all subjects
this site was approximately 1-2 cm anterior to the vertex. Once the hot-spot was
identified, the coil position was maintained by markings made on the head of the
578 N. Mrachacz-Kersting et al.

subject. The coil was fixated by a custom made brace (Balgrist Tec, Zurich,
Switzerland; see [7]). This ensured that the stimulation was always applied over
the same area of the motor cortex during the dynamic task that followed.
Subjects were asked to walk again at their self-selected pace while the active
threshold (ATh), defined as the highest stimulus intensity that produced no more
than five of ten consecutive cGL MEPs with an amplitude of ~ 200 μV, was
identified. Subsequently subjects were exposed to eight conditions while
maintaining walking at the self-selected pace. Five of these involved a single TMS
delivered at 90% ATh and timed at different interstimulus intervals (ISI) in
relation to the iPTN stimulation so that suppression induced by TMS occurred at
(0 ms), or after (+10, +15, +20, +30ms) the onset of the crossed response,. Three
were control conditions in which either no stimuli occurred, only TMS was
applied or only iPTN stimuli were applied. The eight conditions were randomized
within the one walking bout lasting approximately 10 min. The time between
consecutive trials was set to 5-7 seconds and a total of 40 trials per condition were
collected.

2.4 Data Analysis


A typical response in the cGL following iPTN stimulation is shown in Figure 1B.
The red arrow in Figure 1C indicates the time at which iPTN was delivered. Data
for each individual subject was averaged across conditions and quantification of
responses performed on these averaged trials. A window commencing from the
onset of the suppression due to the subTMS until its cessation was individually
specified for each subject using the TMS only condition. Next a moving window
was applied to the five conditions where both TMS and iPTN stimuli were
applied. The respective window was moved according to the specific time delay
between onset of the suppression and onset of the crossed response; 0, 10, 15, 20
or 30ms.
The root mean square (RMS) of the signal in this window was extracted and
compared against the algebraic sum of the combined RMS value for the same time
window for the TMS only and iPTN condition. All background activity was
subtracted from these trials.

3 Results

Across all subjects the onset of the facilitatory response in the cGL was 64 ± 8 ms
and the duration 75 ± 36 ms. In all subjects at least two distinct peaks were
observed which we term the short-latency and long-latency components of the
crossed response (SLC and LLC) respectively. The peak occurrence of the SLC
was 79 ± 7 ms and for the LLC 89 ± 5 ms. The inhibition as measured from the
TMS alone condition had an onset of 41 ± 7 ms.
Cortical Contribution to Crossed Reflexes in Walking Humans 579

A iSOL EMG [μV]

500 μV
50 ms

Control Step
iPTN stimulated step

B cGL EMG [μV]

Late
component 20 μV

Early 50 ms
component

Early
component Late
component

Fig. 1 A. iSOL EMG during iPTN stimulation, B. EMG of cGL during control and iPTN
stimulated trials. C. cGL EMG during control or stimulated trials from the onset of the
stimulation until the cessation of the response. The red arrow indicates the time at which
the iPTN was delivered. All data are the average of 30 trials from one subject.

The total conduction time for a transcortically mediated pathway arising from
the iPTN stimulation is estimated to be 83 ms, considering a somatosensory evoked
potential (SEP) latency of 39 ms [8] as the afferent conduction time, the TMS
suppression latency of 41 ± 7 ms as the efferent conduction time and a central
processing delay of 3-10 ms [9;10].

3.1 Effects of SubTMS on the SLC and LLC


Results from one subject are shown in Figure 2. The onset of the cGL facilitation
occurred at 63 ms (Figure 2A) with a small initial peak followed by a larger peak
580 N. Mrachacz-Kersting et al.

iPTN alone
20μV control

60 ms

iPTN

iPTN alone
iPTN+TMS

TMS

iPTN

Fig. 2 A. The cGL EMG during control (thin trace) and iPTN stimulation (thick trace)
conditions. B: cGL EMG for iPTN stimulation alone (thick trace) and the iPTN+TMS at
that the subTMS suppression occurs 20 ms after the crossed response (thin trace) condition.
C. The two traces in B subtracted to visualize the depression in the time window also
indicated by the gray shaded area.

at 82 ms. For this subject the subTMS intensity was set to 32% of stimulator
output which corresponds to 90% ATh. When only TMS was applied, the
suppression in the ongoing activity of the cGL commenced at 41 ms and lasted for
10 ms. Data in Figure 2B show the combined iPTN and subTMS stimuli so that
the suppression elicited by subTMS occurs 20 ms after the crossed response
elicited by iPTN stimulation. A large suppression may be observed at the time of
the late peak occurrence. This is visualized in Figure 2C where the combined
condition is subtracted from the iPTN only condition.
Figure 3 shows the average data across all subjects for the combined conditions
when the subTMS suppression occurred at (0 ms), 20 and 30ms after the onset of
the crossed response. No attempt was made for statistical comparison in this pilot
study but from Figure 3 it appears that both when the subTMS suppression
Cortical Contribution to Crossed Reflexes in Walking Humans 581

occurred 20 and 30ms after the onset of the crossed response, corresponding to the
convergence with the LLC, it causes a substantial depression of the LLC while no
such effect is observed when subTMS suppression occurred at (0 ms) the onset of
the crossed response.

250
TMS alone or iPTN alone condition]
cGL response [% algebraic sum of

200

150

100

50

0
ISI = 0 ms ISI = 20 ms ISI = 30 ms

Fig. 3 The cGL response when iPTN and subTMS were applied so that suppression induced
by subTMS occurred at (0 ms), 20 and 30ms after the onset of the crossed response. Data
are for all subjects and expressed as the algebraic sum of the TMS alone and the iPTN
stimulation alone trials. The dashed horizontal line marks 100% which indicates no
difference.

4 Discussion

In this pilot study we have investigated whether the late burst observed in the cGL
following iPTN stimulation is generated by a pathway that traverses the motor
cortex. In the six subjects investigated we observed a considerable depression in the
LLC but only when the subTMS was timed such that the induced suppression
would coincide with the LLC.
TMS with intensities below ATh as applied here does not cause any descending
volleys within the spinal cord [11]. In the current study there were no observable
MEPs arising from the stimulation but only a suppression with an onset later than
the conventional MEP. It is thus justified to imply that the depression of the LLC
observed here was due to a neural pathway leading from afferents on the ipsilateral
leg that traverse the motor cortex and converge onto cGL motorneurons either
directly or via interneurons.
In all subjects we observed a suppression of the LLC, however unlike in past
studies where a similar technique has been applied to suppress ipsilateral reflex
responses [12;13], we never observed a complete suppression in any of the
subjects. This may reflect additional control mechanisms that contribute to the LLC
such as those arising from brain stem structures. In the cat, these have been shown
to converge significantly onto the commissural interneurons but also directly onto
contralateral motor neurons [14]. The residual LLC in cGL may also be due to
582 N. Mrachacz-Kersting et al.

insufficient inhibitory circuits being recruited within the motor cortex due to the
relatively weak TMS.

5 Conclusion

Although we only investigated six subjects in this pilot study, the results strongly
suggest cortical control of the LLC in the cGL. Interlimb reflexes such as those
presented here have a functional role in interlimb coordination. The cortical input
to such reflexes enhances their flexibility in ensuring that relevant output is
produced when the situation demands it.
We are currently investigating more subjects and additionally how the response
is adapted in unexpected environmental changes.

Acknowledgment. The authors would like to acknowledge support from the Obelske
Familifonden.

References
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On Electrode Configuration for Low-Back
Peripheral Nerve Field Stimulation

Carsten Dahl Mørch1, Louis Vera-Portocarrero2, and Ken Steffen Frahm1


1
Integrative Neuroscience Group, Center for Sensory Motor Interaction,
Department of Health Science and Technology, Aalborg University, Denmark
2
Neuromodulation Research, Medtronic Inc., Minneapolis, MN, USA

Abstract. Peripheral nerve field stimulation (PNFS) has been proposed as


treatment for chronic low-back pain. With this technique an electrode is implanted
in the subcutaneous tissue in the painful area. No specific nerve is isolated and the
neural target appears to be the tactile cutaneous nerve fiber branches. In order to
understand the neural mechanisms behind PNFS a mathematical model has been
proposed. The aim of the present study is to investigate the activation of tactile
Aβ-fibers and nociceptive Aδ-fibers. A finite element model of the cutaneous and
subcutaneous tissue was used to estimate the electrical field generated by two
subcutaneously implanted electrodes. The estimated electrical field was used to
estimate the activation threshold and location by a stochastically branching nerve
fiber model. The model showed that the area of Aβ-fiber activation was always
larger than the area of Aδ-fiber activation. While most electrode configurations
provided similar areas of nerve fiber activation, the guarded cathode configuration
may be slightly better than the other configurations.

1 Introduction

One fifth of the chronic pain patient in Europe experience pain originating from
the low-back, making the low-back the second most frequent location of chronic
pain (1). Many treatment options exist for treating chronic low-back pain ranging
from physiotherapy over non-steroid anti-inflammatory drugs to opioids. While
these treatments does not always provide a satisfactory pain relieving result
electrodes may be implanted for spinal cord stimulation (SCS) (2,3). While SCS
often relief pain radiating to the legs, the localized axial low-back pain often
appears more difficult to treat by SCS (4). Subcutaneously implanted electrodes
have therefore been proposed for the treatment of low-back pain (5,6). With this
technique a specific nerve is not isolated, but the small cutaneous nerve fiber
branches appears to be the neural target and the technique is therefore often
termed peripheral nerve field stimulation (PNFS). It appears that one of the most
important factors of efficient PNFS is to cover the painful area with Aβ-fiber
induced paresthesia (7). The area of paresthesia can of course be enlarged by
increasing the stimulation intensity, but the patients will not tolerate painful

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 585
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_85, © Springer International Publishing Switzerland 2014
586 C.D. Mørch, L. Vera-Portocarrero, and K.S. Frahm

stimulation caused by activation of cutaneous Aδ-fibers. To optimize PNFS


procedure and elucidate on the neural target, we previously proposed a
mathematical model for nerve fiber activation during PNFS (8). The aim of this
study was to use a similar model to investigate neural activation by commonly
used electrode configuration during PNFS for low-back pain treatment.

2 Methods

A two-step mathematical model of PNFS of the low-back similar to the one


previously presented was established (8). The model will be described in brief and
deviations will be explained buy please refer to the previously published model for
full details (8).

2.1 Volume Conductor Model


A three-dimensional FE model (Comsol Multiphysics 4.3a, Sweden) of the low-
back skin was built. The model represented a 20 x 20 cm area of the human low-
back skin consisting of three horizontal layers: skin, subcutaneous adipose tissue,
and the muscle tissue (Figure 1). Two subcutaneous electrodes were as cylindrical
electrodes with a diameter of 1.3 mm. each electrode had 4 contact areas with a
width of 6.0 mm, separated by a non-conducting spacing of 12.0 mm. The
electrodes were modelled as being parallel with an inter electrode distance of 100
mm at a depth of 10.0 mm below the skin surface.
Six different electrode configurations were modelled; ‘Short Dipole’, where two
adjacent contacts on each electrode were used as anode and cathode, ‘Medium
Dipole’ were the cathode and anode were separated by an inactive contact, ‘Long
Dipole’, where the cathode and anode were separated by two inactive contacts,
‘Guarded Cathode’ where a cathode were surrounded by two adjacent anodes,
‘Guarded Anode’ where an anode were surrounded by two adjacent cathodes, and
‘Crosstalk’ where all contact on one electrodes were set at cathodes and all contact
on the other electrode were set at anodes.

2.2 Estimation of Nerve Fiber Activation


A stochastically branching nerve fiber model previously validated for skin surface
electrical stimulation (9) was used to estimate the activation threshold for
cutaneous Aβ- and Aδ- fibers. For each electrode configuration 30000 Aβ-fibers
and 400000 Aδ-fibers were simulated to obtain a density of nerve fiber endings of
60 mm-2 and 160 mm-2, respectively (10-12). To estimate the area of paresthesia the
activation points of the nerve fibers were projected to the skin surface and the areas
of Aβ- and Aδ-fiber activation were estimated by the ‘Alpha-shapes’ methods
allowing for concavities in the areas with a curvature of 1 mm (13).
On Electrode Configuration for Low-Back Peripheral Nerve Field Stimulation 5887

Fig. 1 Finite element model of peripheral nerve field stimulation of the lower back. Thhe
skin, subcutaneous tissue an nd a muscle layer were modelled as horizontal layers. Two wiire
electrodes were modelled, in n this example with dipole stimulation on each electrode. Thhe
color bar indicates the estimmated electrical potential caused by a 1 V stimulation. The greey
tetrahedrals to the right show
ws the mesh.

Fig. 2 The location of nervee fiber activation. Cathodes are indicated by red and anodes aare
indicated by black. Nerve fibbers activated by a 5 V stimulation are indicated by small dotts;
Aβ-fibers in blue and Aδ-ffibers in green. The nerve fibers are mainly activated at thhe
cathode and some distance frrom the anode, i.e. at a virtual cathode. Please note the unequual
aspect ratio.
588 C.D. Mørch, L. Vera-Portocarrero, and K.S. Frahm

3 Results

Activation of nerve fiber occurred at the cathode or at a short distance from the
anode (virtual cathode) for all electrode configurations (Figure 2). The area of Aβ-
fiber activation was larger than the area activated by Aδ-fibers for all stimulation
intensities and electrode configurations (Figure 3). The model indicated that the
largest ratio between the area of Aβ-fiber activation and the area of Aδ-fibers
activation were similar for all electrode configurations at low stimulation intensities
(below 2V). For stimulation larger then approximately 2V the ration was lower for
the guarded anode configuration while the other configurations retain similar ratios.
For stimulations larger than 6 V the guarded cathode had the largest ratio. The
guarded cathode configuration indicated optimal stimulation intensities from 3V –
8V, whereas the other configurations have optimal stimulation intensities 2.5V –
5V (Figure 4).

Fig. 3 Top view of the peripheral nerve field stimulation model. Six different electrode
configurations are simulated. Cathodes are indicated by red and anodes are indicated by
black. Nerve fibers activated by a 5 V stimulation are indicated by small dots; Aβ-fibers in
blue and Aδ-fibers in green. Please note the unequal aspect ratio.

4 Discussion
The present study indicated that the guarded cathode configuration caused a larger
ratio between the areas of Aβ- fiber and Aδ-fiber activation. Therefore, the guarded
cathode configuration may a priori be the preferred configuration for PNFS
treatment of chronic low-back pain. Still, the differences between the stimulation
configurations may not be clinically significant. Clinical findings have shown that
On Electrode Configuration for Low-Back Peripheral Nerve Field Stimulation 5889

Fig. 4 The ratio between the area of Aβ-fibers activation and the area of Aδ-fibber
activation. The ratio was larger than one for all stimulation configureations at aall
stimulation intensities indicaation the area of Aβ-fiber activation was larger than the area of
Aδ-fiber activation.

the primary predictor for satisfactory outcome of PNFS is the paresthesia coveragge
of the painful area (7). Therefore,
T it is important place the electrode and select a
stimulation configuration that course an area of paresthesia that covers the painfuful
area.
A similar model to thee one used in the present study has been used to estimaate
optimal implantation deptth to be 1-2 cm below the skin surface (8). This estimatioon
appears to be in accordan nce with clinical findings, describing that more superficiial
implants cause painful stimulation
s whereas deeper implants are inefficient in
providing paresthesia (5).
The stochastically bran nching nerve fiber model used in the present study haas
previously been validateed for surface electrical stimulation (9). The moddel
explicitly describes the brranching anatomy of the cutaneous nerve fibers, but thhe
membrane ion currents were not explicitly modelled. This may cause som me
inaccuracy in the estimaation of thresholds and therefore also their locationns
initiation site of the nervee fiber activation (14). However, the passive nerve fiber
model was chosen to faacilitate modeling of the large amount of nerve fiber
branches in the area of thee skin where the electrodes are implanted.

5 Conclusion
The model showed that nerve
n fibers are activated adjacent to the cathode, and thhat
only small differences inn nerve fiber activation appeared between the modelleed
electrode configurations. The guarded cathode may be the initial configuratioon
when the most suitable stiimulation configuration is explored during a clinical triall.
590 C.D. Mørch, L. Vera-Portocarrero, and K.S. Frahm

Acknowledgment. The work was supported by a grant from Medtronic Inc. Drs. Vera-
Portocarrero and Mørch are lectures for ECMT-training.

References
1. Breivik, H., Collett, B., Ventafridda, V., Cohen, R., Gallacher, D.: Survey of chronic
pain in Europe: Prevalence, impact on daily life, and treatment. EJP 10(4), 287–333
(2006)
2. Kumar, K., Taylor, R.S., Jacques, L., Eldabe, S., Meglio, M., Molet, J., et al.: Spinal
cord stimulation versus conventional medical management for neuropathic pain: A
multicentre randomised controlled trial in patients with failed back surgery syndrome.
Pain 132(1-2), 179–188 (2007)
3. Chou, R., Atlas, S.J., Stanos, S.P., Rosenquist, R.W.: Nonsurgical interventional
therapies for low back pain: A review of the evidence for an American pain society
clinical practice guideline. Spine 34(10), 1078–1093 (2009)
4. Sharan, A., Cameron, T., Barolat, G.: Evolving Patterns of Spinal Cord Stimulation in
Patients Implanted for Intractable Low Back and Leg Pain. Neuromodulation 5(3),
167–179 (2002)
5. Paicius, R.M., Bernstein, C.A., Lempert-Cohen, C.: Peripheral nerve field stimulation
for the treatment of chronic low back pain: Preliminary results of long-term follow-up:
A case series. Neuromodulation 10(3), 279–290 (2007)
6. Goroszeniuk, T., Kothari, S., Hamann, W.: Subcutaneous Neuromodulating Implant
Targeted at the Site of Pain. Regional Anesthesia and Pain Medicine 31(2), 168–171
(2006)
7. Kloimstein, H., Likar, R., Kern, M., Neuhold, J., Cada, M., Loinig, N., et al.:
Peripheral Nerve Field Stimulation (PNFS) in Chronic Low Back Pain: A Prospective
Multicenter Study. Neuromodulation (2013)
8. Mørch, C.D., Nguyen, G.P., Wacnik, P.W., Andersen, O.K.: Mathematical model of
nerve fiber activation during low back peripheral nerve field stimulation: Analysis of
electrode implant depth. Neuromodulation (in press)
9. Mørch, C.D., Hennings, K., Andersen, O.K.: Estimating nerve excitation thresholds to
cutaneous electrical stimulation by finite element modeling combined with a stochastic
branching nerve fiber model. Medical and Biological Engineering and
Computing 49(4), 385–395 (2011)
10. Provitera, V., Nolano, M., Pagano, A., Caporaso, G., Stancanelli, A., Santoro, L.:
Myelinated nerve endings in human skin. Muscle & Nerve 35(6), 767–775 (2007)
11. Nolano, M., Provitera, V., Crisci, C., Stancanelli, A., Wendelschafer-Crabb, G.,
Kennedy, W.R., et al.: Quantification of myelinated endings and mechanoreceptors in
human digital skin. Annals of Neurology 54(2), 197–205 (2003)
12. Ebenezer, G.J., Hauer, P., Gibbons, C., McArthur, J.C., Polydefkis, M.: Assessment of
epidermal nerve fibers: A new diagnostic and predictive tool for peripheral
neuropathies. Journal of Neuropathology and Experimental Neurology 66(12), 1059–
1073 (2007)
13. Edelsbrunner, H., Kirkpatrick, D., Seidel, R.: On the shape of a set of points in the
plane. IEEE Transactions on Information Theory 29(4), 551–559 (1983)
14. Moffitt, M.A., McIntyre, C.C., Grill, W.: Prediction of Myelinated Nerve Fiber
Stimulation Thresholds: Limitations of Linear Models. Ieee Transactions on
Biomedical Engineering 51(2), 229–236 (2004)
Novel Approach for Investigation of Neuronal
Alterations Following Ischemic Stroke in a Rat
Model

Rasmus Kragh Nielsen and Winnie Jensen

Center for Sensory-Motor Interaction, Dept. Health Science and Technology,


Aalborg University, 9220 Aalborg, Denmark
{rkn,wj}@hst.aau.dk

Abstract. Ischemic stroke is a complex pathological trauma involving a multitude


of detrimental processes. Due to the complexity of both the neural networks in the
brain and the pathological process following stroke, novel methods to obtain
knowledge about ischemic stroke are needed. One recently suggested model is to
utilize intracortical (IC) microwire electrode-arrays to record from ischemic
cortical tissue. In the present work we report on refinements made to the model,
including design of a novel IC electrode-array and methods for quantification and
analysis of the obtained IC recordings. IC recordings were obtained from one
Sprague-Dawley rat prior to induction of ischemic stroke and in a follow-up
period of 150 min post-stroke. The results showed that the refinements of the
model resulted in a more intuitive way of interpreting the progression of ischemic
stroke. Future enhancements of the model should concern features that focus on
the spatial dynamics within the ischemia affected neural networks. In addition to
assisting in generating knowledge about the pathology of ischemic stroke the
model may be useful for optimization of rehabilitative electrical stimulation
protocols.

1 Introduction

Ischemic stroke occurs as a cascade of events, from energy depletion to cell death,
which evolve in time and space and as a consequence stroke does not affect the
ischemic region homogeneously [1]. Within a few minutes following cerebral
ischemia, the most severely affected regions; the ischemic-core (i.e. the brain
tissue which is subjected to the most dramatic blood flow reduction), is mortally
injured and becomes necrotic [2]. The ischemic-core is surrounded by a region of
less severely affected tissue; the penumbra which is initially able to sustain its
metabolic characteristics due to a sufficient blood perfusion [3]. If no treatment is
provided the penumbra will over time (within hours or a few days) progress to
infarction due to ongoing excitotoxicity, spreading depolarization, inflammation
and apoptosis [4]. Excitotoxicity is a process where the neurotransmitter glutamate
is released from damaged neurons into the extracellular space. As a consequence

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 591
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_86, © Springer International Publishing Switzerland 2014
592 R.K. Nielsen and W. Jensen

neighboring neurons depolarize and become necrotic or damaged if blood perfusion


and thus energy supply is insufficient for the neurons to repolarize. In this way,
excitotoxicity is an important trigger for both acute (necrosis) and delayed types of
cell death (apoptosis), and is related to the hyperexcitability of neural networks
which are affected by the ischemic stroke [5].
At the present time, little knowledge is available on the spatial and temporal
events that occur within ischemia affected neural networks. This inadequateness of
knowledge is mainly a consequence of: 1) the majority of studies utilizing
functional or endogenous methods to infer on the state of the affected neural
network, 2) the simplicity of methods used when analyzing data recorded via
microwire electrode-arrays inserted into the ischemic tissue ,and 3) the complexity
of the neural network within the brain and the pathology of the ischemic stroke [6].
The objective of the present study was to develop a novel approach to
investigate neuronal alterations following ischemic stroke in the sensory cortex.
The developments concerned: 1) design of an intracortical (IC) electrode-array
that enables induction of the ischemic stroke within the center of the recording site
by the photothrombosis method, and 2) quantification and analysis methods that
allow integration of spatial and temporal alterations within in the affected neural
networks. The basis of the rat model has previously been established by our group
(see e.g. [7]–[9]).
IC recordings were obtained from one rat during the acute phase of ischemic
stroke and used to verify and demonstrate the new approaches.

2 Methods
All experimental procedures were approved by the Animal Experiments
Inspectorate under the Danish Ministry of Justice (J. nr.: 2013-15-293400908).
One male Sprague-Dawley rat (450 - 500 g) was included in the experiment. The
rat was anesthetized throughout the experiment and euthanized by a lethal dose of
Pentobarbital at termination of the experiment.

2.1 Experimental Design


The pathological progression of ischemic stroke was assessed by analysis of the
evoked sensory cortical responses following electrical stimulations provided via a
cuff electrode that was inserted around the sciatic nerve. Two baseline recordings
(B1 & B2) were collected in the still healthy animal prior to induction of ischemic
stroke. Subsequently, ischemic stroke was induced within the recording site of the
sensory cortex by application of the photothrombosis method [10]. Post-stroke
recording sessions (P1 – P11) were initiated as soon as the photothrombosis
intervention was completed and the inter-recording interval was 15 min. A total of
11 recording sessions were conducted over a 2½ hours period post ischemic stroke
(fig. 1).
Novel Approach for Investigation of Neuronal Alterations 593

Fig. 1 Timeline for the experiment. Two baseline recordings (B1 & B2) were conducted
after implantation of the cuff- and IC electrode. Photothrombosis intervention was
performed and 11 post-stroke recording sessions (P1 - P11) were conducted over a 150 min
follow-up period.

2.2 Surgery and Stroke Induction


The rat was anaesthetized with a subcutaneous injection of 0.2 ml/100 g body
weight of Hypnorm-Dormicum (a cocktail of fentanyl 0.315 mg/ml, fluanisone 10
mg/ml, midazolam 5 mg/ml). A dose of approximately 0.05 ml/100 g body
weight was administrated every 30 min throughout the experiment in order to
maintain the anesthetic level. The cuff electrode (length ≈ 10 mm, φ ≈ 2 mm)
[11] was implanted around the sciatic nerve in the right hindlimb by making an
incision on the lateral surface of the hindlimb and separating the fascia between
Gluteus superficialis and Biceps femoris. When located, the sciatic nerve was
freed from the surrounding tissue and the cuff electrode was inserted around the
nerve.
Next, the IC electrode-array was implanted. The rat was placed in a stereotactic
frame and a craniectomy was performed over the hindlimb area in the sensory
cortex of the left hemisphere. The dura was removed and a 28-channel IC
electrode-array (array dimension: width = 3.35 mm, length = 3.35 mm,
electrode: φ = 100 µm, spacing ≈ 667 µm, guiding tube: φ = 1.5 mm) with a
guiding tube in the center was lowered into the cortical region that encompasses
the sensory input layer of the hindlimb area (insertion depth 1.4 mm, 0 – 3.5 mm
caudally to bregma, 0.5 - 4 mm laterally to lambda, the guiding tube did not touch
or penetrate the cortical tissue) [12], [13]. Two stainless steel bone screws served
as references during recording (fig. 2).
The ischemic stroke was induced in the center of the sensory cortical recording
site. A fiber optic light probe (φ = 1.5 mm, wavelength 560 ± 50 nm) was
lowered into the guiding tube by the use of a micromanipulator until it was
located approximately 10 mm above the surface of the cortex. A photosensitive
dye (Rose Bengal sodium salt, concentration = 20 mg dye/ml saline, injection
dose = 0.3 ml/100 g body weight, Sigma-Aldrich) was injected through a tail
594 R.K. Nielsen and W. Jensen

Fig. 2 Electrode design and implantation. The left figure shows a caudal to rostral view of
the electrode and the insertion site within the left sensory cortex. The right figure shows the
distribution of the individual electrodes of the array and the guiding tube which is located in
the center of the recording site. The two stainless steel bone screws are located furthest to
the right.

vein catheter (φ = 0.7 mm, length = 19 mm) over a 2 min timespan. The light
source was turned on upon initiation of the dye injection and it remained on for a
total of 30 min. The light causes the dye to react with the blood and cause a local,
ischemic infarct but only in the region where the light beam reaches the cortical
tissue [10].

2.3 Data Acquisition


The electrical stimulation of the sciatic nerve was controlled by a Multi-Channel
Systems STG2008. A triggering signal from the STG2008 was routed to the
Tucker-Davis Technology (TDT) system and used for offline data processing. A
single train of 240 pulses was delivered at 2 Hz (0.1 ms pulse width, 3 mA) via the
cuff electrode during each recording session.
Evoked sensory cortical responses were acquired by the TDT system (RZ2-4
basestation and PZ5-32 Neuro-digitizing pre-amplifier). Data were bandpass
filtered (700 Hz - 5 kHz) and sampled at 24.414 kHz. Neuronal spikes were
detected by applying a threshold of 2.0 x root mean square of the raw data. The
threshold was adjusted for each channel and was based on spontaneous sensory
cortex firing activity while no cuff stimulations were applied.

2.4 Data Quantification and Analysis


A Peri-Stimulus Time Histogram (PSTH) was calculated for each channel on the
basis of the recorded evoked sensory cortical responses (fig. 3.A & 3.B).
The triggering signal from the STG2008 was used as reference point for the
calculations. The maximum firing rate (spikes/s) was calculated within a time
window of 0 - 100 ms that encompasses the latency of the evoked sensory cortical
responses due to the cuff stimulations. For each channel a Poisson distribution
Novel Approach for Investigation of Neuronal Alterations 595

Fig. 3 Data quantification and analysis. (A) Evoked sensory cortical responses were
recorded via the 28 channel IC microwire electrode-array. (B) Spikes were sorted and
PSTHs were generated according to the timing of the cuff stimulations (cuff stim. timing =
0 ms). The cortical activity within the gray area encompassing the 400 – 500 ms interval on
the PSTHs was used to estimate the Poisson distribution. The upper 95% limit (dotted
horizontal line) was used to assess if the maximal evoked sensory cortical response within
the gray area encompassing the 0 - 100 ms interval was significant. (C) The SNAM depicts
the distribution of the 28 electrodes (white dots), the photothrombosis intervention site, and
the estimated distribution of the relative maximum firing rates across the electrode-array.
The black contour line encompasses the SCEA.

with upper and lower 95% confidence intervals was estimated from data recorded
over a 100 ms period just prior to the individual cuff stimulations (fig. 3.B). The
mean of the Poisson distribution was subtracted (hereby obtaining a maximum
firing rate that is relative to the baseline level) if the maximum firing rate
exceeded the upper 95% confidence limit. Channels where the maximum firing
rate did not exceed the upper 95% limit were set to zero. Next, these relative
maximum firing rates were interpolated across a two-dimensional grid that
represents the electrode-array and the area that corresponds to the
photohtrombosis induction site was extrapolated. Through this procedure a 2-D
Sensory Neuronal Activity Map (SNAM) that represents the sensory cortical
responses to the sciatic nerve stimulation was obtained (fig. 3.C).
A threshold (defined as the smallest significant relative maximum firing rate
across all channels) was used to divide the SNAM into regions of significant
neuronal activity, referred to as regions of Sensory Cortical Evoked Activity -
SCEA (fig 3.C). To quantify and compare the SCEAs we calculated the area and
the volume (calculated as the sum of neuronal activity within the SCEA area). In
addition, the global maximum and the Center of Gravity (CoG) within the SNAM
were identified.
596 R.K. Nielsen and W. Jensen

3 Results

3.1 Sensory Neuronal Activity Map


A fast and intuitive interpretation of the evoked sensory cortical responses overt
time can be made on the basis of the SNAMs. It can be observed that the region of
the sensory cortex with significant evoked neuronal responses is similar between
baselines, but decrease after photothrombosis intervention (fig. 4). Similarly, the
amount of evoked neuronal responses across the recording site seems to be similar
between baselines, but decrease post-stroke. The position of the global maximum
does not seem to change, whereas some alterations do occur to the CoG.

Fig. 4 Sensory Neuronal Activity Maps depicting the evoked sensory cortical responses.
The SNAMs based on the baseline recordings and the first two post-stroke recordings are
used as an example. The green triangle corresponds to the position of the global maximum,
whereas the gray circle is the position of the CoG within the SNAM.

3.2 Sensory Cortical Evoked Activity Area and Volume


The calculated SCEA results show that the volume and area are stable prior to
stroke (B1 & B2) but both decreased after stroke (fig. 5). The largest decline
occurred just after the photothrombosis intervention (P1) for both measures.
Following, we observed an increase in both SCEA area and volume (P2 - P3)
compared to recording P1. When looking at recording P3 – P11 the SCEA area
seems to be either stable or to have a slight tendency towards a decrease, whereas
the SCEA volume declines as a function of elapsed time from photothrombosis
intervention.
Novel Approach for Investigation of Neuronal Alterations 597

Fig. 5 Sensory Cortical Evoked Activity area and volume. The upper graph shows the
changes of the SCEA area during the experiment, whereas the lower graph shows the
changes of the SCEA volume. From the graphs it can be observed that both SCEA area and
volume were stable prior to stroke whereas both declined after stroke.

4 Discussion and Conclusion

The objective of the present study was to develop a novel approach to investigate
neuronal alterations following ischemic stroke. A new IC microwire electrode-
array that enables ischemic stroke to be induced within the center of the recording
site was successfully developed and used in the experiment. We found that the
access route for the light probe was applicable for induction of ischemic stroke
since the SNAMs, and SCEA area and volume showed alterations after the
photothrombosis intervention whereas recordings prior to stroke were similar. The
alterations of the sensory cortical responsiveness to the sciatic nerve stimulation
after ischemic stroke is in line with [14]. We found that SNAMs is a valuable tool
for fast, 2-D visual inspection of the information obtained from the IC microwire
electrode-array, since the generated maps with their features are easily
interpretable and intuitive.
The SCEA area and volume are two features which can be obtained from the
SNAMs and used in a more comprehensive statistical analysis of data, hereby
obtaining information about the global alterations within the sensory cortex
following ischemic stroke. The SCEA area describes the amount of significantly
responding sensory cortical tissue, whereas SCEA volume describes the overall
level of activity within the SCEA area.
598 R.K. Nielsen and W. Jensen

However, in order to obtain a more complete interpretation of the detrimental


effects of the ischemic stroke, spatial measures are needed due to the dynamic
nature of the pathology. As such, future works should focus on the CoG and
global maximum and in addition new features should be developed. One
possibility might be to include the distance of the electrode to the photothrombosis
induction site as a parameter when analyzing the SNAMs. This, approach has
previously been used by [14] when analyzing PSTHs from individual electrode
channels. Finally, a control group which is subjected to a placebo photothrombosis
intervention where isotonic saline is injected instead of Rose Bengal Dye should
be included in future studies. The purpose of the control group is to verify the
stability of the cortical signals over time in healthy rats. Hence, with some
additions the model may be utilized to add new knowledge about how to optimize
rehabilitative electrical stimulation protocols and obtaining valuable information
about how the ischemic injury evolves over time in both the acute and chronic
phase.

Acknowledgment. The authors wish to thank Ole Sørensen, Torben Madsen, and Jens
Sørensen for assistance during the experiment.

References
[1] Van Der Worp, H.B., Van Gijn, J.: Acute Ischemic Stroke. N. Engl. J. Med. 357, 572–
579 (2007)
[2] Woodruff, T.M., Thundyil, J., Tang, S.-C., Sobey, C.G., Taylor, S.M., Arumugam,
T.V.: Pathophysiology, treatment, and animal and cellular models of human ischemic
stroke. Mol. Neurodegener. 6(1), 11 (2011)
[3] Astrup, J., Symon, L., Branston, N.M., Lassen, N.A.: Cortical evoked potential and
extracellular K+ and H+ at critical levels of brain ischemia. Stroke 8(1), 51–57 (1977)
[4] Dirnagl, U., Iadecola, C., Moskowitz, M.A.: Pathobiology of ischaemic stroke: an
integrated view. Trends Neurosci. 22(9), 391–397 (1999)
[5] Schiene, K., Bruehl, C., Zilles, K., Qü, M., Hagemann, G., Kraemer, M., Witte, O.W.:
Neuronal hyperexcitability and reduction of GABAA-receptor expression in the
surround of cerebral photothrombosis. J. Cereb. Blood Flow Metab. 16(5), 906–914
(1996)
[6] Cheng, X., Li, T., Zhou, H., Zhang, Q., Tan, J., Gao, W., Wang, J., Li, C., Duan,
Y.Y.: Cortical electrical stimulation with varied low frequencies promotes functional
recovery and brain remodeling in a rat model of ischemia. Brain Res. Bull. 89(3-4),
124–132 (2012)
[7] Nielsen, R.K., Soerensen, K.L., Simonsen, D., Jensen, W.: Modulation of intracortical
motor cortex responses during walking in rats. In: IFESS Smart Mach. – Neural Evol.,
Banff, AB, Canada, pp. 0–3 (September 2012)
[8] Simonsen, D., Soerensen, K.L., Nielsen, R.K., Jensen, W.: Assessment of the effects
of ischemic stroke on intracortical motor cortex responses during walking in rats. In:
IFESS Smart Mach. – Neural Evol., Banff, AB, Canada, pp. 3–6 (September 2012)
Novel Approach for Investigation of Neuronal Alterations 599

[9] Nielsen, R.K., Samson, K.L., Simonsen, D., Jensen, W.: Effect of early and late
rehabilitation onset in a chronic rat model of ischemic stroke- assessment of motor
cortex signaling and gait functionality over time. IEEE Trans. Neural Syst. Rehabil.
Eng. 21(6), 1006–1015 (2013)
[10] Wester, P., Watson, B.D., Prado, R., Dietrich, W.D.: A Photothrombotic ‘Ring’
Model of Rat Stroke-in-Evolution Displaying Putative Penumbral Inversion.
Stroke 26, 444–450 (1995)
[11] Haugland, M.: A flexible method for fabrication of nerve cuff electrodes. In: 18th
Annual International Conference of the IEEE Engineering in Medicine and Biology
Society, pp. 359–360 (1996)
[12] Kolb, B., Tees, R.C.: The Cerebral Cortex of the Rat, 1st edn. The MIT Press (1990)
[13] Skoglund, T.S., Pascher, R., Berthold, C.H.: The existence of a layer IV in the rat
motor cortex. Cereb. Cortex 7(2), 178–180 (1997)
[14] Jensen, W., Rousche, P.J., Chiganos, T.C.: A method for monitoring intra-cortical
motor cortex responses in an animal model of ischemic stroke. Conf. Proc. IEEE Eng.
Med. Biol. Soc. 1, 1201–1203 (2006)
Modular Control of Gait in Incomplete Spinal
Cord Injury: Preliminary Results*

Soraya Pérez-Nombela1,**, Filipe Barroso2,3, Diego Torricelli2,


Julio Gómez Soriano4,5, Ana de los Reyes-Guzmán1,
Antonio J. del-Ama1, José Luis Pons2, and Ángel Gil-Agudo1
1
Biomechanics and Technical Aids Department National Hospital
for Spinal Cord Injury, Toledo, Spain
sperezn@sescam.jccm.es
2
Bioengineering Group (GBIO),
Spanish National Research Council (CSIC), Madrid, Spain
3
Electronics Department, University of Minho, Azurém Guimarães, Portugal
4
“Escuela de Enfermería y Fisioterapia,
Universidad de Castilla-La Mancha”, Toledo, Spain
5
Sensoriomotor Unit, National Hospital for Spinal Cord Injury, Toledo, Spain

Abstract. Muscles synergies, or motor modules, are thought to be the building


blocks of motor control in vertebrates. In human walking, experimental finding
demonstrated that 4 to 5 synergies can explain most of the variability of
electromyographic activity of lower limb muscles. How is modular control
affected in neurologically injured patients is still object of investigation. In this
paper we present preliminary experimental findings on the modular control of
walking in three incomplete spinal cord injury (SCI) patients. Results show that
the impulsive and synergistic control of muscles is preserved in these patients, and
that the basic features are in general similar to the healthy modular control, as
described in the literature. Relevant differences in timing recruitment of muscle
synergies are associated to large deviations in spatiotemporal parameters,
supporting the functional meaning of muscle synergies.

1 Introduction

The consequence of trauma in the spinal cord is a partial or complete loss of


motor, sensory and autonomic functions below the level of lesion [1]. The
interruption of the spinal interneuronal circuits connecting the brainstem and
the supraspinal motor center interfere with several aspects of normal gait [2]. The

*
This research is part of the HYPER project “Hybrid Neuroprosthetic and Neurorobotic
Devices for Functional Compensation and Rehabilitation of Motor Disorders” (Ref.
CSD2009-00067) funded by CONSOLIDER-INGENIO 2010, Spanish Ministry for
Science and Innovation.
**
Corresponding author.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 601
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_87, © Springer International Publishing Switzerland 2014
602 S. Pérez-Nombela et al.

physicians who treat acute injured spinal cord injury (SCI) patients have noted that
most of them ask whether they will walk again. It is important, therefore, to know
the probability that an acutely injured patient with incomplete tetraplegia will
become ambulatory [3]. The percentage of subjects who regain some walking
ability strongly depends on the extent of the spinal cord lesion. Gait assessment
plays an important role in the evaluation of rehabilitation process. In this scenario,
the electromyography (EMG) data may provide powerful information to explore
muscle activity changes during gait [4].
Several studies have shown that the EMG activity of trunk and leg muscles
during human locomotion can be reconstructed as a linear combination of four to
five basic modules, each one activated at a different phase of the gait cycle [5]. A
module has been hypothesized to represent a functional unit of the nervous system
that specifies functionally relevant patterns of muscle activation [6]. These
modules, also called muscle synergies, quantitatively define the groups of muscles
that are activated synchronously [7]. The activation of each synergy can be
associated with kinematic or biomechanical tasks [8]. It has been recently shown
that neurological injuries alter modular control and are associated with walking
impairments [6]. For example, it has been observed that post-stroke patients
present a lower dimensionality of motor control, i.e., a lower number of synergies,
than healthy controls [9, 10].
In SCI, gait training can be used to reeducate walking patterns by means of
kinematic references extracted from healthy subjects. Nevertheless, in patients,
muscle activation patterns utilized to generate these movements may differ
considerably from healthy subjects [11]. For this reason, it is very important to
analyze the muscle activation and relate it with kinematic outcomes. To this aim,
the analysis of muscle synergies can endows clinicians with a synthetic yet
functional analysis of muscle activation [12]. So far, only a very few studies
about muscle synergies focused in SCI patients have been found in the literature
[6, 8]. Moreover, the groups of patients in these studies were heterogeneous.
In this paper we present preliminary results supporting the hypothesis that the
modular control behind over-ground walking in incomplete SCI is affected. In
Section 2, the experimental procedure and data analysis used in this study is
described. Section 3 gives a preliminary description of the muscle control of three
patients with incomplete SCI. In Section 4 we provide a brief discussion of the
results and outline the further efforts that should be done to provide statistically
relevant evidences.

2 Material and Methods

2.1 Subjects
Three patients (see Table 1 for subject’s information) with incomplete spinal cord
injury (iSCI) participated in the experiment. We certify that all the participants
provided informed consent prior to be included in this study and that the
Modular Control of Gait in Incomplete Spinal Cord Injury: Preliminary Results 603

experimental protocol design was approved by local ethics committee. The


research was carried out in the Biomechanical and Technical Aids Department of
the National Hospital for Spinal Cord Injury (Toledo, Spain).

Table 1 Clinical Characteristics of the SCI subjects

SUBJECT SCI 1 SCI 2 SCI 3


VARIABLE
Sex Male Male Male
Age 25 36 51
Level of Lesion C4 C7 D12
ASIA score D D D
Technical aids during gait 1 crutch ----- ------

2.2 Experimental Protocol


Kinematic data were obtained using a three-dimensional motion analysis system
with two scanner units (CODA System6, Charnwood Dynamics, Ltd, UK). Eleven
active markers were positioned and attached to anatomic landmarks as described
previously [13]. Data were recorded simultaneously on both sides, with an
acquisition frequency of 200 Hz. The electromyography (EMG) data were
recorded using a 14 channels surface electromyography system (Noraxon®,
Scottsdale, Arizona, U.S.A.) with an acquisition frequency of 1500 Hz. The
electrodes were positioned as described in Cram et al. [14]. Bilateral EMG signals
were recorded for 7 muscles of the legs: gluteus medius (G), gluteus maximus
(GM), rectus femoris (RF), adductor longus (AL), hamstrings (HAM), tibialis
anterior (TA), gastrocnemius (GT). Kinematic and EMG data were synchronized
and then analyzed offline.
All patients walked with their usual footwear along a 10m walkway at self-
selected speed. Five valid gait trials were obtained for each patient. Subjects rested
for one minute between trials to avoid fatigue.

2.3 Synergy Extraction


Muscle synergies have been extracted from EMG data, according to the following
procedure. Each EMG signal was processed using a high-pass filter with a cutoff
frequency of 20 Hz, demeaned, rectified and smoothed using a low-pass filter with
5 Hz cutoff frequency. This procedure resulted in the EMG envelope [15]. EMGs
from each muscle were normalized by the average of its peaks from the 5
concatenated strides, and resampled at each 1% of the stride cycle.
Spatially fixed muscle synergies (W) and time-varying activation coefficients
(H) were extracted by a non-negative matrix factorization (NNMF) algorithm [16,
17]. As the number of synergies is an input of the NNMF, the algorithm was run
using two, three, four and five synergies, for each subject. The variability
604 S. Pérez-Nombela et al.

accounted for (VAF) [15] was calculated as a metric of the similarity between
original EMG and EMG reconstructed by multiplying matrix W by matrix H. The
optimal number of synergies required to adequately reconstruct the EMG data was
defined as the smallest number for which the overall VAF was ≥90% [6, 15].

3 Results

3.1 Spatiotemporal Parameters


As depicted in Table 2, subject 1 walked at less than the half of the speed achieved
by the other two subjects. This is reflected in most of the other spatiotemporal
parameters, such as stride length, stride time, and stride frequency. Subject 1 is
also affected by a consistent asymmetry, which is not observed in subjects 2 and 3.
In particular, subject 1 requires almost a 30% more time to perform a step with the
left leg than the right leg. Beside this greater step time, left leg contributes only to
40% of the progression, against a 60% of the right leg, forcing the right leg to
remain on the stance phase during the 84% of the stride, consistently above the
values of the other two subjects.

Table 2 Spatiotemporal parameters of SCI subjects

SUBJECT
SCI 1 SCI 2 SCI 3
SIDE Right Left Right Left Right Left

VARIABLE

0.30 0.31 0.69 0.73 0.88 0.91


Speed (m/s)
Stride length (m) 0.78 0.80 1.08 1.17 1.00 1.07
Stride time (s) 2.63 2.56 1.56 1.60 1.15 1.17
Strides/minute 22.91 23.53 38.60 37.55 52.30 51.28
Step length (m) 0.48 0.32 0.59 0.58 0.53 0.54
Step time (s) 1.13 1.43 0.79 0.81 0.59 0.58
Cadence
53.46 42.28 76.53 73.79 101.80 103.40
(steps/minute)

84.15 74.02 71.56 68.03 70.40 70.80


% Stance
Single support (s) 0.66 0.41 0.51 0.44 0.34 0.34
Modular Control of Gait in Incomplete Spinal Cord Injury: Preliminary Results 605

Fig. 1 Muscular activation patterns of each subject, averaged across 5 cycles and
normalized. Muscle abbreviations: Gluteus medius (G), gluteus maximus (GM), Rectus
femoris (RF), adductor longus (AL), hamstrings (HAM), tibialis anterior (TA),
gastrocnemius (GT).
606 S. Pérez-Nombela et al.

3.2 EMG Patterns


Figure 1 shows the mean EMG envelopes of the seven muscles of each subject.
High variability across subjects can be observed, whereas left and right sides
maintain a consistent similarity. An exception to this symmetry is the AL muscle.
In subject 1, AL activity is mostly prominent at the end of the gait cycle for the
right leg, whereas in the left leg the activity is prevalent in the first half of the
cycle. A similar behavior is observed in subject 2, even if less pronounced. In
subject 3, the most asymmetric muscle is the gluteus medius (G), which shows
very relevant activity in the left leg until 60% of the gait cycle, whereas the right
side stops before the activation, around 40% of the gait cycle.

3.3 Muscle Synergies and Activations


A variability accounted for (VAF) value higher than 90% has been obtained with
three modules in subjects 2 and 3, and a value slightly lower than 90% in subject 1
(see Figure 2). Increasing the number of modules to four produced a VAF of
approximately 95% in all subjects. We have chosen the value of four synergies in
order to allow for easier inter subject comparison.
Muscle weightings (synergies) show good similarity across subjects, and are
according to the literature [15] for healthy subjects, with some slight differences,
as following explained. The first synergy, shown in red in figure 3, is composed
mainly by activity of gluteus and rectus femoris in all the subjects and sides. There
are two exceptions. In subject 2, left side, the GM is not present, and in subject 3,
right side, the G has also very low representation. Synergy 2 (shown in violet) is
characterized by the activation of the GT in all the cases, excepting for subject 3,
right side. Synergy 3 (in blue) is characterized by the activation of the TA in all

Fig. 2 Variability accounted for (VAF) values for the three subjects and both sides. Values
are calculated as a function of the number of modules (represented in x-axis).
Modular Control of Gait in Incomplete Spinal Cord Injury: Preliminary Results 607

Fig. 3 Modular control of walking. Time-varying activations (left side of each subplot) and
muscle synergies (right side). Thin grey lines represent activation coefficients of each of the
5 cycles, with each colored thick line representing the average of those cycles.

subjects. Synergy 4 (in green) is characterized by the activation of the HA. In


subject 3, right side, the GT is also present, differently from what happens in all
the other cases. All the synergies are affected by a non consistent presence of the
AL across different synergies, which could be correlated with the very
heterogeneous behavior of this muscle across subjects, as described in the
previous section and shown in Figure 1.
608 S. Pérez-Nombela et al.

As for the time varying activation coefficients (H), all subjects showed an
impulsive behavior, meaning that the activation profiles show clear peaks and a
Gaussian-like waveform, as previously observed in healthy and stroke subjects
[18]. The relative timing of each peak is very well defined, supporting the
hypothesis that each synergy has a clear role throughout the gait cycle [19].
Nevertheless, some differences exist across subjects. In subjects 2 and 3, the
timing of the peaks matches literature data, while in subject 1 all the activation
peaks occur approximately 30% later within the gait cycle. Subject 1 also presents
a higher frequency component in the EMG envelopes with respect to the other two
subjects, whose activations appears smoother.

4 Discussion and Conclusions

The preliminary results here presented indicate that incomplete SCI subjects seem
to preserve a modular control of walking very similar to those observed in healthy
subjects. In particular, activations show a clear impulsive behavior, with a
localized relative timing of the peaks, and muscle synergies appear to contain
most of the muscles that characterize the respective synergies in normal walking.
The number of synergies is also preserved, i.e. equal to 4, even if higher values of
VAF have been observed with respect to literature. This high value of VAF can be
also explained by the low EMG samples considered in this experiment: only 5
cycles have been analyzed, meaning that NNMF algorithm can reconstruct the
variability of the signal better than when 10 to 20 cycles are considered, as
typically done in the literature. This issue also poses a question on which value of
the VAF (or other metrics of reconstruction quality) should be considered as a
confident threshold for the definition of the optimal number of synergies.
Beside this general concordance with the literature, some deviations from the
healthy behavior have been observed. The main abnormal activity is present in
subject 1, regarding the timing of activation, which are translated 30% in time
with respect to the normal values. This is likely to be associated with the abnormal
gait pattern of this subject, as reflected in the spatiotemporal parameters presented
in Section 3.1. Conversely, the same subject presents very healthy-like muscle
synergies (weightings). Subject 3 also presents some irregular synergistic pattern
in the right leg: the gluteus medius (G) and gastrocnemius (GT) muscles do not
belong to the synergy 1 and 2, but to the second and fourth synergies, respectively.
This behavior is not clear and should be explored in more detail. The final remark
is about the activity of the adductor longus (AL), which shows variable behavior
across subjects and sides. Also this aspect will be object of more focused analysis
in the future.
The results presented in this paper provide a qualitative view of the modular
control of walking in SCI subjects. Quantitative results have not been presented,
because their statistical validity cannot be demonstrated, due to the low number of
subjects considered. In order to corroborate the present findings with statistically
significant results, the analysis of further subjects is currently ongoing, also
considering healthy controls.
Modular Control of Gait in Incomplete Spinal Cord Injury: Preliminary Results 609

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EEG-Based Classification of Imagined
Arm Trajectories

Patrick Ofner and Gernot R. Müller-Putz

Institute of Knowledge Discovery, Graz University of Technology,


Inffeldgasse 13/IV, 8010 Graz, Austria
patrick.ofner@tugraz.at

Abstract. A brain-computer interface (BCI) in combination with a neu-


roprosthesis can be used to restore movement functionalities in paralyzed
persons. The BCI detects the movement imagination (MI) and the neuro-
prosthesis transforms it into a real movement. Today’s BCIs can detect the
process of MI, but not the actual imagined trajectories of, e.g., the arm.
Users’ control of a BCI would become more intuitive and natural when the
detailed MI, i.e., trajectories, are detected. This is called movement decoding.
We made a first attempt to decode MIs, and notably, we did not provoke task
depended artefacts like eye movements in our paradigm design. However, that
made it necessary to restrict the MIs to movements in two orthogonal planes.
We classified the movement plane using a decoding method. For this purpose,
we decoded the imagined trajectory and correlated it with two assumed move-
ment trajectories, and then assigned the MI to the assumed movement with
the higher correlation. That way, we reached a significant classification accu-
racy in 7 out of 9 subjects, and showed indirectly the decoding of imagined
movements.

1 Introduction
Persons with a spinal cord injury (SCI) suffer from a substantial loss of move-
ment functions. One way to restore some movement functions is the the use
of neuroprostheses based on functional electrical stimulation (FES). In very
high lesions, a brain-computer interface (BCI) might be an ideal means of
control for such neuroprostheses. Ideally, if a user imagines a certain move-
ment, the detailed and exact movement imagination should be detected by
the BCI and subsequently transformed into real movements by the neuropros-
thesis. In that way a direct link between the brain and a certain body part
(e.g. the right arm) would be restored, and a BCI user would gain control
of his/her body part again. Unfortunately, today’s systems are not sophis-
ticated enough, they do not use natural movement imaginations as control
signals, nor can they control body parts with a high degree-of-freedom.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 611
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_88,  c Springer International Publishing Switzerland 2014
612 P. Ofner and G.R. Müller-Putz

The Graz BCI group demonstrated the restoration of the lateral grasp in
a tetraplegic person’s right hand with foot MI [1], and a person with an im-
planted neuroprosthesis (Freehand system) controlled the lateral grasp with
MI of his paralyzed left hand [2]. Furthermore, hand and elbow functions have
been restored in [3, 4] recently. These non-invasive BCIs are usually based on
sensorimotor rhythms (SMR) [5] which can be deliberately modulated by MI.
Although these BCIs are controlled by MI, the MI is not natural. They detect
the process of the MI, but not the detailed MI itself, e.g. the trajectory of a
right arm MI. Such a detection of the actual MI trajectory is called decoding
and the next big step in non-invasive BCIs.
Invasive BCIs, also called brain-machine interfaces (BMIs), have already
been used to decode MIs. Collinger et al. showed recently the control of a
seven degree-of-freedom robotic arm by a person with a motor complete in-
jury due to a spinocerebellar degeneration [6]. Hochberg et al. demonstrated
the control of a robotic arm by an SCI injured person [7], and two persons
with tetraplegia due to a spinocerebellar degeneration [8]. However, invasive
BCIs have the risk of infections, and one would probably prefer an equivalent
performing non-invasive solution. Fortunately, low-frequency time-domain
signals measured non-invasively from the scalp with electroencephalogphy
(EEG) seem to provide the necessary movement information. Bradberry et
al. [9] demonstrated the decoding of three dimensional arm movements in a
center-out reaching task, and Lv et al. [10] decoded hand movements during a
drawing task. Our group showed the decoding of the position and velocity in
three dimensions of the right hand during arm movements [11]. Notably, we
did not used any targets, but a continuous, self-chosen movement task, and
we investigated longer lasting movements (1 minute each trial). In these stud-
ies, executed movements, but not imagined movements have been decoded.
Thus, the next step is to decode imagined movements. Bradberry et al. [12]
showed already the control of a computer cursor with imagined movements,
but the conclusiveness of the results is questionable [13].
When executing an decoding experiment one has to know the imagined
trajectories to train and test the decoder. However, this must be accomplished
without inducing eye artefacts, because they can affect the decoder and lead
to invalid results. This excludes now the obvious paradigm that subjects
follow a cursor on a computer screen with MI of the, e.g., right arm, because
that would induce strong eye movements. Methods exist to rid the EEG from
eye artefacts, e.g., regression methods or independent component analysis
(ICA). However, usually these methods just attenuate the influence of the eye
dipole on the EEG, but one can not be sure that they remove the influence
completely. Thus, we designed an decoding experiment where we avoided eye
movements by design.
In our decoding experiment, subjects imagined rhythmic right arm move-
ments synchronously to the beats of a metronome, and only horizontal and
vertical MIs were allowed. Due to this restrictions, we knew the imagined
EEG-Based Classification of Imagined Arm Trajectories 613

trajectories without inducing eye artefacts. We then hypothesized that the


imagined hand positions can be decoded and used to classify the movement
plane.

2 Methods

2.1 Subjects
We have recruited 9 right-handed and healthy subjects between 23 and 37
years old (4 females and 5 males) who got paid for their participation. Most
of them had already participated in BCI experiments.

2.2 Paradigm
Subjects sat comfortably in an arm chair with their hands supported by arm
rests. A computer screen was placed in front of them to display a gaze fixa-
tion cross and the cues. Subjects were instructed to either imagine repetitive
rhythmic movements from left to right and back (horizontal MI), or from bot-
tom to top and back (vertical MI), see Figure 1. The cue was an arrow point-
ing to the right informing the subjects to imagine horizontal movements, or
an arrow pointing upwards representing vertical movements. Two seconds af-
ter the cue presentation a metronome started to tick for 20 s with a frequency
of 1 Hz. Subjects were asked to imagine rhythmic, natural and round move-
ments with the extended right arm when the metronome started to tick and
to synchronize their movements with the beats of the metronome. An extreme
position of the arm, i.e. leftmost, rightmost, uppermost, bottommost, corre-
sponds to a beep of the metronome, therefore movements were imagined with
a frequency of 0.5 Hz. See Figure 2 for a visualization of the trial sequence.
We recorded 8 runs, and a run comprised 10 trials with equally distributed
classes. Thus, in total we recorded 80 trials. Additionally, we recorded eye
movements for 30 s to remove later on the influence of eye movements by
means of a linear regression method [14].

2.3 Recording
We used 68 EEG electrodes covering frontal, central and parietal areas, and 3
electrooculography (EOG) electrodes placed on the nasion and on the outer
canthi of the eyes. Reference was placed on the left mastoid, ground on the
right mastoid. We applied an 8-th order Butterworth bandpass filter (0.01 –
100 Hz) and a notch filter at 50 Hz and sampled the signals at 256 Hz.
614 P. Ofner and G.R. Müller-Putz

Fig. 1. Subjects imagined horizontal or vertical rhythmic arm movements

Fig. 2. Sequence of a trial. Within second 1.5 and 2.5 after the trial start started
the metronome to tick for 20 s.

2.4 Preprocessing
We removed muscle, eye, and technical artefacts using an independent compo-
nents analysis (ICA) [15]. Furthermore, we removed independent components
apparently common to all electrodes. Subsequently, we applied a zero-phase
anti-aliasing filter and downsampled the data to 16 Hz. Next, we filtered the
data with a 2nd order zero-phase Butterworth bandpass filter between 0.4
and 0.6 Hz as we were only interested in the EEG around 0.5 Hz. That is
because the decoding is here based on linear operations which do not change
the frequencies of signals, and therefore the usable EEG spectrum has to
be equivalent to the spectrum of the imagined movement, i.e. an imagined
arm movement with a frequency of 0.5 Hz. Afterwards, we removed remaining
eye artefacts with a linear regression method [14]. Finally, we removed sam-
ples when their absolute value exceeded a threshold of 4.4 times the median
absolute deviation (MAD). MAD is a robust variant of the standard devia-
tion measure, and the chosen threshold corresponds to 3 times the standard
deviation when the data are normal distributed.
EEG-Based Classification of Imagined Arm Trajectories 615

2.5 Classification
The classifier is based on the decoding of imagined hand positions. We de-
coded the positions in the horizontal and vertical plane simultaneously and
assigned the trial to the plane in which decoded positions correlate higher
with an assumed sinusoidal movement trajectory of 0.5 Hz, see Figure 3.
We extracted the EEG between second 2 and second 18 after the
metronome started to tick. Thus, we omitted the first and last 2 seconds
of the MI phase of a trial to avoid any transient response of the zero-phase
filter. Then the two linear models (H-model, V-model) were used to decode
the positions in the horizontal and vertical directions from the EEG. We
used the EEG at the current time step and additionally at 3 time lags (62.5,
125 and 187.5 ms) as the input to the models, see (1) (H-model) and (2)
(V-model). N is the number of channels (68), L the number of time lags (3),
T the interval between time lags (62.5 ms), Sn [t] is the preprocessed EEG
signal at electrode n and time point t. h and v are the decoded positions in
the horizontal and vertical plane, respectively. The weights of the models (a
and b) have been found with multiple linear regressions. After the positions
have been decoded in a trial within the 16 s long (trimmed) MI phase, we
correlated them with a sinus of frequency 0.5 Hz. The model which corre-
sponds to the actual MI plane should theoretically output a sinus and reach
a high correlation, whereas the other model should output noise and reach a
low correlation. Therefore, we assigned a trial to the MI associated with the
model which reached the higher Pearson correlation coefficient.


N 
L
h[t] = ah + bnkh Sn [t − kT ] (1)
n=1 k=0


N 
L
v[t] = av + bnkv Sn [t − kT ] (2)
n=1 k=0

To assess the classifier performance, we used a 10×10-fold cross-validation.


We calculated the model weights with a multiple linear regression from the
training trials, and decoded the positions and estimated the classes of the
test trials. Finally, we calculated the classification accuracy of each cross-
validation fold.

3 Results
Table 1 shows the mean values and standard deviations over the cross-
validation folds. The significance level is 59 % with α = 0.05 [16] and 7
out of 9 subjects (s1, s2, s4, s5, s7, s8, s9) reached a significant classification
accuracy. The average over subjects with a significant classification accuracy
is 67 % ± 16 %.
616 P. Ofner and G.R. Müller-Putz

Fig. 3. Schema of the classifier. The EEG was bandpass filtered, subsequently 2
linear models decoded the imagined hand positions in the horizontal and vertical
plane. The 2 decoded position trajectories were correlated with a sinus (the assumed
movement trajectory), and then the MI was assigned to the movement plane which
corresponded to the linear model yielding the higher correlation.

Table 1. Mean values and standard deviations of the classification accuracies in %.


Subjects with a significant classification accuracy are written in bold. The average
was calculated over subjects with a significant classification accuracy.

subject s1 s2 s3 s4 s5 s6 s7 s8 s9 avg

mean 65 63 53 73 62 48 66 69 75 67

std dev 15 14 17 17 16 17 16 16 14 16

Table 2. Pearson correlation coefficients when decoding a horizontal/vertical MI


with the H/V-model. Value are multiplied with 100.

subject s1 s2 s3 s4 s5

model H V H V H V H V H V

hor MI 55 46 23 15 0 6 50 9 13 -4

ver MI 46 71 20 41 9 14 7 49 -1 14

subject s6 s7 s8 s9 avg

model H V H V H V H V H V

hor MI 19 19 15 -6 39 7 49 22 29 13

ver MI 21 9 -3 15 3 31 26 62 14 34
EEG-Based Classification of Imagined Arm Trajectories 617

ver MI + V−model
ver MI + H−model
hor MI + V−model
hor MI + H−model

0.8

0.6

0.4

0.2

0
r

−0.2

−0.4

−0.6

−0.8

−1
s1 s2 s3 s4 s5 s6 s7 s8 s9

Fig. 4. Box-plot of the Pearson correlation coefficients of the trials for all subjects,
grouped by MI plane and V/H-model. A model associated to a MI should reach
higher correlations than a model not associated to a MI.

A trial was assigned to the MI plane depended on which model yields a


higher correlation. Thus, for a correct classification, the model which fits to
the MI should yield the higher correlation. This can be observed in Table 2
which shows the Pearson correlation coefficients averaged over all test trials
of a subject. Figure 4 shows a Box-plot of the Pearson correlation coefficients
for all MI plane and decoding model combinations. The correlations of the
two outermost groups of each subject should be higher than the correlations
of the two innermost groups.

4 Discussion
We demonstrated successfully the offline classification of imagined arm tra-
jectories in two orthogonal movement planes. Seven out of 9 healthy subjects
reached a significant classification accuracy. Furthermore, as our classifier was
based on movement decoding [9, 11] we showed indirectly that the decoding
of MI is basically possible.
618 P. Ofner and G.R. Müller-Putz

The control of a neuroprosthesis requires a good performance of the de-


coder, i.e. a high correlation with imagined movement trajectories, but the
correlations reached in this study are probably too low to be usably for any
direct neuroprosthesis control. In [11] we decoded executed movements and
reached correlation coefficients of 0.70 ± 0.12 (X) and 0.78 ± 0.09 (Y), which
are higher than the average correlations reached in this study 0.29 (horizon-
tal) and 0.34 (vertical). A reason could be that executed movements cause
stronger brain signals than imagined movements. Probably, also the lack of
visual and proprioceptive feedback leads to movement errors, which would
be corrected in the presence of feedback.
We applied a bandpass with a narrow passband to increase the signal-
to-noise ratio. The decoder contains only linear signal processing elements.
This implies that the decoder can not generate or delete frequencies and that
the movement frequencies must be directly presented in the EEG. Therefore,
we were only interested in the EEG at a frequency equal to the movement
frequency.
The decoding models are expected to output a sinus when a model associ-
ated MI is performed and noise when not. Therefore, the model should only
correlate with a sinus when a model associated MI is performed. However,
Figure 4 shows correlations remarkable different from zero for most subjects
when performing a model non-associated MI. This indicates that some neural
signals are common to both types of MIs, or that the beats of the metronome
induced additional common sinus oscillations. However, oscillations induced
by the metronome would not have affected the classification result, as the
physical stimulus was the same in both movement classes.
Subjects synchronized their MIs with a metronome. Although, the
metronome beats could not be accidentally classified (because they were the
same in both classes), we do not know if they are a prerequisite for the clas-
sification. They possibly caused brain oscillations which were modulated by
the MI and then decoded. Indeed, Grahn and Brett [17] and Bengtsson [18]
found that a acoustic perception of rhythms affects the activation of the mo-
tor system. Whether their is a relation or not between beat perception and
the classification presented in this work remains unknown.
It would be interesting to know the brain regions involved in the decoding
or classification, respectively. However, it is not meaningful to analyse the
regression weights of the linear models. The channels are highly correlated in
this frequency range (not shown in this work), and therefore the regression
weights can not be interpreted [19]. A solution might be to use, e.g., partial
least squares regression [20] instead of multiple linear regression when one
wants to analyze the involved brain regions.
Notably, we did not provoked task depended artefacts in our design. We
analyzed imagined movements instead of executed movements to avoid move-
ment artefacts, and we designed a paradigm which does not rely on eye
movements. Furthermore, we removed artefacts by means of an ICA and eye
EEG-Based Classification of Imagined Arm Trajectories 619

movement artefacts with a linear regression method. This makes us confident


that we actually decoded from brain sources and not artefacts.
We have shown the successful classification of the movement plane of imag-
ined arm movements. The restriction to two movement planes and rhythmic
movements was necessary to avoid artefacts. However, the generalization to
unrestricted and non-rhythmic movements remains unknown. Furthermore,
the obtained correlations are too low for direct neuroprosthesis control. How-
ever, maybe such a system can be used to detect certain types of gestures,
which would increase the control classes available to a person with SCI.

Acknowledgment. This work is supported by the European ICT Programme


Project FP7-224631. This paper only reflects the authors’ views and funding agen-
cies are not liable for any use that may be made of the information contained
herein.

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Investigate the Changes of Motor Unit
Recruitment Pattern after Stroke
Using Surface EMG

Pan Li-Ling1, Lai Meei-I1, Kao Chung-Lan2, Tsai Mei-Wun1,


Wei Shun-Hwa1, and Chou Li-Wei1,*
1
Department of Physical Therapy and Assistive Technology,
National Yang-Ming University, Taipei, Taiwan
{hope881212,unicorn30916}@hotmail.com,
{mwtsai,shwei,lwchou}@ym.edu.tw
2
Department of Physical Medicine & Rehabilitation,
Taipei Veterans General Hospital, Taipei, Taiwan
clkao@vghtpe.gov.tw

Abstract. Stroke is a major contributor of functional disability in adults. Muscle


weakness and slowness are the impairments that affect motor control primarily.
Previous studies show rate-coding pattern of motor units (MUs) altered after stroke,
which may cause slowness and weakness of muscle. However, the recruitment
pattern of MU hasn’t been well studied due to instrumental limitations. We
previously developed a new method to investigate MU recruitment using surface
EMG and turns-amplitude analysis (TAA). In this study, we used TAA to
investigate changes in MU recruitment in individuals with stroke. Six stroke
subjects and 6 control subjects (1 female) were recruited. The sEMG were
collected from tibialis anterior muscle during steady-hold and rapid isometric ankle
dorsiflexion. sEMG signals were analyzed offline using TAA. The maximal
recruitment threshold (MaxRT) between groups was compared to determine
changes in MU recruitment pattern. Results showed that MaxRT for tibialis
anterior during steady-hold contractions in stroke and control subjects were at 40%
and 50% MVC, respectively. These MaxRTs were significantly lower compared to
young subjects (70% MVC). During rapid contractions, the MaxRT of both groups
decreased to less than 20% MVC, which is also relatively lower than young
subjects. To conclude, the MU recruitment pattern is altered after stroke.

1 Introduction

Stroke is one of the major contributors of functional disability in adults. Muscle


weakness and slowness are the impairments that affect motor control primarily.
Previous studies show that rate-coding pattern of motor units (MUs) was altered

*
Corresponding author.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 621
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_89, © Springer International Publishing Switzerland 2014
622 P. Li-Ling et al.

after stroke[1][2][3][4][5][6][7], which may cause slowness and weakness of


muscle contraction[1][2]. However, the recruitment pattern of MU hasn’t been
well studied due to instrumental limitations. The maximal recruitment threshold
(MaxRT) is defined as the completion of MU recruitment in an individual muscle
and is usually presented in percentage of MVC. Both rate-coding and
recruitment modulate the force output before reaching the MaxRT[8]. However,
after the MaxRT, the force output is modulated by rate-coding solely. Since the
MU discharge rates decreased after stroke, the MaxRT of the muscle can be
affected as well. We previously developed a new method to investigate MU
recruitment using surface EMG and turns-amplitude analysis (TAA). In this
study, we used TAA to investigate changes in MU recruitment in individuals with
stroke. The finding of his study can give the information of the MU recruitment
change after stroke; furthermore, can be used in clinical practice as an assessment
of improvement after rehabilitation program.

2 Methods

2.1 Subjects
Six stroke subjects (1 female) and 6 age-and-gender matched control subjects were
recruited (Table 1). The duration since onset of stroke in stroke group is between 6
months and 5 years and receive routine rehabilitation programs regularly. The
subjects in control group maintain a regular exercise habits. sEMG signals were
obtained from the tibialis anterior (TA) muscles. In the stroke group, all of them
were in their chronic stage of stroke with mild to moderate weakness of their
affected extremities. None of them had history of other neuromuscular diseases.
The study was approved by the Institutional Review Board of Shin Kong Wu
Ho-Su Memorial Hospital and the subjects gave their informed consent prior to
participation in the investigation. All the experimental procedures were
performed in accordance with the Declaration of Helsinki.

2.2 sEMG Collection and Analysis


Subjects were seated on a secure chair and were positioned in 90-degree hip
flexion, 110-degree knee flexion and ankle in the neutral position. The foot was
secured on a customized ankle force recording device with two Velcro stripes, one
right above the ankle joint and the other around 1~2 cm proximal to
metatarsophalangeal joint. A heel block prevented sliding of the foot. The ankle
dorsiflexion torque was recorded using a force transducer (FT10, Grass
Technologies, RI, USA), which was attached to the customized ankle device.
Subjects were first asked to perform three MVCs with visual feedback of muscle
Investigate the Changes of Motor Unit Recruitment Pattern after Stroke 623

force on the screen and verbal encouragement from the experimenter. There was
a 3-minute break between each MVC attempt to avoid fatigue. The highest value
from the 3 attempts was chosen as the subject’s MVC value. Next, two different
types of isometric muscle contractions were tested: 1) steady-hold contractions and
2) rapid contractions. During steady-hold contractions, the subjects were asked to
perform isometric contractions at 10 different force levels (10%, 20%...100% MVC
with 10%MVC increment) with random order. Both visual feedback and verbal
cue were given to encourage the subjects to reach the targeted force level and hold
for three seconds. During rapid contractions, force levels at 20%, 40%, 60%, and
80% MVC were performed randomly. Subjects were encouraged to reach the
targeted force levels as fast as possible and followed by immediate relaxation;
however, accuracy was not demanded specifically during this trial. There was a
thirty-second break between each contraction and a five-minute break between the
two types of contraction trials to avoid fatigue. sEMG signals were recorded using
the fixed-disc electrodes (3cm inter-disc distance).The sEMG were collected from
TA muscle and the electrodes were placed at the proximal third of the TA muscle
and the ground electrode on the patella. Data were collected on the dominated side
of control subjects and both sides of stroke subjects. The sEMG signals were
collected using Biopac MP150 system (AcqKnowledge, BIOPAC Systems Inc,
USA). sEMG signals were analyzed offline using TAA with Spike 2 (Cambridge
Electronic Design Limited, UK.) The MaxRT was determined by changes in
TAA parameter values and was compared between stroke and control subjects to
investigate changes in MU recruitment pattern.. One of the parameters in TAA,
the number of turns per second (T/s), were found previously to be sensitive to
changes in MU recruitment. The slope of T/s-force relationship were first
calculated (Fig. 1) and the MaxRT was determined at the force level that the value
of slope drop below 2. Using an example from our previous study, the MaxRT of
adductor pollicis muscle is at about 40% MVC. (Fig. 2)

Table 1 Demongraphic data of subjects

Subject data
Items Stroke Contro

Number (M:F) 5:1 5:1


Age (year-old) 60.0 ± 61.3 ±

BMI (kg/m2) 25.6 ± 24.7 ±

Paretic side (L:R) 2:4 NA


M: male, F: female, BMI: body mass index, L: left, R: right
624 P. Li-Ling et al.

Fig. 1 The increasing in number of T/s increases linearly with force during submaximal
contraction and then plateau

Fig. 2 The slope of T/s-force relationship. The slope of 2 was used to determine the MaxRT
in muscle.

3 Results and Discussion


The number of T/s of both groups is shown in Fig. 3. The plateau of the curve can
be discover in both groups. Preliminary results showed that MaxRT during
steady-hold contractions in stroke and control subjects were at 40% and 50% MVC,
respectively. (Fig. 4) However, the slope of T/s-force relationship of 30% MVC
in stroke group is very close to the value of 2. Since there is no scientific support
for the way we picked it at present, if we use a slightly higher number, the MaxRT
may be even lower in stroke group. One outlier was found in control group which
skew the slope, therefore, more control subjects need to be recruited in order to
obtain stable data. The MaxRTs of both groups were significantly lower
compared to previous results of young subjects (70% MVC)[9]. However, the
difference between stroke group and control group is comparatively unobvious.
This result may due to the diversity of the lower extremities functional abilities
among stroke subjects. It is likely that the decrease of the MaxRT of TA during
Investigate the Changes of Motor Unit Recruitment Pattern after Stroke 625

steady-hold contractions in stroke group is caused by both aging and stroke. The
decrease of MaxRT can be the compensation for the decrease in discharge rate of
an individual MU after stroke. In order to generate a certain level of force
output, more MUs would have to be recruited to compensate for lower discharge
rate. One the other hand, during rapid contractions, the number of T/s increased
linearly with force. (Fig. 5) The MaxRT of both groups decreased to less than
20% MVC, (Fig. 6) which is also decreased in comparison with young subject
(20% MVC). However, the difference between the two groups can’t be found due
to greater intervals among different force levels tested. Overall, the early
completion of MU recruitment after stroke may decrease the efficiency of MU in
modulation force output and cause further functional impairment.

Fig. 3 The number of T/s in stroke (hollow square, dotted line) and control (filled circle, solid
line) group during steady-hold contractions. The number of T/s increases linearly at the
beginning and then plateau.

Fig. 4 The slope of T/s-force relationship in stroke and control group during steady-hold
contractions. This showed the MaxRT of TA during steady-hold contraction is at 40% MVC
and 50% MVC for stroke and control group respectively.
626 P. Li-Ling et al.

Fig. 5 The number of T/s in stroke and control group during rapid contractions. The number
of T/s increases linearly with force.

Fig. 6 The slope of T/s-force relationship of strokeand control group during rapid
contractions. This showed the MaxRT of TA during rapid contraction in both groups is less
than 20% MVC.

4 Conclusion

Based on our preliminary results, the change of number of T/s (slope) is correlated
with the MU recruitment. Moreover, we’re the first to quantify MU recruitment in
stroke. It appears that the MU recruitment pattern is affected by stroke and can be
assessed using sEMG in clinical practice. This method can be further used as an
assessment tool to evaluate the MU recruitment pattern before and after the
rehabilitation program as an indicator of improvement for individuals with
neuromuscular disorders.
Investigate the Changes of Motor Unit Recruitment Pattern after Stroke 627

Acknowledgment. The work was supported by National Science Council, Taiwan (NSC
100-2314-B-010 -003).

References
[1] Yan, K., Fang, J., Shahani, B.T.: Motor unit discharge behaviors in stroke patients.
Muscle Nerve 21(11), 1502–1506 (1998)
[2] Garland, S.J., Gray, V.L., Knorr, S.: Muscle activation patterns and postural control
following stroke. Motor Control 13(4), 387–411 (2009)
[3] Jakobsson, F., Grimby, L., Edström, L.: Motoneuron activity and muscle fibre type
composition in hemiparesis. Scand. J. Rehabil. Med. 24(3), 115–119 (1992)
[4] Frontera, W.R., Grimby, L., Larsson, L.: Firing rate of the lower motoneuron and
contractile properties of its muscle fibers after upper motoneuron lesion in man. Muscle
Nerve 20(8), 938–947 (1997)
[5] Hu, X.L., Tong, K.Y., Hung, L.K.: Firing properties of motor units during fatigue in
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Kinesiol. 16(5), 469–476 (2006)
[6] McComas, A.J., Sica, R.E., Upton, A.R., Aguilera, N.: Functional changes in
motoneurones of hemiparetic patients. J. Neurol. Neurosurg. Psychiatry 36(2), 183–193
(1973)
[7] Gemperline, J.J., Allen, S., Walk, D., Rymer, W.Z.: Characteristics of motor unit
discharge in subjects with hemiparesis. Muscle Nerve 18(10), 1101–1114 (1995)
[8] Kernell, D.: Force gradation: recruitment and rate gradation combined. In: The
Motoneurone and its Muscle Fibers, vol. 8. Oxford University Press (2006)
[9] De Luca, C.J., Erim, Z.: Common drive of motor units in regulation of muscle force.
Trends Neurosci. 17(7), 299–305 (1994)
Using Human-Computer Interface for
Rehabilitation of Activities of Daily Living
(ADL) in Stroke Patients:
Lessons from the First Prototype

Johannes Pflügler1, Andrea Schlegel1, Emilie Jean-Baptiste2, Pia Rotshtein2,


Matteo Pastorino3, Javier Rojo4, Jose Maria Cogollor4, Maria Teresa Arredondo3,
Marta M.N. Bieńkiewicz1, and Joachim Hermsdörfer1
1
Technische Universität München,
Lehrstuhl für Bewegungswissenschaft, Georg-Brauchle Ring 60/62,
80992 München, Germany
{johannes.pfluegler,joachim.hermsdoerfer}@tum.de
2
The University of Birmingham, Edgbaston,
Birmingham, B15 2TT, UK
{EMJ198,p.rotshtein}@bham.ac.uk
3
Departamento de Tecnología Fotónica,
Universidad Politécnica de Madrid, Avd. Complutense n30,
28040 Madrid
mpastorino@lst.tfo.upm.es
4
Centro de Automática y Robótica,
Universidad Politécnica de Madrid,
ETSI Industriales, 28040, Madrid, Spain
{javier.rojo.lacal,jm.cogollor}@upm.es

Abstract. Technological progress in the area of health informatics provides new


prospects for the neurorehablitation of neurological patients. The CogWatch
project (www.cogwatch.eu) is dedicated to development of automatized assistance
system to improve motor planning and task execution for stroke survivors, who
suffer from Apraxia and Action Disorganization Syndrome (AADS). The system
is targeted at promoting user independence from the therapist or care-provider
during performance of Activities of Daily Living (ADL). In this study, we present
insights from the evaluation of the first prototype interface, designed to aid users
with hot drink preparation in the kitchen environment (i.e. tea-making). Ten out of
the eleven tested participants (8 patients; 3 controls) were able to prepare the
selected cup of tea using the Cogwatch System. A case studies summary is
presented to illustrate a successful example of patient-computer interactions and a
proof of concept.

Keywords: AADS, Apraxia, Stroke rehabilitation, Cueing, ADL.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 629
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_90, © Springer International Publishing Switzerland 2014
630 J. Pflügler et al.

1 Introduction

AADS is an umbrella term that describes a compromised ability to use objects and
gestures in a goal-directed manner in a naturalistic setting [1]. Most often, AADS
is caused by damage to one of the brain hemispheres caused by cerebrovascular
accident (CVA). The classical form of apraxia is associated with left-brain damage
(LBD) and impaired knowledge to use tools in a purposeful manner, perform
multi-step naturalistic actions and communicate [2]. Action Disorganization
Syndrome affects the ability to plan multi-step actions and has is associated with
damage to the left or right hemisphere (LBD and RBD) [1, 3]. Due to AADS,
patients struggle with ADL and are prone to conceptual errors or perplexity
behavior (pause in the action execution), which limits their daily independence
and may impose safety hazard [4]. For example, patients might not be able to heat
the water to make a hot drink or cannot select the right ingredients for the task [5].
It is estimated that around 30% of CVA survivors, with traits compromising the
ability to use tools and perform ADL in the post-acute phase, have persistent
symptoms of AADS [6, 7]. The aim of the CogWatch project is to provide a
real-time prompting system that can be implemented in the home setting of
patients and promote their independence after dismissal from the hospital
facilities.

2 System Description

In the current version of the prototype interface five technological modules are
implemented: instrumented coasters, CogWatch wrist worn device (MetaWatchTM),
Kinect camera, a Virtual Task Execution (VTE) touch screen and clinician patient-
interface (CPI) (see Fig. 1, CPI not included). Instrumented tools (coaster
sensorized: milk jug, tea mug, kettle body and base) provide online information
how an object is being manipulated to a task model. In addition, a Kinect camera is
mounted over-head in relation to participant’s position to track the movement of
the hands. The task model estimates the current status of the task (e.g., making a
cup of tea) using the sensor and Kinect information as input. A wrist-worn device
can provide a vibration alert to the user when an action error is committed. The
VTE screen provides information (picture, video clip or auditory instruction) about
the appropriate next step in action execution based on the preprogrammed task
model. The CPI is a temporary solution, until the system is fully automatized. CPI
requires an input from the clinician (observing the task performance in real-time) to
recognize action subtasks being completed; pauses in the movement and AADS
errors.
Using Human-Computer Interface for Rehabilitation of ADL in Stroke Patients 631

Fig. 1 Schematic illustration of the CogWatch Prototype 1.2 System showing VTE display
(top left), Kinect Motion system (top right), wrist-watch device (bottom right),
instrumented tea-making items (bottom left and middle)

3 Evaluation

3.1 Experimental Design


The prototype test protocol includes four trials of tea-making, whereof two (2nd and
3rd trial) where performed with the prototype. All trials were performed during a
single test session. At the beginning of every trial participants were asked to choose
and prepare a cup of tea out of four different, in the prototype included variations of
tea (various additional ingredients) within a standardized tea-making setup. The
setup consisted of a cup, kettle, water, milk, sugar, lemons, tea bags and teaspoon
as well as the patient’s screen of the CogWatch prototype (see Fig. 2).

Fig. 2 Experimental setup for the tea-making task (middle), patient (bottom left), patient’s
screen – VTE (bottom right) and clinician - CPI (top right)
632 J. Pflügler et al.

A clinician used the CPI to manually feed the task-model with all required
information related to subtasks in real-time. The VTE provided participants cues,
in form of auditory information related to the current subtask. Either participants
could actively demand for this information by pressing the ‘Help’-Button on the
VTE screen or an error was detected by the system which in succession triggered
the cue. Participants were instructed to actively look at the screen if an error alert
or a cue was displayed. In addition all participants had to fill in a usability
questionnaire concerning subjective usability, workload assessments and
attractiveness of the system.

3.2 Subjects
Eight patients (mean age: 59 years; 2 left brain damage, 6 right brain damage) from
a neurorehabiltation ward (Klinikum München Bogenhausen) and three healthy
elderly controls (mean age: 50 years) were recruited for testing the prototype. All of
them performed the described tea-making tasks. Ethical approval was obtained by
local ethics committee.

3.3 Apparatus
Experimental apparatus consisted of CogWatch system components (described in
section 2.) and custom designed interface. In addition, all trials were videotaped.

3.4 Analysis
The analysis focused on errors committed by the subject during the tea-making
task and on whether the system successfully provided the proper cues to correct
those errors. For this purpose a classification of the detected errors and of the
intervention of the CogWatch system in prompting towards the goal of the
selected tea-making task was conducted. The outcomes of intervention were
classified into the following categories:
1) Successfully prompted: cues led to correction of errors; tea was prepared
as requested.
2) Partly successful: cues for certain errors were missing; tea was prepared
with minor changes (e.g. wrong amount of certain ingredient).
3) Not successful: Participant did not react to cues or a fatal error occurred
(irreversible in terms of failing to achieve task goal) (e.g. putting cold
water into a mug with teabag in).

4 Results
In the trials that were performed with the CogWatch system, six out of the nine
participants who committed at least one error were successfully cued and achieved
Using Human-Computer Interface for Rehabilitation of ADL in Stroke Patients 633

Fig. 3 Distribution of all participants according to their performance (error occurrence)


and the overall outcome after system intervention (cueing)

the task goal (the selected cup of tea). Two participants did only partly achieve
their action goal (e.g. too little of certain ingredient) but were still able to prepare
the selected cup of tea. Only one out of the 11 participants was unable to finish his
cup of tea due to an irreversible fatal error (Fig.3).
The application of the system was successful for example in one patient with
RBD who was unable to use the necessary objects in the right order when trying to
make a cup of tea. With the CogWatch system made available she frequently
demanded help by pressing the corresponding key when she was stuck or unsure in
her task execution. In these cases the task model cued the correct actions and the
patient responded appropriately. Accordingly she finished to prepare the cup of tea
successfully only when using the system. All other participants did not actively use
the VTE screen to demand for help, but still were cued by the system after an error
was detected. In case of the two patients whose outcome is described as partly
successful the system did not have relevant cues for their errors. An example for
this was to not put as much hot water into the cup as one could regard as normal. A
cue like ‘there is not enough hot water in the cup yet’ for such estimation error was
missing in the task-model at this point of time. Hence the general result is a
correctly prepared cup of tea with minor changes in quantity of a single ingredient.
Regarding the possibility of multiple errors during a single trial an overall
number of 39 errors were detected during evaluation (Fig. 4). Thereof 16 (41%)
errors were prompted successfully, 15 (38%) errors were not included in the
CogWatch task model, 5 (13%) cues alerting errors were disregarded and 3 (8%)
fatal errors occurred.
634 J. Pflügler et al.

Fig. 4 Graphical summary of system interventions with regard to patients’ errors

Although - except for one patient - all could prepare the selected cup of tea with
the help of the CogWatch prototype, no improvement in performance during 4th
trial, following the two prototype trials could be observed. Subjects who were
unable to prepare the demanded cup of tea in the beginning, were neither able to do
so after prototype trials. Preliminary results of the ongoing usability investigation
look promising in terms of system stability and user friendliness. So far suit those
of a control group without cognitive impairment also tested with the Cogwatch
System [8]. During evaluation in this study all patients rated the system as useful
and easy to handle, with two of them already asking if it is available for home
setting. Extensive results on usability in a living assistance domain are in process to
be published [9].

5 Technological Challenges

Major steps in development of the CogWatch-System have been accomplished


successfully. Still, this first field test with CVA-patients indicates the demands for
further adjustments. As obvious from the outcome of this evaluation, it is of major
importance to supplement the existing task-model with additional yet missing cues
for certain errors. This step will be critical for the upcoming integration of the
automatized action-recognition which will replace the supervision by the clinician.
In addition, patients tested were heterogeneous, with respect to associated
neurological deficits among which attention deficits or language disorders are the
most relevant. It seems highly desirable to personalize the system so that each
patient gets the best fit of cues matching his/her needs.

6 Conclusions

Currently new prototype versions are being developed –in parallel with present
prototype dedicated to facilitate the action of tooth-brushing. The evaluation of the
first version of the prototype revealed that human computer interface can provide
Using Human-Computer Interface for Rehabilitation of ADL in Stroke Patients 635

an effective guidance for CVA patients to perform an ADL task without assistance
of a therapist or care-provider. Further development is necessary to fully
automatize the system to enable operation without the need for clinician
supervision. In addition, we have identified a need to personalize the sensory and
guidance modes for different users, due to the other co-morbidity symptoms that
might accompany AADS, such as aphasia or visual neglect. This test has not
revealed whether repeated interaction with CogWatch system may restore the
function to perform the ADL task without additional help. Further research is
necessary to define whether restoration of function can be achieved or whether
the main application of the system is an assistive function supporting tasks that the
patients can not complete successfully and safely on their own. One of the
technological and conceptual challenges of the project is to provide a fully-
customizable interface that can be tailored to the capacities and training needs of
AADS patients. Regarding a possible long-term integration of the Cogwatch
System into daily life it will likewise be necessary to extend evaluation to real
home settings and adjust the design to users’ needs.

Acknowledgment. This work was funded by the EU-STREP Project CogWatch (FP7-ICT-
288912). Authors would like thank the patients of the Clinic for Neuropsychology at the
Klinikum München-Bogenhausen for participation in the research and the head of the clinic
Prof. Goldenberg as well as the other staff members for their support.

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Evaluation of a New Exoskeleton for Upper
Limb Post-stroke Neuro-rehabilitation:
Preliminary Results

Elvira Pirondini1, Martina Coscia1,2, Simone Marcheschi3, Gianluca Roas3,


Fabio Salsedo3, Antonio Frisoli3, Massimo Bergamasco3, and Silvestro Micera1,4
1
Translational Neural Engineering Laboratory,
Center for Neuroprosthetics and Institute of Bioengineering, School of Engineering,
École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland
elvira.pirondini@epfl.ch
2
Neuroscience Institute, Consiglio Nazionale delle Ricerche (CNR), Pisa, Italy
martina.coscia@epfl.ch
3
PERCRO, Scuola Superiore Sant’Anna, Pisa, Italy
{s.marcheschi,g.roas,f.salsedo,
a.frisoli,m.bergamasco}@sssup.it
4
Biorobotics Institute, Scuola Superiore Sant’Anna, Pisa, Italy
silvestro.micera@epfl.ch

Abstract. Exoskeletons are becoming very popular for the rehabilitative treatment
of post-stroke subjects. The aim of this study was to characterize the effect of a
new light upper limb exoskeleton on the movement execution and muscular
activity during reaching movements in healthy subjects. The results show that the
exoskeleton used in the passive modality supports the upper limb reducing
the muscular activity of the shoulder’s muscles and increasing the activity of the
elbow flexors, without interfering with the movement execution. Our preliminary
analysis on healthy subjects supports the use of this new exoskeleton for post-
stroke robotic-rehabilitation.

1 Introduction

Stroke is the leading cause of adult disability in western countries [1].


Impairments in reaching movements are among the most common consequences
of stroke. Upper limb functions are altered in the 73-88% of first time stroke
survivors, and in the 55-75% of chronic post-stroke patients [2, 3].The upper limb
impairments mainly consist in an increased spasticity [4], lack of mobility
between structures at the shoulder girdle [5], predominance of stereotypic
movement patterns [6, 7], loss of inter-joint coordination and reduced range of
motion [8].
Systematic reviews suggested that the efficacy of post-stroke motor therapy is
related to the level to which the neuromuscular system is challenged by repetitive

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 637
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_91, © Springer International Publishing Switzerland 2014
638 E. Pirondini et al.

movements [9]. In the last decades, robotic-based rehabilitation became very


common because it can provide intensive and highly repeatable therapy, which
can be varied by the physiotherapist in order to continuously challenge the
patient’s neuromuscular system.
Among the robotic devices for upper limb rehabilitation, the exoskeletons have
the advantage with respect to operative systems of assisting the user during the
execution of wide movements. They are wearable mechatronic systems with the
human-machine interface extended to the entire limb: they can be designed to
follow the anatomy of the limb and to cover many degrees of freedom (DoFs).
Therefore, they allow the independent control of each articular joint and/or they
guide the limb during complex movements requiring multi-joints coordination
[10]. The major limits of the existing exoskeletons are the consistent weight and
dimensions that often restrict the training workspace and augment the complexity
of the control to compensate the high inertia.
Recently, the PERCRO (PERCeptual RObotics) laboratory of Scuola Superiore
S. Anna (Pisa, Italy) has developed a novel exoskeleton for the upper limb (Arm
Light Exoskeleton, ALEx) [11], expressly conceived for the force assistance of
stroke patients during robotic-rehabilitation. The device is characterized by the
low encumbrances, mass and inertia of its moving parts, the low friction of the
actuation system and the large workspace for the movements of the upper limb.
The aim of this study was to assess the effects of ALEx on movement
execution and muscular activity in healthy subjects, in order to evaluate its
application for post-stroke rehabilitation. In particular, we focused on the
influence of the system on the end-effector kinematic, to test if it compromises the
natural movement execution, and on the muscle coordination, to test if it modifies
the strategy adopted by the subjects while reaching.

2 Methods

2.1 Exoskeleton Description


ALEx is a mechanically compliant powered exoskeleton for the upper limb with 6
DoFs: 4 DoFs are sensorized and actuated (3 DoFs at the shoulder and 1 DoF at
the elbow) and 2 DoFs at the wrist are only sensorized (Fig. 1). The mechanical
compliance of the device has allowed implementing a highly robust force control,
without using costly and low reliable force sensors. It measures positions and
velocities at the end-effector and at each articular joint (sample frequency from
100 Hz to 1 kHz). It allows performing wide 3D movements in two different
modalities: passive (i.e., the subject moves the upper limb and the robot measures
the movement) and active (i.e., the robot guides the upper limb of the subject
during movement execution).
Evaluation of a New Exoskeleton for Upper Limb Post-stroke Neuro-rehabilitation 639

2.2 Participants and Motor Task


Six right-handed healthy young subjects (1 female, 5 males, average age 26.5±3.4)
were enrolled in the study. They did not present any evidence or known history of
skeletal or neurological diseases, and they exhibited normal joint range of motion
and muscle strength.
The subject seated behind a target panel frame, with the center of the target
panel aligned with the acromion of the right arm. The distance between the subject
and the panel corresponded to the subject's arm length. The panel frame contained
twelve targets arranged in a clock-like fashion, placed 20 cm from its center. The
starting position was located mid-way between the center of the target panel and
the acromion, at the same high. The subjects had to reach from the starting
position each of the twelve targets on the target panel frame and to come back
from each target to the starting position with the occurrence of a metronome tone.
Each forward and backward movement was constrained by the beat of the
metronome at a frequency of 40 beats per minute (bpm), which corresponds to a
movement speed of 0.23 m/s. The metronome rhythm was chosen as a
low/moderate speed in order to resemble the reaching speed of post-stroke
subjects, but also to allow the healthy subjects to execute the movements in a
natural way. The task (i.e., reaching of the 12 targets in a random order) was
repeated 3 times (i.e., in total 36 movements). Firstly, the subjects performed the
reaching movements wearing the exoskeleton (condition “with” the exoskeleton)
and later without the robotic device (condition “without” the exoskeleton). In the
first condition, the exoskeleton was used in the passive modality, therefore it was
not assisting the user, but it was only measuring the execution of the movement. In
this modality, the weight, the friction and the inertia of the exoskeleton were
compensated by the control’s software. Before starting the experiment, a test for
the maximum voluntary contraction (MVC) was performed for each muscle.

Fig. 1 ALEx, the new Arm Light Exoskeleton [11]


640 E. Pirondini et al.

2.3 Kinematic Recordings


In the condition “without” the exoskeleton, the kinematics was acquired by using
a six-camera motion analysis system (Vicon Oxford Metrics Ltd, Oxford, UK) at
100 Hz. Fourteen spherical markers were placed on specific body landmarks: one
marker along the body midline (C7 vertebra) and 13 markers on the right upper
arm (anterior superior iliac spine, shoulder acromion, lateral and medial
epicondyle of the humerus, three midpoints between shoulder acromion and lateral
epicondyle, radial styloid process, ulnar styloid process, midpoint between lateral
epicondyle and ulnar styloid process, and metacarpophalangeal joint of the little
finger, third finger, and thumb). The subjects held a cylinder with a marker placed
on the top, to mimic the exoskeleton’s handle.

2.4 EMG Recordings


The EMG signals from 16 upper limb muscles (deltoid anterior, DANT, medial,
DMED, and posterior, DPOS, pectoralis major, PEC, latissimus dorsi, LAT,
infraspinatus, INFRA, rhomboid major, RHO, pronator teres, PRO, biceps brachii
short head, BICS, biceps brachii long head, BICL, brachialis, BRA,
brachioradialis, BRAD, lateral head of triceps brachii, TRILAT, long head of
triceps brachii, TRILONG, superior trapezius, TRAPS, medial trapezius,
TRAPM) were recorded by using superficial Ag-AgCl electrodes (Kendall
H124SG, ECG electrodes 30x24 mm). The skin was cleaned and shaved, and the
electrodes were placed, when it was possible, according to the standard procedure
for surface electromyography for non-invasive assessment of muscles (SENIAM)
guidelines [12]. The EMG signals were acquired by using a wireless Noraxon
Desktop DTS system.

2.5 Kinematic Analysis


To segment the data related to each target and to compute the kinematic
parameters, we used the trajectory of the marker on top of the cylinder in the
condition “without” the exoskeleton, and the trajectory of the end-effector
recorded by the exoskeleton in the condition “with” the exoskeleton. The start and
end points of each center-out or out-center reach were defined as the time points
when the speed exceeded or dropped below 2% of the local maximum or
minimum value of the speed profile.
To evaluate the movement execution, for each target, three parameters were
computed: (1) the mean distance (nMD), defined as the mean absolute distance
between the trajectory and the straight line connecting the starting position with
the target, normalized to the length of the theoretical path [13]; (2) the Pace,
defined as the difference between the actual speed and the speed required to
follow the metronome tone; (3) the number of peaks in the speed profile (nPK),
quantifying the smoothness of the movement [13].
Evaluation of a New Exoskeleton for Upper Limb Post-stroke Neuro-rehabilitation 641

2.6 EMG Pre-processing and Comparison


The raw EMG signals were detrended, high-pass filtered at 50 Hz (Butterworth
filter, 7th order), rectified and low-pass filtered with a cut-off frequency of 10 Hz
(Butterworth filter, 7th order). Finally, the EMG signals were normalized for the
MVC value.
In order to estimate changes of muscle activity due to the use of the
exoskeleton, the root mean square (RMSEMG) of each condition and the Pearson's
correlation coefficient between the two conditions (REMG) were computed.

2.7 Muscle Synergies Extraction, Ordering, and Comparison


Muscle synergies were extracted separately for the conditions “with” and
“without” the exoskeleton by pooling together the normalized EMG signals
corresponding to the 12 forward and backward movements in the 3 repetitions.
The non-negative matrix factorization (NNMF) algorithm was used [14]: each
extraction was repeated 50 times, and the repetition with the solution explaining
the highest overall amount of EMG variance was selected. The number of retained
synergies was the number at which an R2 >70% was achieved [15]. The same
number of muscle synergies was retained for all subjects to allow an easy intra-
group comparison.
To simplify the visualization and the comparison, the muscle synergies between
the conditions “with” and “without” the exoskeleton were matched according to
the degree of similarity on their weighting coefficients measured by using the
scalar products (DOT>0.49).
The similarity in shape and amplitude of the timing coefficients between two
muscle synergies were assessed by using the Pearson’s correlation coefficient (R)
and the root mean squared value (RMS), respectively.

2.8 Statistics
The effect of the use of the exoskeleton on movement execution (nMD, Pace, and
nPK), on muscle activity (RMSEMG), on each muscle contribution to the
weighting coefficients, and on the timing activation of muscle synergies (RMS)
were assessed using a t-test for repeated measures (α=0.05). The analyses were
performed by using custom routines written in Matlab environment (Mathworks
Inc., Natick, MA, USA).

3 Results
The end-effector kinematics was generally maintained across the two conditions
(Fig. 2). The accuracy (nMD) was in general higher for the condition “with” the
exoskeleton, in particular it was significantly higher for the targets 2, 3, 4, 7, 8, 9,
10, and 12 (p<0.05). The pace (Pace) and the smoothness (nPK) were comparable
642 E. Pirondini et al.

Fig. 2 Evaluation of the movement execution "with" and "without" the exoskeleton. The
averaged mean distance (nMD), pace (Pace), and number of peaks in the speed profile
(nPK) are represented for each target (each mean value refers to 6 subjects and 3
repetitions of forward and backward movements). Red and blue lines code the condition
“with” and “without” exoskeleton. * indicates a significant difference between the two
conditions (p<0.05).

in the two conditions. In the condition “with” the exoskeleton, the pace was
significantly lower for the target 9, while the smoothness was significantly lower
in the target 7 and 12 (p<0.05). The smoothness was lower in the condition “with”
the exoskeleton also in the target 1 and 6. However, statistical analysis did not
reveal significant trends due to the high variability among subjects.
Some muscle groups (in particular, the postural muscles in the back and the
elbow flexors) presented differences in amplitude and timing between the two
conditions (Fig. 3). Concerning the amplitude, the RMSEMG highlighted a higher
activity of DANT, LAT, BRA, TRILAT, TRILONG, DMED, and DPOS in the
condition “without” the exoskeleton; whereas the RMSEMG of INFRA, RHO,
BICS, BICL, BRAD, and TRAPM was significantly higher for the condition
“with” the exoskeleton (Fig. 3). Concerning the timing (REMG), it was preserved
between the two conditions for the DANT, PEC, BRA, TRILAT, TRILONG,
TRAPS, and TRAPM. The muscles that presented a major different timing
modulation between the two conditions were i) the postural muscles in the back
(RHO, LAT, INFRA) and the flexors of the elbow (BICS, BICL), in which in
general the activation was higher in the condition "with" the exoskeleton except
than for the LAT, and ii) the PRO, in which the activation using the exoskeleton
was lower (Fig. 3).
Muscle synergies analysis was performed to assess possible effects of the use
of the exoskeleton on muscle coordination. Eight muscle synergies were extracted
for each subject for both conditions (R2>0.7, 8±1 for condition “with” the
exoskeleton and 8±0.5 for condition “without” the exoskeleton, Fig. 4). Six
muscle synergies matched in the two conditions (DOT>0.49): S1 and S6 grouped
the muscles dedicated to the control of the shoulder (i.e., DMED and DPOS), S2
and S3 mainly involved DANT and PEC, S4 accounted for the contribution of
BICS and PEC in the backwards movements, and S5 represented the contribution
of the muscles in the back. The weighting coefficients and the timing activation of
the common synergies (S1-S6) were similar in the two conditions.
Evaluation of a New Exoskeleton for Upper Limb Post-stroke Neuro-rehabilitation 643

Fig. 3 Muscle activity “with” and “without” the exoskeleton. On the left, the pre-processed
EMG signals averaged among 6 subjects, 12 targets, and 3 repetitions are reported for both
conditions. Red and blue lines code the condition “with” and “without” the exoskeleton. On
the x-axis the duration of the movement is represented in percentage, and it includes the
forward and backward movement. On the top right, the root mean square (RMSEMG) of
EMG signals for each condition is reported. On the bottom right, the Pearson’s correlation
coefficient (REMG) between the two conditions is reported by using black bars. In both
cases, each bar represents the average across 6 subjects, 12 targets, and 3 repetitions (mean
± SE). * indicates significant difference between the two conditions (p<0.05).

Fig. 4 Muscle synergies “with” and “without” the exoskeleton. On the left, the weighting
and the timing coefficients of the muscle synergies are represented for both conditions. On
the right, the RMS and the R (calculated only for the matched synergies) are respectively
reported on the top and on the bottom. Red and blue bars code the condition “with” and
“without” the exoskeleton. The mean and standard errors refer to 6 subjects, 12 targets, and
3 repetitions. For the timing coefficients, on the x-axis, the duration of the movement is
represented in percentage, and it includes the forward and backward movement. * indicates
significant differences between the two conditions (p<0.05).
644 E. Pirondini et al.

Among the contributions of the muscles in each weighting coefficient only


TRAPM in S1 had a weighting coefficient > 0.3 [16] and a significant difference
between the two conditions (p<0.05). The amplitude of the timing coefficients was
significantly but slightly higher in the condition “with” the exoskeleton, except in
S3. R was low for S4 and S5, where the activity was almost constant in the two
conditions, and in S6, where the activation was higher in the condition “with” the
exoskeleton during the forward movement to the targets. In the condition "with"
the exoskeleton, the control of the elbow flexion was predominant on the postural
control: the two muscle synergies including LAT, and DMED and DPOS in the
condition "without" the exoskeleton (S9 and S10, respectively), were substituted
by two muscle synergies accounting for BICS and BICL (S7 and S8, respectively).

4 Conclusion

Our results show that the use of ALEx in the passive modality does not interfere
with the movement execution: it favors the execution of straight and smooth
movements in different directions, even following the pace of a metronome.
The muscle activity and coordination are slightly modified by using the
exoskeleton. In particular, the decreased activity of postural muscles of the
shoulder and their contribution to movement execution are substituted by an
enhanced activity of the elbow flexors. This result can be due to the support
provided by the exoskeleton to the shoulder joint and to a not optimal
compensation of the friction in the elbow joint.
In conclusion, ALEx seems a promising exoskeletric device for neuro-
rehabilitation; however an improvement in the compensation of the weight,
friction, and inertia at the elbow joint is required and further investigations on the
joint kinematics and on post-stroke subjects are necessary to confirm our
preliminary results.

References
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[16] Sabatini, A.M.: Identification of neuromuscular synergies in natural upper-arm
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Experimental Architecture to Analyse
Brain Signals during Walking

Daniel Planelles, Álvaro Costa, Andrés Úbeda,


Eduardo Iáñez, and José Marı́a Azorı́n

Biomedical Neuroengineering Group,


Miguel Hernández University,
Elche, CP 03202 Spain
dplanelles@umh.es

Abstract. In this paper, the complete set up used to perform several walking
experiments are shown. A Brain Machine Interface (BMI) system is used
to record Electroencephalographic (EEG) signals from the cerebral cortex
of the subject. EEG signals are analysed in order to study the cognitive
mechanisms related to self-adjustments or attention during walking and to
decode the locomotion. Moreover, a group of Inertial Measurement Units
(IMUs) are used to know the gait kinematics and to a better understanding
of correlation between electrophysiological and biomechanical data.

1 Introduction
In the short term, wearable robots (WRs) will be used to assist some daily
functions as walking. WRs are usually in the form of exoskeletons which
can be worn by humans. The exoskeleton is an external structural mecha-
nism with joints and links corresponding to those of the human body. This
transmits torques from proximally located actuators through rigid exoskele-
tal links to the human joints. Thus, the mobility or motor rehabilitation of
injured patients can be improved by using exoskeletons.
Therefore, robotic lower limb exoskeletons hold significant potential for
gait assistance and rehabilitation. Currently, some researches as the project
BETTER [1] and the project HYPER [2] have designed lower limb exoskele-
ton to assist gait rehabilitation of injured patients. However, exoskeletons
still induce fixed and somewhat nonvolitional motion patterns on its user.
This paper is performed as part of the project BioMot - Smart Wearable
Robots with Bioinspired Sensory-Motor Skills (FP7-ICT-2013-10) funded by
the Commission of the European Union. Project BioMot is focused on under-
standing motor primitives through the analysis of neurophysiological, biome-
chanical and perceptual responses using WRs during human locomotion. The
main objective of the project is to improve existing wearable robotic exoskele-
tons exploiting dynamic sensorimotor interactions and developing cognitive

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 647
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_92,  c Springer International Publishing Switzerland 2014
648 D. Planelles et al.

capabilities that can lead to symbiotic gait behaviour in the interaction of


a human with a wearable robot. Therefore, the experimental architecture of
this paper will be used to analyse gait processes with electrophysiological and
biomechanical representations and taking into account aspects of cognitive
function during walking.

2 Proposed Experimental Procedures


2.1 Cognitive Mechanisms Related to
Self-adjustments during Walking
This task is focused on studying, with a noninvasive technique, the cogni-
tive mechanisms related to the initiation and the termination of the gait,
and changes in direction/orientation during walking in healthy people. This
way, the electroencephalographic (EEG) signals of healthy volunteers will be
registered during real walking. The EEG signals will be analysed in order to
detect the intention of the initiation/termination of the gait, self-adjustments
of the gait speed and cadence, and the change in direction/orientation dur-
ing walking before they actually happen [3]. Thus, this information could be
used to manage a symbiotic control of the WR and to monitor the opera-
tors’ performance. To develop this task, the Event Related Desynchronization
(ERD) phenomenon that is found in the mu and beta frequency range dur-
ing movement will be used [4], previously removing the artifacts from the
EEG signals [5, 6]. Other phenomenon related to motor preparation, called
Bereitschaftspotential [7], will be considered.

2.2 Decoding of Locomotion during Walking from


EEG Signals
The goal of this task is to decode the information of locomotion during walk-
ing in healthy people from the EEG signals. Concretely, the goal is to infer
from EEG signals information about the gait kinematics during walking. The
EEG signals will be analysed in order to define a model that establishes a re-
lationship between the gait kinematics and the EEG signals [8, 9]. Thus, this
model could be used for partial control of the WR locomotion. The common
methodology applied for decoding, among others, is the multidimensional
linear regression. It will be applied according to the formula:


N 
L
x [t] = a + bnk Sn [t − k] (1)
n=1 k=0

Where x[t] is the kinematics state (ankle, knee or hip angle) at time t and
Sn is the voltage measured at electrode n. L are the number of lags and N
Experimental Architecture to Analyse Brain Signals during Walking 649

the number of channels. a and b, are the decoding parameters. Previously,


EEG signals and hand kinematics is filtered between 0.1-2 Hz (low frequency
components) and, afterwards, EEG data from each electrode is standardized
by subtracting, for each time sample (t), the mean (V̄ ) of the signal and
dividing the result by the standard deviation (SDV ).

2.3 Cognitive Attention Mechanisms Contributing to


Stability and Adaptation to Environment
This task is focused on studying the attention mechanisms contributing to
stability and adaptation to environment of people during walking using a
non-invasive technique. Thus, the EEG signals of healthy people will be reg-
istered during realistic walking considering changes of environment. The EEG
signals will be analysed in order to determine the degree of human attention
on walking and to detect changes of environment. This way, the WR con-
trollers could be automatically adapted to the environment. One hypothesis
to develop this task is to analyse the changes in Error-related EEG Potential
(ErrP) amplitudes [10]. ErrP appears when something behave different than
expected for a user, so when an obstacle appears or the environment change
it can be detected. There are not many studies on this research field, so other
hypothesis will be considered as frequency analysis and systems based on
classifiers.

3 Experimental Setup
The system architecture is composed of a Brain-Machine Interface (BMI)
that will capture and process EEG signals to command the exoskeleton and
seven Inertial Measurement Units (IMUs) managed by the Motion Capture
System of Technaid company, which will be distributed over the lower body
to register kinematics. Moreover, a treadmill will be used to obtain stable
and controlled velocity walking in some of the studies.

3.1 Brain-Machine Interface


Brain signals are acquired using the two commercial amplifiers g.USBamp
of the g.Tec company with the g.GAMMAcap, which has active electrodes
to increase signal/noise ratio. The amplifiers are synchronized by using
g.INTERsync and they have two preamplifiers g.GAMMAbox. The acqui-
sition of EEG signals is done using 32 electrodes with a sampling frequency
of 1200 Hz. The electrodes are placed over the scalp with the following distri-
bution: FZ, FC5, FC3, FC1, FCZ, FC2, FC4, FC6, C5, C3, C1, CZ, C2, C4,
C6, CP5, CP3, CP1, CPZ, CP2, CP4, CP6, P3, P1, PZ, P2, P4, PO7, PO3,
POZ, PO4 and PO8, according to the International System 10/10 (Fig. 1).
650 D. Planelles et al.

Fig. 1 Placement of 32 electrodes over frontal and parietal lobes

Moreover, a reference electrode placed on right ear lobe and a ground elec-
trode on AFz are used. This distribution has been chosen to cover all the
relevant surface of the scalp and, particularly, the regions where motor activ-
ity, ERD and ErrP occurs. The EEG signals are internally 100 Hz low-pass
filtered and a 50 Hz Notch filter is applied to remove the power line interfer-
ence. In order to facilitate the free movement of the user, g.INTERsync and
both g.GAMMAbox and g.USBamp are put into a backpack (Fig. 2).

3.2 Motion Capture System


The motion capture system Tech MCS is a complete wireless motion analysis
system. It manages the seven IMUs of the company Technaid which are used
in our experiments (Fig. 3). Each Tech IMU integrates three different types
of sensors as an accelerometer, a gyroscope and a magnetometer. A sophis-
ticated and robust algorithm, calibrated also taking into account changes in
temperature, results in a very precise and robust estimation of 3D orientation,
even during changing environmental conditions.
Experimental Architecture to Analyse Brain Signals during Walking 651

Fig. 2 The structure with all devices which is tucked inside the backpack and
cap with 32 EEG electrodes. The user has to wear the backpack to perform the
experiment (top). Devices to register EEG signals (bottom).
652 D. Planelles et al.

Fig. 3 A: Inertial Measurement Unit (IMU) from Technaid. B: Tech Hub that
manages all IMUs. The user is wearing seven IMUs, right and left quadriceps,
biceps and ankle and another one in the lumbar (top).
Experimental Architecture to Analyse Brain Signals during Walking 653

Fig. 4 Treadmill has 2.25 CV and the possibility to change tilt up to 10 %

3.3 Treadmill
To decode the movement from EEG signals or study the cognitive attention,
the Pro-Form Performace 750 treadmill is used (Fig. 4). The treadmill allows
controlling velocity and it makes easier to perform normal gait than when
walking freely where the cadence is not controlled by an external system.

Acknowledgment. This research has been funded by the Commission of the Eu-
ropean Union under the BioMot project - Smart Wearable Robots with Bioinspired
Sensory-Motor Skills (Grant Agreement number IFP7-ICT-2013-10-611695), by the
Spanish Ministry of Economy and Competitiveness as part of the project DPI2011-
27022-C02-01, and by Conselleria d’Educació, Cultura i Esport of Generalitat Va-
lenciana of Spain through grant VALi+d ACIF/2012/135.
654 D. Planelles et al.

References
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Adapted to Stroke Rehabilitation Practice. In: World Congress on Medical
Physics and Biomedical Engineering (2012)
2. Bortole, M., del-Ama, A.J., Rocon, E., Moreno, J.C., Brunetti, F., Pons, J.L.:
A Robotic Exoskeleton for Overground Gait Rehabilitation. In: 2013 IEEE
International Conference on Robotics and Automation (ICRA), May 6-10, pp.
3356–3361 (2013)
3. Velu, P.D., de Sa, V.R.: Single-trial classification of gait and point movement
preparation from human EEG. Frontiers in Neuroscience 7, 1 (2013)
4. Pfurtscheller, G., Lopes da Silva, F.H.: Event-related EEG/MEG synchroniza-
tion and desynchronization: basic principles. Clinical Neurophysiology 110(11),
1842–1857 (1999)
5. Akhtar, M.T., Mitsuhashi, W., James, C.J.: Employing spatially constrained
ICA and wavelet denoising, for automatic removal of artifacts from multichan-
nel EEG data. Signal Processing 92(2), 401–416 (2012)
6. McFarland, D.J., McCane, L.M., David, S.V., Wolpaw, J.R.: Spatial filter se-
lection for EEG-based communication. Electroencephalography and Clinical
Neurophysiology 103(3), 386–394 (1997)
7. Shibasaki, H., Hallett, M.: What is the Bereitschaftspotential? Clinical Neuro-
physiology 117, 2341–2356 (2006)
8. Presacco, A., Goodman, R., Forrester, L., Contreras-Vidal, J.L.: Neural decod-
ing of treadmill walking from noninvasive electroencephalographic signals. J.
Neurophysiol. 106, 1875–1887 (2011)
9. Úbeda, A., Hortal, E., Iáñez, E., Planelles, D., Azorı́n, J.M.: Passive robot assis-
tance in arm movement decoding from EEG signals. In: 6th Anual International
IEEE EMBS Conference on Neural Engineering, pp. 895–898 (2013)
10. Ferrez, P.W., Millán, J.R.: Error-Related EEG Potentials Generated During
Simulated Brain-Computer Interaction. IEEE Transactions on Biomedical En-
gineering 55(3), 923 (2008)
Processing EEG Signals to Detect
Intention of Upper Limb Movement

Daniel Planelles, Enrique Hortal, Eduardo Iáñez,


Álvaro Costa, and José Marı́a Azorı́n

Biomedical Neuroengineering Group,


Miguel Hernández University, Elche, CP 03202 Spain
dplanelles@umh.es

Abstract. In the world there is a large number of people who have trouble
performing movements that are simple for others, such as people who have
suffered a stroke or have damage in the spinal cord. However, thanks to
neuroscience, there is knowledge about the cognitive processes that occur
in the brain and it is possible to help these people by using brain-computer
interfaces. In this paper the movement of the arm of a healthy person is under
research. Different processing methods and classifiers are studied in order to
obtain the minimum false positive rate with the best true positive rate to
detect the intention to make such movement in future real time tests. The
ultimate goal is to use this system with an exoskeleton attached to the user
arm. Thus, these kind of disabled people will perform movements on their
own will by activating the exoskeleton joints. This system could be used in
motor rehabilitation processes since it would allow the patient to recover the
damaged communication channels of the brain or create new ones due to
brain plasticity.

1 Introduction
In view of the increasing requirements for improving the daily life of disabled
people, a lot of studies are trying to develop systems for this purpose. There
are already systems that allow reducing the effect of the different types of
disabilities such as a navigation system for assisting blind people [1] and a
web browser controlled by ocular movements [3], but there is still much to be
done. In this work, we give our attention to people with physical disability
since they usually cannot fend for themselves because their mobility is really
limited. Mainly, we intend to give them a way to move their limbs and to
improve their rehabilitation as part of the project Brain2Motion.
Electroencephalographic (EEG) signals collected from the cerebral cortex
have been used to learn about cerebral processes. The cerebral cortex central-
izes and interprets sensations, makes conscious responses, controls voluntary
movements and it is the seat of consciousness, memory and intelligence [2].

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 655
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_93,  c Springer International Publishing Switzerland 2014
656 D. Planelles et al.

For decades, scientists thought the brain’s networks became fixed but, in
recent years, researchers have discovered the concept of neuroplasticity. It
means that our brains can be rewired and adjusted. Therefore, brain signals
have begun to be used in motor rehabilitation [4, 5].
A Brain-Computer Interface (BCI) is used to manage EEG signals. A BCI
is a hardware and software communications system that allows collecting
cerebral activity to control computers or external devices [6, 7]. This work is
one of the first steps in developing a complete system based on a phenom-
ena called Event-Related Desynchronization (ERD) that occurs just before
starting a movement [8]. This phenomena is described by a decrement in the
spectral power of mu and beta frequency bands (8-30 Hz) mostly in signals
recorded over frontal and parietal lobes that begins up to 2 seconds prior the
movement onset.
Our system will consist of a BCI that will capture the ERD process and an
exoskeleton that will be attached to the arm of the disabled. An exoskeleton
is an articulated system that can have several engines to move them. Con-
sequently, the arm of the disabled will be displaced when the engines move
the joints. Lastly, ERD will be used to control the joints of the exoskeleton.
In this experiment, data registered from two sessions with a healthy user
performing arm extension movements are processed and classified. The aim
is to find a method to obtain a good detection index using a single model
or multiple models to define the classifier. Moreover, two spatial filters and
different kind of classifiers will be checked. In the future, the engines of an
exoskeleton or a control based on Functional Electrical Stimulation (FES)
will be managed with the classifier output that it is obtained in this kind of
ERD-based system.

2 Materials and Methods


2.1 Registration
The BCI implemented to detect movement intention consists of a non-invasive
system. The signals are acquired using the commercial amplifier g.USBamp
of g.Tec company with g.GAMMAcap which has active electrodes to increase
signal/noise ratio. The acquisition of EEG signals is done using 16 electrodes
placed over the scalp with the following distribution: Fz, FC5, FC1, FCz,
FC2, FC6, C3, Cz, C4, CP5, CP1, CP2, CP6, P3, Pz and P4, according to
the International System 10/10. A sample frequency of 256 Hz has been used.
In order to register the position of the arm in a 2D space, the user has
to move a mouse. The position of the mouse in the screen of the interface
determines the beginning and also the phase of the movement. A frequency
sample of 16 Hz to register the mouse position is used. The complete set up
is shown in Fig. 1.
Processing EEG Signals to Detect Intention of Upper Limb Movement 657

Fig. 1 Experimental set up

2.2 Experimental Procedure


The test was done by one healthy subject in an isolate room to prevent noise
and distraction. Human data presented in this article have been acquired
under an experimental protocol approved by the ethics committee in the
experimental research department of the Miguel Hernandez University of
Elche, Spain. Written consent was obtained from each subject. The subject
was instructed to perform an extension movement with the mouse in his hand
and then to return to the initial position. A graphical interface was used to
guide the subject on each performance and it is used to separate the data
between resting and movement time. The interface shows a cross for 5 seconds
when the subject must remain at rest with the cursor at the bottom of the
screen, after that, a point is shown for 5 seconds. During this period, the
subject should freely make a movement and go back to the initial position.
No sound or instruction about the exact time to perform the movement have
been indicated to the user, so the registered EEG signals does not correspond
to any evoked potential, only to the ERD. The subject has performed two
sessions. One of them consisted of 8 runs that last 160 seconds each, i.e.,
16 movements. In the other one, 6 runs of 260 s each without any cue were
performed where the subject could carry out movements whenever he wanted
658 D. Planelles et al.

but he was instructed to remain at rest at least 5 seconds between movements.


The total of movements was 125, one each 12,48 seconds. The first session is
used to train classifiers whilst the second one is used to test them.
arm forward/backward movement

2.3 Data Selection


In this study two states will be considered: rest and pre-movement/movement.
The EEG data are fed into the classifiers using a 1 second sliding window
without overlap. Windows of pre-movement are those that start 1 second
prior to the onset movement sample obtained with the mouse position. Rest-
ing data are those between 1 second after the end of the movement and 1
second before the next movement. In overlapping windows between resting
and pre-movement, the window is discarded. Thus, the number of instances
of each class will be different and higher in resting class.

2.4 Signal Processing and Features Extraction


The whole EEG data in both sessions are pre-processed with a notch filter in
50 Hz to eliminate the electrical network noise and a bandpass filter between
5 and 40 Hz is applied to remove some high frequency artifacts and also
the DC component. Afterwards, a spatial filter is used in all EEG channels
to reduce the contribution of the remaining electrodes in each channel. In
this work, the spatial filter is a variable of study and it will be tested using
a Surface Laplacian (LAP) filter and a Common Average Reference (CAR)
(for details refer [9]).
Once the data selection has been done, each window selected is processed
with a Fast Fourier Transform (FFT) to know its spectral power. The features
are the sums of three frequency bands, 8-12 Hz, 13-24 Hz and 25-30 Hz per
each electrode which represents mu and beta bands, so 48 features define
each instance of the class.

2.5 Classifiers
There are several classifiers normally used in BCI based systems [10]. In this
study we will use Support Vector Machine (SVM) and K Nearest Neighbours
(KNN).
As it has been mentioned above, two spatial filters will be considered.
Moreover, two methods to determine the classifier will be examined. On the
one hand, the 8 runs of the training session are used to create a unique
model considering all pre-movements and resting windows selected. On the
other hand, a set of 8 classifiers formed from all the possible combinations
of 7 runs is also used. The idea is to find the best option to detect a
Processing EEG Signals to Detect Intention of Upper Limb Movement 659

pre-movement/movement and 8 classifiers allow us to manage a new param-


eter to make a final decision.
The classifiers chosen are:
1. Least Square (LS) SVM, Radial Basis Function (RBF) kernel with ϕ 2.2
and C 0.2. Using LAP filter. This classifier will be named as C1.
2. LS-SVM, RBF kernel with ϕ 2.3 and C 1.8. Using CAR filter. (C2)
3. LS-SVM, RBF kernel with ϕ 14 and C 1.7. Using LAP filter. (C3)
4. LS-SVM, RBF kernel with ϕ 18 and C 0.5. Using CAR filter (C4)
5. KNN with 5 neighbours and city block distance. Using LAP (C5) and
CAR (C6) filters
6. KNN with 11 neighbours and city block distance. Using LAP (C7) and
CAR (C8) filters
7. KNN with 22 neighbours and city block distance. Using LAP (C9) and
CAR (C10) filters
8. KNN with 11 neighbours and cosine distance. Using LAP (C11) and CAR
(C12) filters
These are used both for creating a unique model and 8 models. The decision
is 1 when the classifier/s detect/s pre-movement or otherwise 0. The selection
of the classifier parameters has been carried out considering the rate of false
positives obtained in a 8-fold cross-validation of the training session to be as
minimum as possible, except from cases 3) and 4), where efforts were made
to obtain a higher rate of true positives.

2.6 Pseudo-real Time


The test session is used as input to validate the classifiers. The data of this
session are treated like a real time acquired data, namely, 2 second window
time of data is pre-processed with notch, band pass and spatial filters and
then the last second is used to extract features for the classifier. The first
second is omitted because filters need some samples to stabilize themselves.
The selecting data window is sliding each 0.0625 s (16 samples) and it goes
across the session. Thus, the classifier generates an output per each window.

3 Results and Discussion


After performing the pseudo-real time process, the classifier decisions are
analysed in order to know if they are right or not. A True Positive (TP) is
considered when a pre-movement decision is taken around 2 seconds before
movement onset and 0,5 after finishing it. However, any pre-movement deci-
sion out of this range is considered as False Positive (FP). Moreover, if two
or more consecutive pre-movement decisions are taken in a 0,5 s interval only
the first one will be taken into account and the rest will be discarded (DD)
as in a real application with an exoskeleton to introduce a security delay on
660 D. Planelles et al.

Fig. 2 Each small rectangle represents one arm forward/backward movement and
the wider ones are the period defined to detect them. Circles with solid colour are
considered as a TP or FP depending on where they are produced. Circles without
colour are DD.

the actuation. These concepts are shown in Fig. 2. Table 1 shows the results
obtained using a unique model per each classifier. In order to facilitate its
interpretation and discussion, more indexes are attached. The table shows a
column of TP in % of the total that corresponds to the number of movements
that have at least one detection inside the pre-movement window. FP in %
is the number of wrong detections over all the trials not included in pre-
movement/movement range as it was previously defined. Our main objective
is to obtain the minimum number of FP detections. For this reason, a fre-
quency of appearance of FP (FP T(s)) is also shown. As a second challenge,
TP has to be as high as possible.
Furthermore, INDEX TP and INDEX FP are values to assess these objec-
tives in each classifier. To calculate these indexes, the columns of TP % Total
and FP T(s) are reorganized from the lowest to the highest value. The value
assigned as index is the ordenation number of these vectors. In case that two
or more classifiers match their TP or FP rates, the mean of the ordenation
number of all of them is used instead. The INDEX column is the sum of
INDEX TP and INDEX FP. The classifier that obtains the lowest INDEX is
better rated than the rest.
Classifiers C3 and C4 show a high TP rate (96,00 % and 91,20 %, respec-
tively) although they have lots of FP (1 each 4,83 and 6,51 seconds). This
is a problem that should be corrected. Therefore, classifiers with parameters
selected to reduce FP have been used. C8 obtains the best final index (11,0).
This classifier recognized almost 1 of 5 movements and only produced 1 false
Processing EEG Signals to Detect Intention of Upper Limb Movement 661

Table 1 Results of Classifiers with Only One Model


UNIQUE MODEL
CLASSIFIER TP TP % Total FP FP % Total FP T(s) DD INDEX TP INDEX FP INDEX
C1 26 20,80 28 0,14 64,22 26 5,0 8,0 13,0
C2 2 1,60 7 0,03 256,87 1 12,0 3,0 15,0
C3 120 96,00 372 1,82 4,83 703 1,0 12,0 13,0
C4 114 91,20 270 1,35 6,51 477 2,0 11,0 13,0
C5 51 40,80 72 0,35 24,97 99 4,0 9,0 13,0
C6 56 44,80 94 0,46 19,13 109 3,0 10,0 13,0
C7 20 16,00 14 0,07 128,43 18 8,0 4,0 12,0
C8 24 19,20 19 0,09 94,63 23 6,0 5,0 11,0
C9 3 2,40 3 0,01 599,35 2 11,0 1,5 12,5
C10 5 4,00 3 0,01 599,35 4 10,0 1,5 11,5
C11 19 15,20 24 0,12 74,92 18 9,0 6,0 15,0
C12 22 17,60 27 0,13 66,59 22 7,0 7,0 14,0

detection each minute and a half. In a real application where the subject will
not be able to perform the movement but he is trying to do it, this result
means that the user could carry out a voluntary arm extension movement
in approximately one minute (in this experiment 5 movements take 62,4 sec-
onds). Other classifiers got better TP rate like C1, C5 or C6. However, FP
rate worsens in a greater extent and C2, C9 and C10 are reverse cases. An
ideal classifier would be that one able to return a pre-movement decision
only when a movement is actually performed although it could not detect all.
This is still far of being achieved but improvements in processing, features
extraction, classifiers selection and also determine a better high level decision
could reach a success factor higher than the current.
In an attempt to improve the results obtained with a single model, instead
of using the whole train session to make a single classifier, all combinations of
7 runs of the 8 runs of the same session are used. Thus, 8 models are used to
define each classifier. The results obtained are shown in Table 2. This table
adds a FINAL DECISION column. It specifies the high level rule to make a
pre-movement decision. It could be
• SAME DECISION (S). All models of the classifier agree.
• MAJORITY (M). At least 5 models have a pre-movement decision.
• AT LEAST ONE (U). Only one model with pre-movement decision is
needed.
It is possible to see that C5-U and C7-U detect 1 out of 4 movements.
In this sense, each minute the classifier would have one right and one wrong
detection. Therefore, the relation of the appearance time between TP and
FP is lower than with a single model. C7-D has a smaller final index than
C5-U and C7-U. It achieves to detect 1 movement in 406,25 seconds but this
is absolutely unacceptable because in a real application it could discourage
the user. As it was commented before, the same things occur in this case
with other classifiers. Consequently, in future works we will do changes in
662 D. Planelles et al.

Table 2 Results of Classifiers with Eight Models Per Classifier


MULTIPLE MODELS
CLASSIFIER FINAL DECISION TP TP % Total FP FP % Total FP T(s) DD INDEX TP INDEX FP INDEX
SAME DECISION 14 11,20 14 0,06 128,43 7 20,0 18,0 38,0
C1 MAJORITY 21 16,80 28 0,13 64,22 15 15,5 22,0 37,5
AT LEAST ONE 26 20,80 30 0,15 59,94 29 14,0 25,5 39,5
SAME DECISION 1 0,80 1 0,01 1798,06 0 31,5 6,0 37,5
C2 MAJORITY 2 1,60 6 0,03 299,68 0 29,5 11,0 40,5
AT LEAST ONE 4 3,20 8 0,04 224,76 2 25,5 12,5 38,0
SAME DECISION 110 88,00 254 1,25 7,08 449 5,0 32,0 37,0
C3 MAJORITY 118 94,40 332 1,63 5,42 623 3,0 34,0 37,0
AT LEAST ONE 121 96,80 361 1,77 4,98 698 1,0 36,0 37,0
SAME DECISION 98 78,40 203 1,00 8,86 308 6,0 31,0 37,0
C4 MAJORITY 112 89,60 273 1,34 6,59 446 4,0 33,0 37,0
AT LEAST ONE 119 95,20 349 1,71 5,15 538 2,0 35,0 37,0
SAME DECISION 16 12,80 13 0,03 138,31 11 17,5 17,0 34,5
C5 MAJORITY 21 16,80 18 0,09 99,89 29 15,5 20,0 35,5
AT LEAST ONE 32 25,60 29 0,14 62,00 51 9,5 23,5 33,0
SAME DECISION 10 8,00 11 0,05 163,46 10 23,5 14,5 38,0
C6 MAJORITY 44 35,20 65 0,32 27,66 72 8,0 29,0 37,0
AT LEAST ONE 70 56,00 112 0,55 16,05 187 7,0 30,0 37,0
SAME DECISION 4 3,20 1 0,01 1798,06 0 25,5 6,0 31,5
C7 MAJORITY 16 12,80 12 0,06 149,84 9 17,5 16,0 33,5
AT LEAST ONE 32 25,60 29 0,14 62,00 51 9,5 23,5 33,0
SAME DECISION 0 0,00 1 0,01 1798,06 0 34,5 6,0 40,5
C8 MAJORITY 10 8,00 11 0,05 163,46 5 23,5 14,5 38,0
AT LEAST ONE 28 22,40 30 0,15 59,94 50 12,5 25,5 38,0
SAME DECISION 0 0,00 1 0,01 1798,06 0 34,5 6,0 40,5
C9 MAJORITY 2 1,60 2 0,01 899,03 1 29,5 9,0 38,5
AT LEAST ONE 11 8,80 8 0,04 224,76 6 22,0 12,5 34,5
SAME DECISION 0 0,00 0 0,00 Inf 0 34,5 2,0 36,5
C10 MAJORITY 1 0,80 0 0,00 Inf 0 31,5 2,0 33,5
AT LEAST ONE 3 2,40 4 0,02 449,52 5 27,5 10,0 37,5
SAME DECISION 3 2,40 1 0,00 1798,06 0 27,5 6,0 33,5
C11 MAJORITY 15 12,00 19 0,09 94,63 18 19,0 21,0 40,0
AT LEAST ONE 31 24,80 44 0,22 40,87 69 11,0 28,0 39,0
SAME DECISION 0 0,00 0 0,00 Inf 0 34,5 2,0 36,5
C12 MAJORITY 12 9,60 15 0,07 119,87 11 21,0 19,0 40,0
AT LEAST ONE 28 22,40 36 0,18 49,95 42 12,5 27,0 39,5

the processing. Also we will test new classifiers as Artificial Neural Networks
to improve the current results.

Acknowledgment. This research has been funded by the Spanish Ministry of


Economy and Competitiveness as part of the project Brain2Motion - Development
of a multimodal brain-neural interface to control an exoskeletal-neuroprosthesis
hybrid robotic system for the upper limb, Reference: DPI2011-27022-C02-01.

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Preliminary Findings of Feasibility and
Compliance of Technology-Supported Distal
Arm Training at Home after Stroke

Gerdienke B. Prange1,2, Sharon M. Nijenhuis1, Patrizio Sale3, Alfredo Cesario3,


Nasrin Nasr4, Gail Mountain4, Farshid Amirabdollahian5, Jaap H. Buurke1,6
1
Roessingh Research and Development, Enschede, The Netherlands
2
Department of Biomechanical Engineering,
University of Twente, Enschede, The Netherlands
3
Department of NeuroRehabilitation, IRCCS San Raffaele Pisana, Rome, Italy
4
School of Health and Related Research,
University of Sheffield, Sheffield, United Kingdom
5
Adaptive Systems Research Group,
University of Hertfordshire, Hatfield, United Kingdom
6
Department of Biosystems and Signals,
University of Twente, Enschede, The Netherlands

Abstract. After stroke, intensive and active training is important to regain


functional use of the arm and hand. By applying a telerehabilitation system
(SCRIPT1) supporting active, distal arm practice at home, a patient can practice
independently, which enables a larger dosage of treatment than possible during
one-to-one supervised rehabilitation. Currently one of the major, but rarely
addressed, questions concerning telerehabilitation is whether patients actually use
such a system in a self-administered training approach. This paper presents
preliminary results about feasibility of self-administered post-stroke home-based
SCRIPT1 training. So far, data of 20 chronic stroke patients is available, who have
trained for six weeks at home using interactive gaming exercises and a passive
wrist/hand orthosis supporting hand opening (SCRIPT1). Findings so far indicated
positive perceptions of usability and showed actual use of the system with a mean
training duration of 107 min/week. This was accompanied by modest
improvements in motor function and dexterity, correlated positively with training
duration. These preliminary findings indicate that self-administered, technology-
supported distal arm training at home is feasible for chronic stroke patients.

1 Introduction

Functional recovery from stroke requires extensive rehabilitation. Research into


motor relearning and cortical reorganization after stroke has provided a
neurophysiological basis for key aspects that stimulate restoration of arm function
(Schaechter, 2004; Krakauer, 2005): high training dose, active initiation and
execution of movements, and application of functional exercises. In the setting of

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 665
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_94, © Springer International Publishing Switzerland 2014
666 G.B. Prange et al.

the rehabilitation centre, intensive training of arm and hand is supervised by


highly skilled professionals. However, the time that can be spent on training in
such intramural settings is limited. Due to the high costs of clinical
neurorehabilitation, post-stroke treatments are limited to only a few weeks with
limited treatment resources in many countries.
Technological innovations provided an opportunity to design interventions that
take many key aspects of motor relearning into account, of which rehabilitation
robotics is a well-known example. With such a device, the required amount of
movement support can be provided, allowing active practice when this is not
possible otherwise. This increases the potential to train intensively, with the
patient’s active contribution to functional exercises. Contemporary robot-aided
therapy focuses mainly on the proximal arm, and results in improvements in the
proximal arm only, without generalization to the wrist and hand (Prange, 2006),
while the wrist and hand play a major role in a person’s functional independence.
In order to maximize independent use of the upper extremity in daily life, it is
important to include functional practice of the wrist and hand [1].
If a system that supports active, distal arm practice can be applied in a patient’s
home within a telerehabilitation concept [2], a larger dosage of treatment can be
delivered while the patient practices independently with remote supervision by a
healthcare professional. Augmented dosage of treatment is a major determinant of
functional outcome after post-stroke neurorehabilitation, with a recommended
amount of added practice of at least 16 hours to improve functional recovery [3].
Besides the amount of treatment available, the adherence of a patient to the
training programme affects the actual dosage of treatment delivered [3], which is
unclear in many cases. In addition, a technology-supported home-based
application enables distributed practice throughout the day or week instead of
massed practice, which is associated with better retention performance as well [4].
In the present ongoing study (Supervised Care and Rehabilitation Involving
Personal Tele-robotics, SCRIPT), a custom-designed orthosis that passively
supports wrist and hand function is combined with a motivational user interface
with gaming environment, connected to a remote module for off-line supervision
by a healthcare professional. This system (SCRIPT1) is intended to be used
independently at home by chronic stroke patients for distal arm training. Besides
feasibility of technology-supported arm/hand training at home in chronic stroke
patients, currently one of the major, but not often addressed, research questions
concerning telerehabilitation is whether patients actually use such a system when
provided with the opportunity. Therefore, the present paper aims to examine the
feasibility of post-stroke home-based SCRIPT1 training in terms of usability,
compliance and associated changes in arm function.

2 Methods

The present feasibility study applied a longitudinal (pre-post) experimental study


design, with an intervention of six weeks of home-based arm/hand training with the
Preliminary Findings of Feasibility and Compliance of Technology 667

SCRIPT1 system. The SCRIPT1 system was custom developed involving a user-
centred design approach, taking needs and abilities of stroke patients, their carers
and healthcare professionals into account through repeated usability testing.

2.1 Participants
In total, 24 chronic stroke patients with impaired arm/hand function have been
included in this study across 3 clinical sites: Roessingh Research and Development
(the Netherlands), IRCSS San Raffaele Pisana (Italy) and University of Sheffield
(United Kingdom). Main inclusion criteria were between 6 months and 5 years
after stroke and 18-80 years of age, displaying limited arm/hand function (having at
least 15° active elbow flexion and a quarter range of active finger flexion, but not
having full active function of wrist and hand). Also, participants had to be able to
accommodate the SCRIPT1 system at their homes. The study was approved by the
local medical ethics committees of the 3 sites and all participants provided written
informed consent before entering into the study.

2.2 Intervention
Participants performed six weeks of self-administered distal arm training at home.
They were recommended to exercise 180 minutes per week with the SCRIPT1
system, but they were free to train more (or less) if they preferred. They trained
independently using custom-designed games displayed on a touchscreen, while
they were supervised remotely, off-line, by a trained healthcare professional (HCP).
During training, they wore a custom-designed hand/wrist orthosis (Fig. 1) that
passively supported wrist extension and hand opening across all fingers of the
affected arm. A more detailed description of the SCRIPT passive orthosis can be
found in [5].

Fig. 1 SCRIPT1 passive hand/wrist orthosis


668 G.B. Prange et al.

During weekly home visits, the HCP adjusted the amount of support by
adjusting elastic bands over the wrist and fingers to provide just enough support, so
that a participant was able to actively open the hand to grab a 2.5 cm cube, while
being supported by the orthosis. Additionally, all participants used the SaeboMAS
(Saebo Inc, Charlotte NC, USA) arm support for the proximal arm, set to provide
100% of arm weight compensation. The HCP remotely selected suitable games for
each participant in terms of number and type of wrist and hand movements
involved in the exercises, once a week through a web-based, secured portal.

2.3 Measurements
Evaluation of feasibility involved usability measured by the System Usability
Scale (SUS), compliance in terms of actual use (training duration in minutes), arm
motor function measured by the upper extremity part of the Fugl-Meyer
assessment (FM [6, 7]) and dexterity measured by the Action Research Arm Test
(ARAT [8-10]). ARAT focuses specifically at functional hand ability, whereas
FM assesses more general arm function, which is included because an increased
hand movement ability may (also) affect proximal arm function. The SUS is a 10-
item questionnaire giving a global view of subjective assessments of usability of a
technological system [11]. Scores are translated to a scale of 0% to 100%,
indicating: <50% = system will almost certainly have usability difficulties in the
field; 50-70% = promising, but guarantees no high acceptability in the field; >70%
= high chances for acceptance in the field [12].
Evaluation of arm function and dexterity was done before (T01) and after
training (T08) and at 2 months follow-up after the end of training (T15). Because
the dataset isn’t complete yet in this ongoing study, only available data of T01 and
T08 is presented here. Usability was assessed at T08 only and training duration
was recorded within the SCRIPT1 system throughout the 6-week training period.

2.4 Data Analysis


Since the data presented here represents preliminary data of a subset of the
complete dataset, changes in motor function and dexterity were compared between
pre- and post-training evaluation sessions using the non-parametric Wilcoxon
signed-rank test (significance level α < 0.05). In addition, a correlation analysis of
training duration with changes in FM and ARAT and SUS score was performed
using Spearman’s correlation.

3 Results

At present, 23 chronic stroke patients (10 from the Netherlands, 10 from Italy and
3 from the United Kingdom) have completed T01 and T08 evaluations. Of these, 3
have stopped participation during the training, due to shoulder complaints acting
Preliminary Findings of Feasibility and Compliance of Technology 669

up, dislike of the system and technical issues. Mean age of the remaining 20
participants was 58 years; mean time post-stroke was 17 months.
Twenty participants (87%) completed the training period and were able to work
with and use the SCRIPT1 system independently. The group average of the SUS
score is 69%, indicating that usability of the SCRIPT1 system is promising with a
good chance of acceptance in the field. Individually, “usability difficulties in the
field” (SUS <50%) was scored by 4 participants, usability was perceived as
“promising” (SUS 50-70%) by 8 participants and 8 reported the SCRIPT1 system
to have “a high chance of acceptance” (SUS >70%). Of the 3 participants that
dropped out during training (13%), 1 was not related to limited usability of the
SCRIPT1 system, as her SUS score was 95%. The other 2 participants (9%)
experienced substantial usability problems, as represented by SUS scores of 30%
and 38%.

Table 1 Clinical outcomes pre-post training

Mean (±SD) values

Outcome measure T01 T08


FM (points) 34 38

ARAT (points) 27 29

SUS (%) n/a 69

Average training duration was 107 (±67) minutes per week. Overall, this
amounted to a total training duration of 644 (±403) minutes (i.e., 10 hours and 44
minutes) per participant over 6 weeks. This comes down to about 15 minutes of
self-administered training each day for 6 weeks. Individually, training duration
varied substantially, ranging from 13 up to 284 minutes (4 hours and 44 minutes)
per week.
Clinical outcomes showed improvements after training (Table 1). FM scores
increased significantly by 4.0 points (±4.9) on group level (p=0.002). Similarly,
ARAT scores increased significantly by 1.8 (±3.7) on group level (p=0.014). On
individual level, 4 out of 20 participants exceeded minimal clinically important
differences (MCID +6.6 points [13]) on FM and 1 approached MCID with FM
improvement of 6 points. For ARAT, 2 participants exceeded MCID (of +5.7
points [13]).
To further examine associations between training duration and clinical outcomes
correlation analysis was performed, showing that training duration was correlated
(Fig. 2) with changes in ARAT (ρ=0.70, p=0.001), indicating that a higher training
duration is associated with a larger improvement in ARAT. This correlation
remained significant without the one participant with the highest training duration
(ρ=0.64, p=0.003). Correlation of training duration with change in FM was weak
(ρ=0.34, p=0.143), but there was a positive trend associated with SUS (ρ=0.40,
p=0.094).
670 G.B. Prange et al.

Fig. 2 Scatter plot of training duration and change in ARAT

4 Discussion

The majority of participants (87%) were able to use the SCRIPT1 system as tool
for self-administered training, with an average compliance of 107 minutes per
week. In addition, usability was perceived as positive across the majority. Only
9% of participants quit using the SCRIPT1 system due to serious usability issues.
Experienced use issues have been noted to provide input for design adaptations for
a second generation. The preliminary findings of the present study so far indicate
that technology-supported distal arm training at home is feasible for chronic stroke
patients.
As this is one of a few studies in which technology-supported arm/hand
training is performed in the patient’s home, it is difficult to compare the actual
training duration with other home-based training studies. A review by Coupar
2012 involved four studies on telerehabilitation focusing on training of the upper
limb after stroke in the home situation, indicating home-based upper limb
programmes to be no more or no less effective for arm motor impairment
outcomes [14]. In all of these studies, the patients were remotely supervised at a
fixed time, so with direct real-time (remote) supervision of a therapist. Therefore,
the times and duration of training each day were fixed [14], and the actual amount
of self-administered training at home wasn’t examined. This was also the case for
the study by Holden et al., in which therapists in a remote location conducted
treatment sessions with a patient located at home using a virtual environment
based motor-training system [15], and the studies by Taub and Lum et al.,
in which a therapist supervised the training from a different room in the clinic
Preliminary Findings of Feasibility and Compliance of Technology 671

[16, 17]. In contrast, the SCRIPT1 system allowed stroke patients to have a more
active role in their rehabilitation, involving their family members and carers as
well, and make their own decisions about their training schedule. Thus, in our
study patients were free to choose their own training time and duration. Anecdotal
evidence from physiotherapists involved in the present study have mentioned that
the achieved adherence of about 15 minutes per day is rather high for chronic
stroke patients to exercise at home after discharge from rehabilitation, which is
promising for the potential to engage people in home-based arm/hand training
post-stroke.
The improvements in motor function of the arm in the present study are along
similar lines as those found in robot-aided studies in chronic stroke [18], as well as
actively [19] and passively [20, 21] actuated arm support for the proximal arm.
Again, these studies involved face-to-face supervision and a fixed schedule of
practice (ranging from 1½ hours per week [19, 21] to 3 hours per week [20]). The
preliminary findings in the present study indicate that when provided with the
opportunity at home, stroke patients have the personal incentive to perform
comparable amounts of practice as a mean training duration of 1¾ hours per week
was observed.
It has to be noted that individual variation in training duration was large, ranging
from ¼ of an hour to over 4½ hours per week. Since dosage of treatment is
regarded as an important determinant of treatment outcome [3], a positive
correlation with clinical improvements was expected. This relation was observed
for dexterity, but it was less pronounced for motor function. As the present study is
ongoing, it is of particular interest to examine these relations more closely in the
complete sample, along with other factors that might be involved as mediators in
clinical improvements (e.g., initial stroke severity, age, motivation, etc.).

5 Conclusion

The preliminary findings of this ongoing study for usability and compliance are
positive and promising. Also, modest improvements in motor function and
dexterity have been found at this point. On individual level, more pronounced
improvements have been observed for a limited number of participants. The data
so far suggest a moderate correlation of clinical improvement with training
duration, where participants who train more achieve larger improvements of
dexterity, but other potential mediators should be investigated as well in the larger
sample.
If these results so far are indicative of the ongoing study, technology-supported
arm/hand training may be a feasible and promising tool to enable self-
administered practice at home for chronic stroke patients. Ultimately, home-based
training could be considered as a neurorehabilitation application at an earlier stage
after stroke, for instance as soon as inpatient rehabilitation is finished or even as
addition to inpatient rehabilitation. In many countries, this would involve patients
in the sub-acute phase as well, where larger treatment effects would be expected.
672 G.B. Prange et al.

Acknowledgement. This work has been partially funded under Grant FP7-ICT-288698
(SCRIPT) of the European Community Seventh Framework Programme. We are grateful to
the SCRIPT consortium for their ongoing commitment and dedication to the project and to
a large number of stroke patients, their families and healthcare professionals that have
provided us with formative and summative feedback during this project.

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Exploring Relations between Functional Task
Kinematics and Clinical Assessment of Arm
Function and Dexterity Post-stroke

Gerdienke B. Prange1,2, Sharon M. Nijenhuis1, Stefanie M. Kersten1,2,


Arno H.A. Stienen3, and J.S. Rietman1,2
1
Roessingh Research and Development, Enschede, The Netherlands
g.prange@rrd.nl
2
Department of Biomechanical Engineering,
University of Twente, Enschede, The Netherlands
3
University of Twente, Department of Biomechanical Engineering,
Enschede, The Netherlands
and
Northwestern University,
Physical Therapy and Human Movement Sciences,
Chicago (IL), USA

Abstract. After stroke, technology-supported treatment, enables more


independent, self-administered exercises of the arm. Preferably, such treatment is
applied in the home setting, to enable increase of treatment dosage. Although such
interventions are effective to improve motor function of the affected arm, their
influence on functional abilities is less understood. The present paper examines
which motor control limitations are related to limitations in arm and hand function
in stroke patients. A functional reach and grasp task has been performed by 14
chronic stroke patients, during which kinematic parameters were recorded, in
addition to maximal grip strength. Also, clinical assessments of arm function and
dexterity were done. Peak hand speed, elbow extension range, maximal hand
opening and grip strength correlated strongly with clinically assessed sensorimotor
arm function and dexterity in mildly to severely affected chronic stroke patients
(ρ=0.66-0.85), whereas trunk displacement showed a weaker correlation (ρ=-
0.50). The present findings suggest that it may be valuable for treatment
applications in neurorehabilitation for stroke to focus on at least movement speed
and movement coordination for both the proximal and distal arm in order to
stimulate functional improvements.

1 Introduction
Research into underlying mechanisms of motor recovery of the upper extremity
after stroke has provided a neurophysiologic basis of important treatment aspects
of neurorehabilitation: actively moving the arm and hand, increased dosage of
treatment and application of task-specific exercises [1, 2]. The amount of
treatment for a stroke patient is primarily limited by the availability of skilled

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 675
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_95, © Springer International Publishing Switzerland 2014
676 G.B. Prange et al.

professionals. Technology-supported treatment, such as robot-aided therapy,


enables more independent, self-administered exercises of the arm and could
enhance the dosage of treatment [3, 4]. Preferably, such treatment is applied in the
home setting, to enable increased treatment dosage even more [5, 6].
Although several technology-supported interventions, including robot-aided
therapy, are effective to improve motor function of the affected arm after stroke,
their influence on functional abilities involving both the arm and hand is less
supported and understood [4, 7]. Therefore, more insight is needed into the
mechanisms that underlie recovery of motor function (restitution) and its relation
with learning compensational strategies (substitution) for functional improvements
[7, 8].
To differentiate between restoration of function by either recovery or
compensation, kinematic movement analysis increasingly receives attention to
quantify move-ment execution [8, 9]. When combining clinical assess-ments of
function and activity with kinematic measures at motor control level in a multi-
level testing approach, the impact of interventions targeted at functional
improvement and their underlying mechanisms can be better understood [9, 10].
For instance, reduced movement execution during a functional task (drinking) has
been associated with activity limitations in mildly and moderately affected stroke
patients by Alt Murphy et al. [10, 11].
With a better understanding of the relation between specific aspects of
functional limitations and movement execution of the affected arm and hand after
stroke, targeted interventions can be identified. Moreover, the effect of
interventions on recovery and/or compensation can be discerned, which contributes
to the development of evidence-based practice in neurorehabilitation.
As extension to an ongoing project (SCRIPT) [5], the present paper focuses at
one of the first steps: examining which motor control limitations are related to
limitations in arm and hand function in mild-severely affected stroke patients,
measured at baseline of a longitudinal study into home-based, technology-
supported arm and hand training.

2 Methods

2.1 Participants
Data of movement execution during a functional reach and grasp task is available
from 14 chronic stroke patients, a partial set of participants from a clinical trial
investigating technology-supported distal arm training at home within the ongoing
SCRIPT project [5, 12]. Participants had to be between 6 months and 5 years after
stroke and 18-80 years of age, displaying limitations in arm/hand function (with at
least 15° active elbow flexion and a quarter range of active finger flexion). They
had to be able to understand and follow instructions and have no additional
orthopaedic, neurological, or rheumatologic disease. The study was approved by
the local medical ethics committee and all participants provided written informed
consent prior to study entrance.
Relations between Functionaal Task Kinematics and Clinical Assessment 6777

2.2 Procedure
During a single session ev valuation (cross-sectional design), participants performeed
clinical assessments to evvaluate status of arm function and dexterity, a functionnal
reach and grasp task to reecord movement execution and hand grip dynamometry tto
measure maximal grip streength.

2.2.1 Clinical Assessm


ment

Arm motor function was measured by the upper extremity part of the Fugl-Meyer
assessment (FM), assessin ng the ability to perform gross shoulder, elbow, wrist annd
hand movements, which has h a maximum score of 66 [13]. Proximal and distal arrm
ability was evaluated by the
t Action Research Arm Test (ARAT), consisting of 119
items testing grasp, grip, pinch and gross arm movements, with a maximum scorre
of 57 points [14]. The Bo ox and Blocks Test (BBT) was used to measure manuual
dexterity, where as many 2.5 cm cubes as possible have to be moved, one at a tim me,
from one compartment to o the other within 60 seconds. More blocks transporteed
indicates better manual deexterity [15].

2.2.2 Movement Execcution

A standardized functionaal movement task was defined to record arm and hannd
movements. The reach an nd grasp task involved subsequently forward reaching in
the horizontal plane to a cup
c (point A), grasping the cup, holding it while bringinng
it to the starting point an
nd back (to point A), releasing the cup and bringing thhe
hand back to the start possition. Point A corresponded with the position of the wriist
at near-maximal (80%) reach distance (d) for each participant (Fig. 1). Thhe
task was repeated until at least 7 repetitions (of at least reaching part) werre
recorded.

Fig. 1 Measurement setup for reach and grasp task on table top, with arm in startinng
position and point A corresp
ponding with position of wrist at 80% of maximal reach distancce
(d)
678 G.B. Prange et al.

2.2.3 Grip Strength

Maximal hand grip strength (GS) of the affected hand was measured using a hand-
held dynamometer, which the participant held with the arm at right angles and the
elbow by the side of the body [16]. Participants were verbally encouraged to
generate maximum isometric effort by squeezing the dynamometer and to maintain
this for about five seconds. This was done three times, of which the highest value
was used for analysis.

2.3 Measurements
During the reach and grasp task, the position of the trunk, shoulder, elbow, wrist,
and hand was recorded using 3D movement analysis by a 6-camera VICON
system with passive markers (VICON MX13+ motion capture system; Oxford
Metrics Ltd, Oxford, United Kingdom). Markers were placed on 18 (bony)
landmarks of the thorax, upper and lower arm and hand according to guidelines of
the International Society of Biomechanics (ISB) [17] for the arm and an adapted
version of a validated marker model [18] for the hand.

2.4 Data Analysis


All marker data were labelled using VICON Nexus software (v1.8.3) and filtered
with a second order Butterworth filter, with a cut-off frequency of 20 Hz and zero-
phase shift, using custom-written Matlab software (R2012b, MathWorks Inc.,
Natick, Massachusetts, USA). The following six parameters were calculated from
the 3D position data measured during the reach and grasp task, averaged over the
available 7 repetitions that displayed the largest hand opening.
Total movement time (MT) was defined as the time between movement onset
and movement offset. Movement onset was defined as the moment at which the
velocity of the hand marker (MCP3) exceeded 2% of the maximum velocity
during the total movement task. Movement offset was defined as the moment that
MCP3 velocity was lower than 2% of the maximum velocity [11].
Movement smoothness (MS) was defined as the number of movement units in
the tangential velocity profile of the hand marker per second. This profile was
searched for local minima and maxima. A difference between a minimum and
next maximum velocity value that exceeded the amplitude limit of 20 mm/s
signified a velocity peak. The time between 2 subsequent peaks had to be at least
150 milliseconds [11]. MS was normalized to number of movement units per
second to account for differences in MT between participants.
Maximal forward trunk displacement (TD) was defined as the difference
between the maximal forward movement of the trunk marker in the sagittal plane
and the initial position of this marker during the movement task.
The elbow extension range (EE) was determined between the largest angle
and smallest angle between the lower arm and the upper arm during the movement
Relations between Functional Task Kinematics and Clinical Assessment 679

task. Maximum extension was defined as 0 degrees. This was calculated with (1),
where A represented the vector of the upper arm, B represented the vector of the
lower arm, represented the length of the upper arm, represented the
length of the lower arm and Ɵ represented the angle between the vector of
the upper arm (A) and the vector of the lower arm (B). was determined by the
distance between the marker on the acromioclavicular joint and the marker on the
lateral epicondyle. was determined with the distance between the marker on
the lateral epicondyle and the middle of both wrist markers.
· (1)
The peak hand speed (HS) was defined as the maximum of the tangential
velocity profile of the hand marker during the complete movement task.
The maximum hand opening (HO) was determined as the maximum
Euclidean distance (x, y, z) between the tips of the thumb (FT1) and middle finger
(FT3) during the first reaching phase of the movement task using (2).

1 , 3 , 1 , 3 , 1 , 3 , (2)

2.5 Statistical Analysis


A correlation analysis was performed for movement execution parameters, grip
strength and clinical scores (FM, ARAT and BBT) using Spearman´s correlation
with SPSS (IBM Statistical Packages for the Social Sciences, 20.0; SPSS Inc,
Chicago Illinois).

3 Results

The average age of the 14 participants was 59.2 years (±11.7), mean time post-
stroke was 17.7 (±13.3) months, 9 were male and 5 were female. Participants had
severe to mild stroke: FM varying from 9-57 (median 46.5) points, ARAT 3-53
(median 32.5) points, mean BBT of 17.3 (± 13.9) blocks. Four participants (FM
ranging from 9-22) were not able to grasp and hold an object, resulting in values
of 0 for HO. Also, they performed the movement task only partially, affecting the
values of MT (data of MT is presented for both situations: with and without these
four participants). There was missing data of the finger markers of one other
participant (FM = 35). GS was only measured from 11 participants (not available
for participants with FM of 52-57). Group values of all movement execution
parameters and clinical scores are displayed in Table 1.
Most movement execution parameters correlated strongly with all three clinical
scales, FM, ARAT and BBT (p≤0.028): movement smoothness, MS (ρFM=0.65,
ρARAT=0.58, ρBBT=0.59); hand speed, HS (ρFM=0.85, ρARAT=0.71,
ρBBT=0.76); elbow extension range, EE (ρFM=0.76, ρARAT=0.75, ρBBT=0.67);
and hand opening, HO (ρFM=0.68, ρARAT=0.66, ρBBT=0.68). The relation
680 G.B. Prange et al.

Table 1 Mean valueas of kinematic outcome measures

N Mean (± SD)
GS (kg) 11 14.5 (± 9.4)

MT (s) 14 10.64 (± 4.34)


10a 8 95 (± 3 33)
MS (nmu/s) 14 2.99 (± 0.77)
HS (mm/s) 14 579.62 (± 290.78)
TD (mm) 14 104.09 (± 63.23)
EE (deg) 14 42.63 (± 15.89)
b
HO (mm) 13 115.87 (± 81.85)
a
Excluding 4 participants who couldn’t grasp cup
b
Missing marker data for 1 participant

Fig. 2 Scatter plot of peak hand speed and FM score

between HS and FM is illustrated in Fig. 2. Grip strength (GS) correlated (p≤0.020)


strongly with FM and ARAT (ρFM=0.77, ρARAT=0.69), but only moderately with
BBT (ρBBT=0.54; p=0.085). In general, the correlation of these movement
execution parameters was most pronounced with FM with respect to the other
clinical scales. The negative correlation of MT with FM was significant when
including the four non-grasping participants (ρFM=-0.66, p=0.011), but wasn’t
significant when excluding those participants (ρFM=-0.51, p=0.136). Maximal
trunk displacement had a moderate negative correlation with ARAT and BBT
(ρARAT=-0.50, ρBBT=-0.47), but this was not significant (p≥0.070).
Relations between Functional Task Kinematics and Clinical Assessment 681

4 Discussion

The present results showed that most kinematic variables were strongly associated
with sensorimotor function (FM) as well as with activity capacity (ARAT and
BBT). The correlations were stronger with sensorimotor function than with
activity capacity. This is probably because the kinematic parameters and the FM
both reflect body function level. Nevertheless, correlations with ARAT and BBT
were substantial as well.
Number of movement units, movement time and peak angular velocity of the
elbow have been identified as best discriminating parameters between moderately
and mildly affected chronic stroke patients (based on FM) and healthy persons
during a drinking task [11]. In the present study, comparable parameters showed
correlations with FM for chronic stroke patients, including severely affected
patients: movement time, movement smoothness, peak hand speed, elbow
extension range, as well as maximal hand opening and grip strength. Remarkably,
movement smoothness (number of movement units per second) correlated
positively with body function level and activity level in the present study,
implying that a larger number of movement units would be associated with a
higher clinical score, whereas the opposite relation would have been expected
[11]. This relation is likely mediated by movement time, as total number of
movement units during a task is highly correlated with movement time in chronic
stroke [11]. Total number of movement units during the entire task have been
calculated as well in the present study, but showed no significant correlation with
clinical scales. However, this value is biased, because four severely affected
patients weren’t able to perform the entire reach and grasp task, so the total
number of movement units could only be validly compared for ten participants.
Regarding the activity level, Alt Murphy et al. showed that variance in ARAT
of moderate to mildly affected patients was explained predominantly by
movement time, smoothness and trunk displacement [10]. The associations of
these parameters were weaker with FM than with ARAT. In the present study
correlations of FM, ARAT and BBT were more pronounced with hand speed and
elbow extension range instead of movement time and smoothness, and
correlations with trunk displacement were weaker and non-significant. In addition,
we found stronger associations of kinematic parameters with FM than ARAT or
BBT. This may be related to less impaired patients involved in the study of Alt
Murphy et al., with a shorter time post-stroke [10]. Also, the task during which
movement execution was recorded was in both cases of a functional nature
(reaching and grasping), but focused more on an actual purposeful activity
(drinking) in their study. Finally, they also involved only patients who could
perform the drinking task (i.e., were able to grasp the glass), whereas our study
included more severely affected stroke patients. Moreover, the present study
included additional measures of hand function, such as hand opening and grip
strength, which showed strong correlations with sensorimotor function and
activity capacity as well.
682 G.B. Prange et al.

Main contributors to limitations in post-stroke reach performance and arm


function were found to be muscle weakness and reduced isolated (selective)
movement control [19-22]. The strong correlations of elbow extension range, hand
speed, hand opening and grip strength with FM, ARAT and BBT in the present
study likely reflect the relevance of these aspects during a functional task
including hand movements as well. Regarding impaired selective movement
control, abnormal coupling between the shoulder abductors and elbow flexors is
known to limit elbow extension and thus reaching, in a way that is unrelated to
weakness of elbow extensors [23]. Moreover, the extent of this limitation is
associated with FM, where more severely affected patients experience stronger
limitations [24]. Although we didn’t include a specific parameter to quantify
selective movement control yet in this ongoing work, the correlation with elbow
extension range indicates that selective movement control is involved in such a
functional task as well. These topics will be explored in future work with an
ongoing clinical trial into technology-supported arm and hand training of stroke
patients at home.
The finding that larger elbow extension range, hand opening, hand speed and
grip strength correlated strongly with higher scores on FM, ARAT and BBT
suggests that if treatment applications pay specific attention to speed of hand
transportation together with movement ability and/or coordination of the elbow
and hand in functional exercises, this may potentially stimulate functional
improvements.

5 Conclusion

Peak hand speed, elbow extension range, maximal hand opening and grip strength
correlated strongly with sensorimotor arm function and dexterity in mildly to
severely affected chronic stroke patients during performance of a functional reach
and grasp task, whereas trunk displacement showed a weaker correlation. The
present findings suggest that it may be valuable for treatment applications in
neurorehabilitation for stroke to focus on at least movement speed and movement
coordination for both the proximal and distal arm in order to stimulate functional
improvements. Subsequently, examination of training-induced changes in
kinematic parameters (of speed and/or coordination and trunk displacement)
during any post-stroke intervention can provide a better understanding of the
mechanisms of recovery involved.

Acknowledgement. Part of this work has been done in association with the SCRIPT
project, partially funded under Grant FP7-ICT-288698 (SCRIPT) of the European
Community Seventh Framework Programme.
Relations between Functional Task Kinematics and Clinical Assessment 683

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A Combined Interfascicular-Cuff
Electrode (ICE) for Selective
Recruitment of Polyfascicular
Peripheral Nerves Using Transversal
Stimulation

Alessandro Ranieri, Rasmus Elbæk Andersen,


Mette Vandborg Lauridsen, and Kristian Rauhe Harreby

Center for Sensory-Motor Interaction, Aalborg University, Aalborg, Denmark


{aranie13,rean08,mvla10}@student.aau.dk,
krauhe@hst.aau.dk

Abstract. Selective electrical stimulation of peripheral nerves has shown


potential in reducing symptoms of Phantom Limb Pain (PLP). The cuff
electrode design is used in clinical applications, however, it is not able to
selectively activate deeper fascicles of large human sized nerves. This work
investigates the effects of combining an Interfascicular and a Cuff Electrode
(ICE). An ICE was constructed, consisting of an eight contact cuff (two full
ring contact sites in each end, six contact sites in a center ring configura-
tion) and an interfascicular wire electrode, which was placed in the center of
the nerve. In vitro experiments were conducted on three pig median nerves.
During in vitro experiments transversal stimulation was performed using the
cuff alone or in combination with the interfascicular electrode. The evoked
Compound Action Potentials (eCAP) were recorded from 26-30 individual
fascicles and used to quantify the selectivity performance of the different
stimulation configurations.
Device selectivity was 0.25 ± 0.10 for the ICE and 0.20 ± 0.11 for the cuff.
This is an improvement of 22.08% ± 13.60% for the ICE over the cuff. The
ICE could therefore prove to be a simple and effective improvement over ex-
isting cuff electrodes, which could see potential use in treatment of PLP and
other areas where selective stimulation is required.

Keywords: Electrical stimulation, Phantom limb pain, Cuff electrode, In-


terfascicular electrode, ICE.

1 Introduction
Injuries to peripheral nerves can result in partial or total loss or alteration
of motor, sensory and autonomic functions [1]. Amputation of a limb can

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 685
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_96,  c Springer International Publishing Switzerland 2014
686 A. Ranieri et al.

lead to neuropathic pain called phantom limb pain (PLP), which may stem
from maladaptive changes of the nervous system resulting from the lost or
altered neurological function [2]. Incidence of postoperative PLP in patients
that have undergone amputation can be as high as 80%. The exact etiology
of PLP is not known, but the condition is associated with reorganization in
the somatosensory cortex [3]. Reversal of cortical reorganization (CRO) have
in several studies been associated with a reduction in PLP and have been
observed after intensive use of myoelectric prosthesis [3] and in experiments
with different types of electrical stimulation to the amputation stump as
part of sensory discrimination training [4] [5]. It is believed that through
increased stimulation selectivity, Peripheral neural electrodes (PNE) can be
used to induce more varied and natural sensation than is possible with surface
electrodes; this could improve reversal of CRO [6], for which the ability to
exclusively activate specific subsections of a peripheral nerve is believed to
be an important factor [6].
Two types of PNE, Longitudinal Intrafascicular Electrode (LIFE) and
Transverse Intrafascicular Multichannel Electrode (TIME), have been used in
research within treating PLP [7] [6]. The thin-film longitudinal intrafascicular
electrode (tfLIFE) are implanted longitudinally into a single fascicle, which
can then be selectively activated. However, for a large polyfascicular nerve
that would mean implementing many electrodes to cover all fascicles [7]. The
TIME is implanted transversally to cover more fascicles but could still require
several electrodes to fully cover a whole human sized nerve [6].
Cuff electrodes have proven to be stable and safe [8], but as their contacts
are restricted to the surface of the nerve, it is difficult to selectively activate
deeper fascicles [9]. The Flat-interface nerve electrode (FINE) flattens nerves
to increase their surface to cross-sectional area ratio [10]. There may, however,
be limitations to its application in nerves that cannot be deformed enough to
see an improvement over cuffs. One alternative electrode, which was tested
by Riso et al. [11], consisted in the combination of an intrafascicular and cuff
electrode, and was tested using different longitudinal tripolar configurations
with either an interfascicular anode and two cuff cathodes or two cuff anodes
and one cuff cathodes. Results from the study indicated that the addition of
the intrafascicular contact site added variety to the patterns of fascicles that
could be stimulated.
This work seeks to investigate the approach of combining an Interfascic-
ular and Cuff Electrode (ICE) using bipolar transversal stimulation, to as-
sess selectivity of such a combination in a polyfascicular nerve model, in
comparison to stimulation conducted with a cuff electrode alone, to ex-
plore the potential for an alternative to FINE or multiple TIME or LIFE
electrodes.
A Combined ICE for Selective Recruitment 687

 

,()$
 

 
,()$
()$



5 5

%

Fig. 1 A) Transversal view of the ICE showing the six contact sites in a center
ring configuration and the interfascicular contact site (IEFA). B) Longitudinal view
of the ICE. The electrode consists of a full ring on each end, named R1 and R2,
and a central ring configuration with six contact sites. The black line represents the
interfascicular electrode with a contact site on the centerline of the nerve and cuff.
The illustrations are not to scale.

2 Method
2.1 Electrode Design and Construction
The ICE consisted of a cuff electrode and an interfascicular electrode placed
in the center of the cuff (Fig. 1). Three cuff electrodes with eight contact
sites were constructed with different inner diameters (3.4 ± 0.8mm), based
on the mean diameter plus minus standard deviation of median nerves from
50 kg landrace pig as found by [12]. In each end of the cuff a platinum contact
site 1 mm wide and spanning the entire inner circumference was made. In
the center of the cuff six 1x1 mm platinum contact sites were placed with 60
degrees spacing in a ring around the inner circumference. The construction
of the cuffs was based on the procedure described in [13].
The interfascicular contact site were constructed using a thin teflon coated
wire (0.3 mm in diameter) connected to a curved needle for implantation.
A 2 mm long portion of the wire was de-insulated 5 cm from the needle.
The wire was marked 2 cm on each side of the contact site to allow correct
longitudinal placement of the interfascicular contact site with regards to the
central contact sites in the cuff.

2.2 Nerve Extraction and Preparation


The left median nerves were explanted from three farm pigs euthanized after
non related experiments. Access to the nerve was obtained by cutting ap-
proximately 5-7 cm proximal to the elbow joint, where the ulnar and median
688 A. Ranieri et al.

Fig. 2 Epineurium is carefully removed to free individual fascicles and allow the
insertion of the recording electrodes

nerve split, and 1-2 cm distally to the elbow joint, where the median nerve
divides into three branches, including ca. 1 cm from each. The sample was
then transported to the laboratory in Krebs-Ringer solution [14] at a tem-
perature of 10 ◦ C, and placed in a temperature controlled (20 ◦ C) nerve bath
with the same circulating solution, bubbled with Carbox (95% O2 and 5%
CO2 ). Up to 31 fascicles (the number of channels) were then separated from
the epineurium in the distal end and pinned with tungsten-tipped monopolar
electrodes for recording (Fig 2). The reference electrode was also placed in
the bath, not in contact with the nerve. The ICE was then implanted on the
proximal end. Preparation took between 1.5 and 2 hours.

2.3 Experimental Setup


Stimulation (STG4008, MultiChannel Systems, Germany) was controlled by
a custom made MATLAB script (running under MATLAB R2013b, Math-
Works, U.S.A.) which also handled synchronous recording.
The eCAPs obtained with the monopolar tungsten needle electrodes were
then amplified (gain = 50.000, PGA64 & MPA32I, MultiChannel Systems,
Germany) and sampled (fs = 20kHz, USB-6259, National Instruments, USA).

2.4 Experimental Stimulation Procedure


A series of 52 contact sites combinations was tested, 42 experimental (in
randomised order for each sample) and 10 for supramaximal stimulation (at
fixed time intervals). For each contact combination, stimulation was per-
formed with a sequence of gradually increasing, current controlled, charge
balanced pulses (0 to 3000μA, steps of 150μA; 100μs, 1000μs and 400μs for
A Combined ICE for Selective Recruitment 689

$ % &
$ & $
& $

&

' $ ( $

&

&

Fig. 3 The five types of contact combinations investigated in the experiments.


With reference to the primary (stimulating) phase, ”C” indicates the cathode, an
”A” indicates the anode. A) IEFA to a surface contact; B) Surface contact to IEFA;
C) From a surface contact site to its diametral opposite; D) From a surface contact
site to its neighbour; E) From a surface contact site to its second neighbour.

the cathodic, interpulse delay and anodic pulse, respectively). The sequence
was repeated ten times in each combination.
The different experimental combinations were limited to transversal bipo-
lar configurations due to time constraints. They were divided in 5 categories
(Fig. 3):

A Interfascicular contact site as cathode and a surface contact site as anode


(6 total).
B Surface contact site as cathode to the interfascicular contact site as anode
(6 total).
C Surface contact site as cathode to the diametral opposite contact site as
anode (6 total).
D Surface contact site as cathode to its neighbouring contact site as anode
(12 total).
E Surface contact site as cathode to its second neighbouring contact site as
anode (12 total).
Supramaximal stimulation of the nerve was conducted at the beginning
of the experiment and after each 10 combinations (ca. every 20 minutes) by
nonselective longitudinal stimulation using all contact sites in central ring of
the cuff as cathodes and the two full rings in the cuff as anodes, both with
and without the use of the IEFA as a cathode.

2.5 Data Processing


The stimulation artifacts present in all recordings were removed by replacing
the signal with the baseline in a window around the beginning of stimulation
(t0 − 0.5 ms to t0 + 2 ms); bandpass filtering (100-2000 Hz, conducted in two
690 A. Ranieri et al.

steps, an order 1375 highpass and an order 259 lowpass, both FIR equiripple
designs) was then applied, and median averaging was performed on responses
from all repetitions of the same stimulation current level. Linear regression
was used for evaluating drift in average Area under the curve (AuC) for neural
responses obtained with the maximum stimulation combinations over the
course of the experiment as an indicator for possible decay of the nerve. Then,
”relative recruitment” levels of each fascicle in each experimental combination
were calculated by dividing the AuC of each neural response (over a window
0 − 13 ms after stimulus initiation) by the maximum AuC obtained by the
closest maximum recruitment combination in time. These values were then
used to evaluate the fascicular selectivity in the different combinations and
current levels, by computing the following selectivity index [15], SIj :
N
μi
i=1,j=i
SIj = μj − (1)
N −1
μj is the relative recruitment of a target fascicle j, μi is the relative re-
cruitment of nontarget fascicle and N is the number of fascicles. Nontarget
fascicles were only included in the calculation when they exceeded 10% rela-
tive recruitment (μi > 0.1) to decrease the effect of noise in a large number
of nontargets. When target fascicles were not activated above 50% relative
recruitment (μj > 0.5) or when the calculated SIj did not exceed N1 , SIj
was set to N1 .
To evaluate the device selectivity of the ICE and the cuff the following
formula was used [16]:

N

SID = N max(SIj ) (2)
j=1

As the cuff constitutes a subset of the ICE (cuff + interfascicular elec-


trode), the overall performance of the ICE will always be equal or better
than the cuff. A statistical comparison between the two interfaces was there-
fore not performed.

3 Results
Results in all three experiments have shown an average activation threshold
of 1200 ± 100 μA, with no significant drift from the starting value (via linear
regression fit; slope coeff. β = 0 with p > 0.05 in all cases). Linear regression
was also performed on all three samples for the supramaximal stimulation
both with and without the use of the IEFA as a cathode; in both cases,
two out of three samples showed a statistically significant increase (slope
coeff. β = 0 with p < 0.05) in the order of 17% of the initial value over the
experimental time (80min).
A Combined ICE for Selective Recruitment 691

Fig. 4 The device selectivity SID of the ICE and the cuff combinations, C, D and
E (Fig. 3), f!or all three nerves and their mean. The blue bars (left) shows the
SID possible using all the contact sites of the ICE. The Red bars (right) shows the
SID for the combinations possible using only the cuff contact sites. The error bars
indicate the standard deviation.

The range for maximum selectivity of the fascicles in nerve 1-3 was 0.41-
0.07 (0.17), 0.93-0.22 (0.39) and 0.61-0.10 (0.25) respectively (max - min
(mean)).
The device selectivity SID of the whole electrode, the interfascicular con-
figurations (A and B (Fig. 3)), and the cuff configuration (C, D and E (Fig.
3)) were calculated for the three nerves. In all three experiments the device
selectivity of the ICE were higher than that of the cuff and interfascicular
combinations, showing that for each experiment the combinations possible for
the ICE increased selectivity. On average the ICE had an SID of 0.25 ± 0.10
(0.15, 0.36 and 0.23 for nerve 1-3, respectively), and the cuff alone had an
SID of 0.20 ± 0.11 (0.12, 0.33 and 0.17 for nerve 1-3, respectively). The mean
improvement in SID when using the ICE was 22.08% ± 13.60 (mean ± STD)
over the cuff combinations.
Combinations that included the IEFA as a cathode, A (Fig. 3), or anode, B
(Fig. 3), activated an average of 16.5 and 15.2 fascicles over the 50% threshold
with in the investigated current levels. First neighbour and second neighbour
combinations, D (Fig. 3) and E (Fig. 3), activated an average of 4.2 and 10.4
fascicles per combination using the same current levels. Diameteral combi-
nations, C (Fig. 3), activated on average 14.7 fascicles per combination. For
nerve 1-3 respectively 7, 3 and 7 first neighbour combinations did not acti-
vate any fascicles over the threshold. For second neighbour combinations the
numbers for nerve 1-3 was 2, 3 and 0 respectively. For the combinations that
included the IEFA the numbers for nerve 1-3 was 0, 0 and 1 respectively. For
diameteral combinations no combinations in any of the nerves were unable
to activate fascicles above the threshold.
692 A. Ranieri et al.

4 Discussion
The ICE design used in this study brought a 22.08 ± 13.60% improvement
on selectivity by adding a simple interfascicular contact, indicating that the
principle behind the ICE is sound. The lower number of fascicles activated
by each of the first and second neighbour combinations, compared with the
interfascicular combinations, indicate a difference in the area of stimulation
induced by the cuff and the ICE. Despite the large number of fascicles ac-
tivated by the IEFA combinations they still managed to add to the SId of
the ICE. Larger currents might allow one combination type to increase their
selectivity by increasing their average fascicles activation or decrease their
selectivity by increasing noise in the non-target fascicles.
Working with explanted samples means losing the anatomical link between
fascicles and the innervated structures, unlike previously used in vivo models,
such as living rabbits or rats. In comparison to such models, due to the higher
number of fascicles that it is possible to obtain direct recordings from, this in
vitro model is able to provide a different view to the muscle based selectivity.
The choice of how selectivity is quantified can greatly influence the results,
making comparisons between different studies and electrodes difficult. For
example, in the calculation of SIj , a 10% minimum activation threshold was
introduced to reduce the effect of noise in nontarget fascicles. This along with
the rather harass thresholds for activation of target fascicles have lead to an
overall lower selectivity but one that is more certainly the result of actual
activation.
No significant decay in neural response (as measured by AuC) or activa-
tion thresholds were observed; the increase in the neural response, observed
in two of three samples, could be a consequence of adaptation to the sur-
rounding environment over time, or simply recovery from the explantation
process. Longer experiments could therefore be designed, with more potential
for repeated measures or more complex experimental designs.
It is well known [17] [18] that the longitudinal components of current flow-
ing in a nerve can better activate single nerve fibers; stimulation between
longitudinally separated contacts could then combine the advantages of be-
ing able to reach deep fascicles and of having the current flow more parallel
to the individual fibers in the nerve. Further studies in this direction should
be carried out to better characterise the potential of the ICE.
Several new electrodes have been designed to improve or offer alternatives
to the well known cuff design, with the aim of developing more selective pe-
ripheral neural interfaces. An interfascicular electrode by [19] consisting of
longitudinally placed electrodes in a nylon tube achieved an overall selectiv-
ity as high as 0.98 in a study using in vivo rabbit sciatic nerves. Such elec-
trodes can be expected to have increased difficulty with stimulating fascicles
close to the surface in larger, polyfascicular nerves. The principle behind the
ICE shows potential in achieving better selectivity by improving on the well
known cuff design, at a small cost in invasivity. As mentioned above, similar
A Combined ICE for Selective Recruitment 693

conclusions have been drawn independently and using a different model [11],
supporting the idea that interfascicular electrodes can effectively be com-
bined with a cuff to increase the possible combinations and further improve
selectivity, partially addressing potential scaling issues of existing interfaces.

Acknowledgment. The authors would like to thank Aalborg University Hospital’s


Animal Laboratories personnel, Thomas Nielsen and Cristian Sevcencu for technical
assistance and guidance in extraction, as well as the possibility of extracting pig
nerves. This study was supported by The Obel Family Foundation and The Spar
Nord Foundation.

References
1. Navarro, X., Vivó, M., Valero-Cabré, A.: Neural plasticity after peripheral nerve
injury and regeneration. Progress in Neurobiology 82(4), 163–201 (2007)
2. Hunter, J.P.: The effect of tactile and visual sensory inputs on phantom limb
awareness. Brain 126(3), 579–589 (2003)
3. Flor, H.: Phantom-limb pain: characteristics, causes, and treatment. Lancet
Neurology 1(3), 182–189 (2002)
4. Flor, H., Denke, C., Schaefer, M., Grüsser, S.: Effect of sensory discrimination
training on cortical reorganisation and phantom limb pain. Lancet 357(9270),
1763–1764 (2001)
5. Huse, E., Preissl, H., Larbig, W., Birbaumer, N.: Phantom limb pain.
Lancet 358(9286), 1015 (2001)
6. Jensen, W., Micera, S., Navarro, X., Stieglitz, T., Guiraud, D., Divoux, J.L.,
Rossini, P.M., Yoshida, K.: Development of an implantable transverse intrafas-
cicular multichannel electrode (TIME) system for relieving phantom limb pain.
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gineering in Medicine and Biology Society, vol. 2010, pp. 6214–6217 (January
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7. Rossini, P.M., Micera, S., Benvenuto, A., Carpaneto, J., Cavallo, G., Citi, L.,
Cipriani, C., Denaro, L., Denaro, V., Di Pino, G., Ferreri, F., Guglielmelli, E.,
Hoffmann, K.-P., Raspopovic, S., Rigosa, J., Rossini, L., Tombini, M., Dario,
P.: Double nerve intraneural interface implant on a human amputee for robotic
hand control. Clinical Neurophysiology: Official Journal of the International
Federation of Clinical Neurophysiology 121(5), 777–783 (2010)
8. Navarro, X., Krueger, T.B., Lago, N., Micera, S., Stieglitz, T., Dario, P.: A
critical review of interfaces with the peripheral nervous system for the control
of neuroprostheses and hybrid bionic systems. Journal of the Peripheral Nervous
System: JPNS 10(3), 229–258 (2005)
9. Grill, W., Mortimer, J.: Stimulus waveforms for selective neural stimulation.
IEEE Engineering in Medicine and Biology Magazine 14(4), 375–385 (1995)
10. Tyler, D.J., Durand, D.M.: Functionally selective peripheral nerve stimulation
with a flat interface nerve electrode. IEEE Transactions on Neural Systems and
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11. Riso, R., Dalmose, A., Stefania, D., Schuttler, M.: Addition of an intrafascicu-
lar electrode at the site of application of a multipolar nerve cuff enhances the
opportunity for selective fascicular activation. In: 2001 Conference Proceed-
ings of the 23rd Annual International Conference of the IEEE Engineering in
Medicine and Biology Society, vol. 1, pp. 711–714. IEEE (2001)
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morphology of Danish landrace pigs and Göttingen mini pigs. In: Annual Con-
ference of the . . . , pp. 1–4 (2012)
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Configurations for Stimulation and Recording With an Interfascicular Inter-
face. IEEE Transactions on Neural Systems and Rehabilitation Engineering: a
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2013)
Integration of Neurodynamics
into Neurorehabilitation

Carlos Rodríguez-López1, Bibiana Da Rocha-Souto1, and Nora Kern2


1
UDC (University of La Coruña), Spain
2
Schule für Physikalische Therapie am AKH (Vienna), Austria

Abstract. Since the early stages in the Neurorehabilitation field both clinicians
and researchers had to deal with spasticity and the so-called spastic patterns as
limiting factors to the individuals´ daily life activities being the main cause of the
reduction in their level of participation.
Nowadays therapeutic approaches are focused on clinical results and there are
several ideas about how to lower spasticity or hypertone and how to measure it
before and after a treatment, like the Ashworth modified muscle tone measurement
scale. Also there are different surgical approaches, such as rhizotomies or tendon or
muscles cut, which try to deal with this patterns and a lot of discussion about the
outcome of this operations in terms of functionality. Yet, nobody has reached a
convincing explanation about the origin of spastic positions and spasticity further
than the lack of inhibition after damage in the Central Nervous System (CNS) and
its tracts. What we want to show is a complete new way of understanding these
patterns and the whole concept of spasticity through the profound analysis of the
neurodynamic tests and their components.

Keywords: spasticity, neurodynamics, spastic pattern, median nerve, clinical


reasoning.

1 Introduction

Further than methodologies and techniques that are available for therapists working
in the Neurologic field, we think that we are able to show another explanation for
many of the signs and symptoms that patients are showing after a central lesion and
which are limitating them in their daily life activities (DLA) and their participation.
One of the main items is lack of muscle control, perhaps due to spasticity,
showing abnormal movement patterns.
Integrating the Peripheral Nervous System (PNS) into our clinical reasoning, it
allows us to understand a lot of the patients‘ reactions like when, how and why
they show changed movement patterns or why they are unable to fulfill a certain
task in one position but not in another. It underlines the importance of starting
therapy very early to minimize the onset of pathological or non functional
patterns. Furthermore, considering the PNS and its characteristics could

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 695
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_97, © Springer International Publishing Switzerland 2014
696 C. Rodríguez-López, B. Da Rocha-Souto, and N. Kern

gain relevance as a new item to take into account in surgical interventions


and orthopaedics, being part of the treatment of individuals after a lesion to
their CNS.

2 Neurodynamics and Neurorehabilitation

If we take a look back to the onset of manual therapy, we can see that therapists
focused mainly on joints and ligaments, not including the PNS as one possible
source for the signs and symptoms that individuals asking for therapy were
complaining of. [1]
Nowadays there are several studies on the biomechanical and physiological
properties of the peripheral nervous system [2], [3],[4],[5] and it has become part of
the clinical reasoning process to analyze the origin of pain syndromes in orthopaedic
patients, but it has never really been introduced into Neurorehabilitation.
Back in the sixties, the neurosurgeon Alf Breig [6] was the pioneer in
remarking the importance of understanding the movement of the nerves. His
investigations lead the clinicians consider the adverse mechanical tension within
the nervous system. . In time, researchers started to analyse extra and intraneural
nerve movements [7], [8]. They found an interdependent influence between the
ability of a nerve to glide and slide freely against all kind of mechanical interface,
and the afferent and efferent impulse transport. [9]
Most of Traumatic Brain Injury (TBI) or stroke patients have both motor and
sensory impairments that can lead to altered perception, “learned non use”,
movement disorders and many other symptoms that are usually related directly to
the central lesion. In fact, therapists working with those patients know that some
of the problems appear only after a long time after the onset of the lesion, so we
could see them as secondary problems.

3 Spasticity and Spastic Patterns


Nowadays the idea of describing spasticity as the main negative outcome after a
stroke is unpopular. More significance has the description of the Upper Motor
Neuron Syndrome (UMNS), [10], [11] divided into plus and minus symptoms,
from which spasticity is only one of the multiple plus symptoms.
The actual literature shows more evidence for treating the minus symptoms to
regain motor function and daily life performance rather than focusing too much on
the plus symptoms. Regarding the list of all the plus and minus symptoms, it can
be seen as a summary of lack of correct impulse transport- either too much, not
precisely enough or not well regulated, or too little.
Considering the fact that the function of peripheral nerves is dependent upon
their gliding within the body, it makes much sense to introduce neurodynamic
tests as a basic assessment tool after a central lesion. That includes analysing the
ability of peripheral nerves to adapt to body movements as well as to measure the
amount of their mechanosensitivity.
Integration of Neurodynamics into Neurorehabilitation 697

The idea of integrating neurodynamics into Neurorehabilitation can help to


understand many of the most common symptoms patients are suffering from after
a central lesion. Target tissues, like muscles for instance, will function more
effectively, if an adequate impulse transport is guaranteed. In some positions there
is more tension on the PNS, therefore the patient cannot activate the muscle as
good as in other positions and that ends up in poor execution of DLA. So the
function of the nervous system determines the function of its target tissues and
vice versa. Some researchers like Bernstein have already underlined the
importance of considering body biomechanics to evaluate the function of the
nervous system.
The theoretical separation between CNS and PNS has been useful in matters of
learning how it works but the fact, as D. Butler stated in 1991, is that there is not
such a separation. When it comes to tissue, the neurotransmitters along the whole
system and the electrical communication between neural cells remark the idea of
considering the nervous system as an organ. [12]
Both D. Butler and M. Shacklock have mentioned unload positions (or off
loaders) for the nervous system, those described as positions the patients are
choosing in order to get rid of pain. These positions are very similar to those we
find in neurologic patients, here usually called spastic patterns.
If we analyze for instance the test for the median nerve, and look at every
single joint position (defined as “component” in literature) that has to be
performed in order to unfold the nerve to its limit, we find that the completely
unloading position (the opposite of the test position) is exactly the typical spastic
flexion pattern.

Joint Test components Unloaded position


ULNT 1 (spastic pattern)

Glenohumeral Abduction Adduction

Extension Flexion

External rotation Internal rotation

Elbow Extension Flexion

Forearm Supination Pronation

Wrist Dorsiflexion Wrist extension

Fingers Extension Flexion


Thumb Abduction Adduction

Fig. 1 ULNT 1 (Upper Limb Neural Test). Median nerve.


698 C. Rodríguez-López, B. Da Rocha-Souto, and N. Kern

As Nora Kern states [13], the unloading position for this particular nerve is
precisely the most common pattern in the upper limb we observe with patients. In
the literature it is referred to as a typical pathological pattern or associated reaction
or even an involuntary movement. Using the idea of unloading positions for
peripheral nerves, we might think that the so called spastic, associated or mass
pattern is just a mechanical problem, a restriction of the ability of the nerve to
adapt to a movement.
With patients after a central lesion we first have to do the test on the non
affected side to get a general idea of the expectable mobility and of the patient´s
reactions and to give him the idea of the testing process. On the more affected
side, we often have to stop after only few components because of the early onset
of the symptoms like intense pulling, stretching, pain or obvious evasive
movements at other parts of the patient´s body. Patients describe it like a elastic
string that is pulling and holding them back when they are trying to move
themselves, but sometimes even when they are getting moved passively from
helpers or therapists.
The edema that occurs in the brain after a lesion forces the periphery to avoid
too much mechanical input to the CNS, and that could be seen as a self protecting
effect.
This as well means that there is no proper impulse transport to the different
target tissues (muscles, organs, joint receptors and all other body tissues). Also,
the lack of selective muscle activity can lead to pulling, stretching or squeezing of
the nerves locally.
Even the non-use aspect makes sense because if there is a disturbed impulse
transport, there is a lack of information coming from the periphery to the brain as
with hypaesthesia, or a distorted feedback, like allodynia or paraesthesia and that
might result in a wrong representation of the body in the brain, which leads to a
bad perception.
To summarize: all these observations and thoughts lead us to think that spastic
patterns are the result of the nervous system protecting itself from too much
mechanical input (as this is the fact with hypermechanosensitivity). Therefore
over time it loses the ability to adapt to all kind of body movements, because the
intrinsic and extrinsic connective tissues are losing their flexibility without being
moved sufficiently. The less movement, the more tissue restrictions, the worse the
impulse transport will be and that leads to less control over movement: a vicious
circle. However we manage to interrupt this ongoing process, either by training
more selective muscle function (and it has to be selective, in order to protect a
peripheral nerve from getting too much local stress), or by mobilising all body
tissues including peripheral nerves, or by a combination, always as a result of a
good clinical reasoning process, the ways to choose are various. But in many
times we are more successful and faster with our treatment effects if we consider
the mobility restriction of peripheral nerves as a possible fact as well.
Integration of Neurodynamics into Neurorehabilitation 699

4 Conclusion

Considering peripheral nerves with their lost ability to adapt to movements and
their increased mechanosensitivity, it leads to review common explanations about
spasticity, spastic and non physiological movement patterns individuals are
showing after a lesion to the central nervous system, and to the sometimes not
satisfying treatment approaches for these phenomena. It opens the doors to
develop further treatment approaches in order to gain a better outcome on
function, activity and participation level for the affected individuals.

References
[1] Butler, D.: The sensitive Nervous System. Noigroup Publications (2006)
[2] Elvey, R.: Physical evaluation of the peripheral nervous system in disorders of pain
and dysfunction. J. Hand. Ther. 10(2), 122–129 (1997)
[3] Coppieters, M.W., Stappaerts, K.H., Wouters, L.L., Janssens, K.: The immediate
effects of a cervical lateral glide treatment technique in patients with neurogenic
cervicobrachial pain. J. Orthop. Sports Phys. Ther. 33(7), 369–378 (2003)
[4] Butler, D.: Adverse mechanical tension in the nervous system: a model for assessment
and treatment. Aust. J. Physiother. 35(4), 227–238 (1989)
[5] Coppieters, M.W., Alshami, A.: Longitudinal excursion and strain in the median
nerve during novel nerve gliding exercise for carpal tunel syndrome. Journal of
Orthopaedic Research 25(7), 972–980 (2007)
[6] Breig, A.: Biomechanics of the central nervous system. Almqvist and Wiksell (1960)
[7] Rydevik, B., Lundborg, G.: Permeability of Intraneural Microvessels and Perineurium
Following Acute, Graded Experimental Nerve Compression
[8] Tanoue, M., Yamaga, M., Ide, J., Takagi, K.: Acute stretching of peripheral nerves
inhibits retrograde axonal transport. J. Hand Surg. Edinb. Scotl. 21(3), 358–363
(1996)
[9] Shacklock, M.: Neurodynamics. Physiotherapy (1995)
[10] Taylor, S. (ed.): On certain relations of the cerebrum and cerebellum (On rigidity of
hemiplegia and on paralysis agitans), 2nd edn. Selected Writings of J.H. Jackson.
Basic Books, New York (1958)
[11] Fries, W., Freivogel, S., Beck, B.: Spastik. In: Frommelt, P., Grötzbach, H. (Hrsg.):
Neuro Rehabilitation 2. Auflage in Druck (2005)
[12] Butler, D.: Movilización del sistema nervioso. Paidotribo, Barcelona (2002)
[13] Kern, N.: Integration der Neurodynamik in die Neurorehabilitation (INN). Zeitschrifit
für Physiotherapeuten 62(2), 59–64 (2010)
Movement Related Cortical Potentials and
Sensory Motor Rhythms during Self Initiated
and Cued Movements

Andrej Savić1, Romulus Lontis3, Ning Jiang4, Mirjana Popović2, Dario Farina4,
Kim Dremstrup3, and Natalie Mrachacz-Kersting3
1
Signals and Systems Department at University of Belgrade,
School of Electrical Engineering and Tecnalia Serbia Ltd., Belgrade, Serbia
{andrej_savic,mpo}@etf.rs
2
Signals and Systems Department at University of Belgrade,
School of Electrical Engineering, Belgrade, Serbia
mpo@etf.rs
3
Department of Health Science and Technology at Aalborg University,
9220 Aalborg Ø, Denmark
{lontis,kdn,nm}@hst.aau.dk
4
Department of Neurorehabilitation Engineering,
Bernstein Focus Neurotechnology Göttingen,
Bernstein Center for Computational Neuroscience,
University Medical Center Göttingen, Georg-August University,
Göttingen, Germany
{ning.jiang,dario.farina}@bccn.uni-goettingen.de

Abstract. In this study we have explored the two EEG phenomena that
accompany movement preparation and execution: movement related cortical
potentials (MRCP) and event-related desynchronization/synchronization
(ERD/ERS). The experiments comprised the two conditions for motor task
initiation, self paced and cued. The aim of the study was to explore how the
introduction of the cue influences the morphological features of the MRCP and
ERD/ERS curves. Preliminary results of the tests in 9 healthy subjects showed
statistically significant differences in MRCP components for the two conditions
and no significant differences in ERD/ERS morphology. Brain-Computer Interface
algorithms for online control of assistive devices for restoration of movement may
benefit from these results.

1 Introduction
Brain Computer Interface (BCI) technology has been used to restore lost motor
function in stroke patients or other traumatic brain disorders by helping to guide
activity-dependent brain plasticity [1]. Treatments that combine functional
electrical stimulation (FES) or assistive robots with motor tasks (imagined or
attempted) are expected to be more effective than using them separately [2]. EEG

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 701
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_98, © Springer International Publishing Switzerland 2014
702 A. Savić et al.

signal acquisition can be used for detecting the changes that accompany these
tasks and a BCI device can convert those changes into commands that trigger FES
or activate an assistive robotic system [3].
Two types of EEG movement related signals have been investigated as potential
candidates for the control of the restorative BCI system based on attempted or
imagined movements: event related desynchronization/ synchronization
(ERD/ERS) of the sensory motor rhythms and movement related cortical
potentials (MRCP) [4, 5]. Although both responses originate in the related cortical
regions and display common temporal features, their magnitudes and spatial
distributions appear to be independent of each other, which suggests that the
physiological mechanisms governing these two signals are different and may
represent distinctive aspects of motor cortex activation [6]. Both modalities have
certain advantages and disadvantages when used as control signals for BCI that
appear to be of a complementary nature. ERD/ERS have often been implemented
for asynchronous BCI control since in trained users they can be accurately
detected on a single-trial basis [7, 8]. Additionally, mu ERD initiates 0.5-2
seconds prior to movement giving the possibility of online detection of movement
intention [9, 10].
Precise temporally synchronized contingent sensory feedback is essential, for
Hebbian-based restorative BCI control [5]. The main drawback of ERD/ERS as a
potential control signal for such restorative BCI is the fact that they do not provide
information on precise timing of the stages during movement preparation/execution
[6]. The MRCP, on the other hand, comprises precise phases corresponding to the
early preparation, initiation and execution of movement [11]. Therefore, with
MRCPs, these phases can be exactly detected, which is crucial for the
synchronization of the motor commands with the sensory input (i.e. electrical
stimulus, movement of the orthosis) [5]. Recent publications show the possibility of
movement intention detection from single trial MRCP [12, 13]. However, in the
past they were rarely considered as a control signal for asynchronous restorative
BCI due to the low signal to noise ratio, which limits the detection accuracy in
online studies [2, 10].
We believe that MRCPs and ERD/ERS can be used in a joint mode considering
they are complementary to each other in decoding the real and imaginary motor
tasks. A hybrid BCI that complements advantages from both, MRCPs and ERD
could make the system more robust and suitable in neural rehabilitation. For
example, ERD may be used for asynchronous detection of movement intention
followed by MRCP-based FES triggering in a synchronized manner with detection
of the following negative peak of the MRCP. The presented results are a part of
an ongoing study with the aim of exploring features of both MRCP and ERD/ERS
to be used for the control of restorative BCI device.
The treatment of combining motor imagery (MI) or motor attempt with
precisely temporally synchronized sensory feedback requires repetitive executions
of attempted/imagined motor tasks. This can be accomplished in an asynchronous
(self-paced) or synchronous (cue-based) mode. Within this study the two
paradigms often used in BCI control have been investigated and compared,
namely the cued and the self-paced real movements.
Movement Related Cortical Potentials and Sensory Motor Rhythms 703

2 Methods

Nine healthy (6 male, 3 female, 21-43) subjects participated in this study. The
EEG was recorded using the active electrode system (ActiCap, Brain Products,
Germany) and gUSBamp EEG amplifier (gTec GmbH, Germany). 28 EEG
channels were acquired at a standard 10/20 locations: F1, F2, F3, Fz, FC1, FC2,
FC3, FC4, FCz, C1, C2, C3, C4, C5, Cz, PC1, PC2, P3, P4, P5, Pz, P1, P2, P3, P5,
Pz. The ground was located on AFz and the reference on the left earlobe. Data
were sampled at 256 Hz. Hardware band-pass filter cut-off frequencies were 0.01
Hz and 30 Hz. Impedances of the skin-electrode junctions were kept below the
recommended values given by the manufacture of the active electrode system. The
participants were seated in a chair with a computer screen in front of them at a
distance of 1.5 m. Subjects were instructed to perform brisk (~1 s) palmar grasp
movements with the right hand consisting of hand opening (all fingers extension)
followed by a hand closing (all fingers flexion). The subjects performed the same
task in the two experimental conditions, self-paced and externally cued. In
the self-paced condition, the decision on when to perform the task was left to the
subjects’ own will. In the other condition the series of cues were presented to
the subjects on the computer screen. The subjects were instructed to gaze at the
fixation cross in the middle of the screen. At certain time points the arrow pointing
at the right direction appeared over the cross. The pauses between the two cues
(arrow appearances) varied between 8 and 12 s. In each experimental condition,
the subjects performed a total of 50 movements. Electromyographic (EMG)
activity was recorded from the extensor carpi radialis (ECR) and flexor carpi
radialis (FCR) muscles using two bipolar EMG derivations. EMG signals served
as a reference for extracting the exact onset of the movements.

3 Signal Processing

3.1 MRCP Extraction


Offline EEG processing was conducted using custom MATLAB (The Mathworks,
Natick, MA, U.S.A.) routines. EEG signals from all channels were low-pass
filtered using a zero-phase 2nd order Butterworth filter with 6 Hz cut-off
frequency. EEG channel data were then segmented into epochs ranging from 2
seconds before (-2 s) to 1.5 seconds after (+1.5 s) the movement onset. The onsets
of the movements were extracted from the recorded EMG signals. The baseline
was corrected in all EEG channels by subtracting from each epoch the mean value
of the signal in the interval -2 to -1.5 s. Epochs contaminated with ocular-
movements and/or other artefacts were rejected from further analysis if the
absolute value of the signal from any of the channels exceeded a threshold
manually determined for each subject from a range 40 – 60 µV. For each subject a
minimum of 30 MRCP trials per condition were selected for further averaging.
704 A. Savić et al.

F5 F3 F1 Fz F2

FC5 FC3 FC1 FCz FC2 FC4

C5 C3 C1 Cz C2 C4

PC5
PC3 PC1 PCz PC2 PC4

10 (μV)
P5 P3 P1 Pz P2
0

-10
-1 0 1 (s)

Fig. 1 – Grand average MRCP curves for 28 channels. Blue curves represent the self-paced
and green curves the cued condition.

The individual movement related cortical potential (MRCP) was calculated by


averaging all trials over each subject in both experimental conditions. Grand
average MRCP curves over all subjects tested for 28 channels are presented in
Figure 1.

3.2 ERD/ERS Curves Extraction


EEG signals from each subject were band-pass filtered using a zero-phase 2nd
order Butterworth filter of 3 Hz bandwidth with 7 Hz being the minimal low cut-
off frequency and 13 Hz the maximal high cut-off frequency. For finding the
subject specific frequency band within the alpha band (7-13 Hz) with most
pronounced movement related ERD, we selected the sub band with the highest
value of power difference between the intervals -1 s to 0 s (pre movement band-
power) and 0 s to 1 s (movement execution band-power). Band-pass filtered
signals were squared and smoothed in a windows of 100 ms. These band-power
signals were segmented in the same manner as the MRCP (-2 s to 1.5 s). The same
subset of trials used for MRCP averaging was used for ERD/ERS analysis.
Additional epochs were excluded based on a threshold manually set on the signal
band-power of each subject. For each subject, a minimum of 30 ERD/ERS trials
per condition were used for averaging. Trials were averaged according to
conditions and the relative ERD/ERS power for each average was calculated
according to the following equation:
100
/ , ,
Movement Related Cortical Potentials and Sensory Motor Rhythms 705

where ERD/ERS(t) is a percentage value of ERD or ERS (ERD are the negative
and ERS the positive values) at each time point t of the epoch, A is the power
within the frequency band of interest at time point t, and the R is a mean power in
the same band over a reference time interval, the same as the baseline in the
MRCP processing, t1 is a starting time point of epoch interval (-2 s) and t2 the
ending time point of epoch interval (1.5 s). Grand average ERD/ERS curves over
all subjects tested for 28 channels are presented in Figure 2.
For the statistical analysis, three time intervals of interest were selected: I1 (-1 s
to -0.5 s), I2 (-0.5 s to 0 s) and I3 (0 s to 0.5 s). The mean amplitude values in
these intervals were calculated for MRCP and ERD/ERS curves of each subject.
Paired-sample t-tests were used to compare these means for the self paced and
cued conditions.

F5 F3 F1 Fz F2

FC5 FC3 FC1 FCz FC2 FC4

C5 C3 C1 Cz C2 C4

PC5 PC3 PC1 PCz PC2 PC4

(%)
P5 P3 P1 Pz P2
50

-50 -1 0 1 (s)

Fig. 2 Grand average ERD/ERS curves for 28 channels. Blue curves represent the self-
paced and green curves the cued condition.

4 Results and Conclusions

The results of the statistical analysis were obtained for each channel. Analysis of
the MRCPs showed statistically significant differences (p<0.05) between the self-
paced and cued conditions, where lower voltages in the self paced task were found
in the interval I1 for channels: FC1, FC2, FCz, C1, Cz, CP2, CP3; in interval I2
for channels: F1, F3, Fz, FC1, FC2, FC3, FC4, FC5, FCz, C1, C2, C3, C5, Cz,
PC1, PC2, PC3, PC5, PCz, P1, P3, Pz; and in interval I3 for channels: F1, F3, Fz,
FC1, FC2, FC3, FC4, FC5, FCz, C1, C2, C3, C5, Cz, PC1, PC2, PC3, PC5, PCz,
P1, P3, P5.
For the ERD/ERS curves, no statistical differences were found between the two
conditions in any of the predefined intervals.
706 A. Savić et al.

The results show that introducing a go-cue, that is, the cue which demands
instantaneous motor reaction of the subject, induces significant differences in
MRCP morphology before and during the movement execution in the regions of
interest. Less pronounced negativity in the movement preparation phase (interval
I2) was expected for cued movements since the planning and preparation phase
was shortened by the introduction of the reaction task. However, during the
movement execution (interval I3), these changes persist in previously stated
channel subsets. ERD/ERS curves on the other hand were not affected by the
introduction of the cue. These results indicate that the cueing could affect the
MRCP-based MI detection, also. Therefore, the type of cueing should be carefully
considered when designing the potential MI based restorative BCIs. These
preliminary results may be of importance for improvement of BCI protocols and
upgrading online control of assistive devices.

Acknowledgment. The authors would like to thank the volunteers who participated in the
measurements and tests. This work was partly supported by the Ministry of Education,
Science and Technological Development, Belgrade, Serbia, Project no. 175016, and by the
Tecnalia Research & Innovation, Spain.

References
[1] Daly, J.J., Wolpaw, J.R.: Brain-computer interfaces in neurological rehabilitation. The
Lancet Neurology 7(11), 1032–1043 (2008)
[2] Ang, K.K., Guan, C.: Brain-computer interface in stroke rehabilitation. Journal of
Computing Science and Engineering 7(2), 139–146 (2013)
[3] Wolpaw, J.R., Birbaumer, N., McFarland, D.J., Pfurtscheller, G., Vaughan, T.M.:
Brain–computer interfaces for communication and control. Clinical
Neurophysiology 113(6), 767–791 (2002)
[4] Caria, A., Weber, C., Brötz, D., Ramos, A., Ticini, L.F., Gharabaghi, A., Braun, C.,
Birbaumer, N.: Chronic stroke recovery after combined BCI training and
physiotherapy: a case report. Psychophysiology 48(4), 578–582 (2011)
[5] Mrachacz-Kersting, N., Kristensen, S.R., Niazi, I.K., Farina, D.: Precise temporal
association between cortical potentials evoked by motor imagination and afference
induces cortical plasticity. The Journal of Physiology 590(7), 1669–1682 (2012)
[6] Toro, C., Deuschl, G., Thatcher, R., Sato, S., Kufta, C., Hallett, M.: Event-related
desynchronization and movement-related cortical potentials on the ECoG and EEG.
Electroenceph. Clin. Neurophysiol. 93, 380–389 (1994)
[7] Pfurtscheller, G., Müller-Putz, G.R., Pfurtscheller, J., Rupp, R.: EEG-based
asynchronous BCI controls functional electrical stimulation in a tetraplegic patient.
EURASIP Journal on Applied Signal Processing, 3152–3155 (2005)
[8] Leeb, R., Friedman, D., Muller-Putz, G.R., Scherer, R., Slater, M., Pfurtscheller, G.:
Self-paced (asynchronous) BCI control of a wheelchair in virtual environments: a case
study with a tetraplegic. Computational Intelligence and Neuroscience 2007, Article
ID 79642, 8 (2007)
[9] Neuper, C., Wörtz, M., Pfurtscheller, G.: ERD/ERS patterns reflecting sensorimotor
activation and deactivation. Progress in Brain Research 159, 211–222 (2005)
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[10] Bai, O., Rathi, V., Lin, P., Huang, D., Battapady, H., Fei, D.-Y., Schneider, L.,
Houdayer, E., Chen, X., Hallett, M.: Prediction of human voluntary movement before
it occurs. Clinical Neurophysiology 122(2), 364–372 (2011)
[11] Deecke, L., Grozinger, B., Kornhuber, H.H.: Voluntary finger movements in man:
cerebral potentials and theory. Biol. Cybern. 23, 99–119 (1976)
[12] Niazi, I.K., Jiang, N., Tiberghien, O., Feldbæk-Nielsen, J., Dremstrup, K., Farina, D.:
Detection of movement intention from single-trial movement-related cortical
potentials. Journal of Neural Engineering 8(6), 66009 (2011)
[13] Xu, R., Jiang, N., Lin, C., Mrachacz-Kersting, N., Dremstrup, K., Farina, D.:
Enhanced Low-latency Detection of Motor Intention from EEG for Closed-loop
Brain-Computer Interface Applications. IEEE Transactions on Biomedical
Engineering 61(2), 288–296 (2013)
Use of Dynamic Movement Orthoses as
Rehabilitative Method to Improve Gait Stability
in Ataxic Patients

Mariano Serrao1,2 Alberto Ranavolo3,*, Carlo Casali2, Silvia Mari1,


Carmela Conte1, Francesco Draicchio3, Giorgio Sandrini4, and Francesco Pierelli2
1
Rehabilitation Centre Policlinico Italia, Piazza del Campidano 4, Roma 00162, Italy
2
Department of Medical and Surgical Sciences and Biotechnologies,
Sapienza University of Rome, Polo Pontino, via Faggiana 34, 40100, Latina, Italy
3
INAIL, Department of Occupational Medicine, via Fontana Candida 1,
00040 Monte Porzio Catone, Italy
a.ranavolo@inail.it
4
IRCCS ‘‘C. Mondino Institute of Neurology” Foundation,
via Mondino, 2, Pavia 27100, Italy

Abstract. Patients with cerebellar ataxia have an irregular gait with a high
variability of all time–distance parameters and wide trunk oscillations,
alterations linked to dynamic instability. In order to reduce such instability, we
propose the use of dynamic movement orthoses (DMO). Thus, we aimed at
quantitatively evaluating the effect of the DMO use on gait in a sample of ataxic
patients. Gait analysis of 10 ataxic patients was performed without and with the
customized DMO. In addition to the joint kinematics, the variability of spatio-
temporal parameters, as well as shoulder and pelvis ranges of motion in the
anterior-posterior and medio-lateral directions were investigated. With DMO,
ataxic patients showed a reduction of the variability of the spatio-temporal
parameters and a reduction of shoulder and pelvis range of motion in the medio-
lateral direction. Moreover, knee and ankle joint kinematics was improved by the
use of DMO.

1 Introduction

Patients with cerebellar ataxia typically exhibit an irregular, unsteady, stumbling


gait characterized by irregular steps, wide base of support and increased
variability of gait parameters [1], [2], alterations known to be linked to a high falls
risk. Moreover, greater upper body oscillations have long been reported in
literature as a clinical feature of ataxia [3]. Such wider upper body oscillations,
moving the center of mass at the edges of the base of support, may generate
instability. It has been suggested that ataxic patients, in order to control such

*
Corresponding author.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 709
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_99, © Springer International Publishing Switzerland 2014
710 M. Serrao et al.

instability caused by the loss of cerebellar functions, adopt a strategy based on


increased antagonistic muscle co- activation [4]. However, such compensatory
mechanism, carries some negative effects, such as the increased metabolic
cost and the risk of cartilage degeneration [5], [6]. Thus, it would be useful in
ataxic patients to use specific devices for the trunk stabilization during walking.
Ataxic patients may benefit from elastic or semi-rigid orthoses that can reduce the
axial oscillations on the sagittal and frontal planes without constraining the lower
limb movements during walking.
Dynamic movement Lycra orthoses (DMO) have been used in recent years as
a treatment tool for children with motor and posture impairments, such as
scoliosis and cerebral palsy [7], [8]. These elastic orthoses (suits) are made to
measure to achieve a snug fit so that the increased pressure on certain muscle
groups improves proprioception and facilitates the joint movements. Moreover,
the resistance created by additional layers of reinforcing material adds a
biomechanical influence to constraint/stabilize body segments (e.g. trunk). As a
result, the DMO improve function from better posture, increase stability and
reduce involuntary movements.
We hypothesized that patients with cerebellar ataxia may benefit from the
use of DMO in terms of gait stability mainly by improving the trunk control.
Thus, the aim of this work was to investigate the effect of the use of DMO on
gait variability and trunk oscillations in a sample of ataxic patients.

2 Material and Methods

2.1 Patients
A sample of 10 patients (8 males, 2 females; mean age: 49.9±9.5 years) with
cerebellar ataxia was enrolled in the study. Six had a diagnosis of autosomal
dominant ataxia (spinocerebellar ataxia, SCA; 3 patients with SCA1 and 3
patients with SCA2), while the other 4 had sporadic adult onset ataxia of
unknown aetiology (SAOA). Ten age- matched healthy subjects (8 males, 2
females; mean age: 51.4±11.1 years) were also enrolled and considered as
control group.

2.2 Dynamic Movement Orthoses


The Lycra suits (Figure 1) were individually made for each subject according to
their anthropometric measures. Extra layering was provided in order to reduce
involuntary trunk movements in the sagittal and frontal planes. Each panel or
section of the Lycra material is measured using specific tensions and directions
of pull to support the patient's need for maintaining biomechanical alignment. At
the shoulder, the DMO is measured to provide a snug fit and to support the
shoulder girdle, in order to improve the control of movement and function. Zips
Use of Dynamic Movement Orthoses as Rehabilitative Method 711

were present where necessary but kept to the minimum to preserve traction. Lycra
DMO usually take 2 to 5 minutes to put on and have appropriate apertures for
toileting. None of the enrolled patients was under rehabilitative treatment, and all
of them were told to perform their common daily activity when wearing the
DMO.

Fig. 1 One ataxic patients, wearing the DMO

2.3 Gait Analysis


Two gait analysis sessions were performed for each patient: a first session
before they received the DMO (DMO-) and a second session after one month of
continuous use of the Lycra suit. In the second session, the gait analysis was
performed while wearing the DMO (DMO+). One gait analysis session was also
performed for the control group.
An optoelectronic motion analysis system (SMART-D System, BTS, Italy)
consisting of 8 infrared cameras (300 Hz) was used to detect the movements
of 22 reflective spherical markers placed over anatomical landmarks according
to Davis et al [9]. Anthropometric data were collected for each subject [10].
Participants were required to walk barefoot at self-selected speed along a
walkway approximately 10 m in length.

2.4 Data Analysis


Three-dimensional marker trajectories were acquired using a frame-by-frame
tracking system (SMART Tracker - BTS, Milan, Italy). Data were processed
using 3-D reconstruction software (SMART Analyzer, BTS, Milan, Italy).
Kinematic data were normalized between two consecutive heel strikes and were
analyzed considering the right and left limb together. The following spatio-
temporal parameters and their coefficient of variation (CV) were considered for
712 M. Serrao et al.

Fig. 2 Spatio-temporal parameters, and the relevant CV, in DMO- and DMO+ conditions
and in controls. * = p<0.05

the statistical analysis: step length and width, stance, swing and double support
percentage duration. Ranges of motion (ROM) in the sagittal plane of hip, knee
and ankle were also considered. In order to have a measure of the trunk
oscillations, we also included the ROMs of shoulder and pelvis in the sagittal,
frontal and transverse plane. Moreover, the anterio-posterior and medio-lateral
displacements of the center of pelvis and center of shoulder were measured.
The non-parametric Wilkoxon test for paired samples was used to investigate
differences between the two sessions in the analyzed variables. Differences
between ataxic patients and controls were not statistically investigated, but data
of healthy subjects are reported in the results section in order to provide a
reference value for each parameter. A p-value less than 0.05 was considered
statistically significant.
Use of Dynamic Movement Orthoses as Rehabilitative Method 713

Fig. 3 At the top of the figure, center of shoulder and center of pelvis displacements in the
medio-lateral and anterior-posterior directions are depicted. At the bottom, shoulder and
pelvis ROMs in the sagittal (tilt), frontal (obli.) and transverse (rot.) plane are illustrated. *
= p<0.05.

3 Results

Spatio-temporals parameters values were not modified (all, p>0.05) with the use
of DMO, whereas a significant difference was revealed for the CV of stance
and swing percentage duration (Figure 2). A significant reduction of the ROM
of the center of shoulder and pelvis in the medio- lateral direction was found with
the DMO (Figure 3). As regards the angular ROMs, a significant lower value
was obtained for the pelvic tilt in the DMO+ respect to DMO- (Figure 3).
Moreover, significant increases in knee and ankle ROM in the sagittal plane
was observed in DMO+ compared with DMO- (Figure 4). Hip flexion-
extension ROM, instead, was not influenced by the use of DMO.
714 M. Serrao et al.

Fig. 4 Hip, knee and ankle joint ranges of motion in the sagittal plane. * = p<0.05.

4 Discussion and Conlusions

In this preliminary study, we investigated the effect of the use of DMO to


restraint trunk movement and reduce gait variability in a sample of ataxic
patients. Our findings indicate that even though the spatio-temporal parameters
were not influenced by the use of Lycra suits, the trunk oscillations and gait
variability were reduced. In our study all patients declared to be more stable
and safer when performing daily life activities wearing the DMO and a less
staggering gait was noted by their relatives. Since no rehabilitative treatment
was followed by patients during the trial period (1 month), the observed gait
parameters improvements may be attributed to the use of DMO. Thus, we propose
to use the DMO in the neurorehabilitation of cerebellar ataxias to improve the
trunk control and gait stability. However, the DMO may be considered as a
prototype that can be modified in terms of material characteristics, textile
layers, elastic components and so on aimed at improving gait stability in ataxic
patients. Moreover, since this is a preliminary study, further investigations are
needed to more thoroughly evaluate the effect of DMO use in ataxic patients.

References
[1] Palliyath, S., Hallett, M., Thomas, S.L., Lebiedowska, M.K.: Gait in patients with
cerebellar ataxia. Mov. Disord. Off. J. Mov. Disord. Soc. 13(6), 958–964 (1998)
[2] Serrao, M., Pierelli, F., Ranavolo, A., Draicchio, F., Conte, C., Don, R., Di Fabio, R.,
LeRose, M., Padua, L., Sandrini, G., Casali, C.: Gait pattern in inherited cerebellar
ataxias. Cerebellum Lond. Engl. 11(1), 194–211 (2012)
[3] Holmes, G.: The Cerebellum of Man. Brain 62(1), 1–30 (1939)
Use of Dynamic Movement Orthoses as Rehabilitative Method 715

[4] Mari, S., Serrao, M., Casali, C., Conte, C., Martino, G., Ranavolo, A., Coppola, G.,
Draicchio, F., Padua, L., Sandrini, G., Pierelli, F.: Lower Limb Antagonist Muscle
Co-Activation and its Relationship with Gait Parameters in Cerebellar Ataxia.
Cerebellum Lond. Engl. (2013)
[5] Peterson, D.S., Martin, P.E.: Effects of age and walking speed on coactivation and
cost of walking in healthy adults. Gait Posture 31(3), 355–359 (2010)
[6] Griffin, T.M., Guilak, F.: The role of mechanical loading in the onset and progression
of osteoarthritis. Exerc. Sport Sci. Rev. 33(4), 195–200 (2005)
[7] Elliott, C., Reid, S., Hamer, P., Alderson, J., Elliott, B.: Lycra(®) arm splints improve
movement fluency in children with cerebral palsy. Gait Posture 33(2), 214–219
(2011)
[8] Matthews, M., Crawford, R.: The use of dynamic Lycra orthosis in the treatment of
scoliosis: a case study. Prosthet. Orthot. Int. 30(2), 174–181 (2006)
[9] Watson, M.J., Crosby, P., Matthews, M.: An evaluation of the effects of a dynamic
lycra orthosis on arm function in a late stage patient with acquired brain injury. Brain
Inj. BI 21(7), 753–761 (2007)
[10] Davis III, R.B., Õunpuu, S., Tyburski, D., Gage, J.R.: A gait analysis data collection
and reduction technique. Hum. Mov. Sci. 10(5), 575–587 (1991)
[11] Winter, D.A.: Biomechanics of human movement. Wiley (1979)
A Blood Pressure-Related Profile Extracted
from Pig Left Vagus Nerves Using Cuff
Electrodes

Cristian Sevcencu, Thomas Nørgaard Nielsen, and Johannes J. Struijk

Department of Health Science and Technology, Aalborg University, Denmark


{sevcr,thnn,jjs}@hst.aau.dk

Abstract. Vagus nerve (VN) stimulation (VNS) is used in epilepsy and tested for
blood pressure (BP) control. Whereas the present VNS methods are scheduled,
closed-loop VNS (CL-VNS) may be safer and more efficient. However, CL-VNS
for epilepsy and BP control require implantable means to monitor seizures and BP
changes and such means are not available yet. It is known that the VN conducts
afferent BP-related signals, and that seizures are often preceded by BP changes.
This study was performed to investigate if such BP-related signals can be recorded
using implantable means and if information regarding BP changes can be derived
from such recordings. The experiments were performed in two pigs subjected to
adrenaline administration for BP increase. The left VN electroneurogram (VENG)
was recorded using cuff electrodes, the BP using carotid catheters and the ECG
using surface electrodes. By ensemble averaging the VENG activity relative to the
R-peaks, afferent BP-related VENG profiles (BP-VENGs) were extracted from the
VENG. The BP-VENGs were morphologically similar, proportional and in phase
with the carotid BP pulses. The maximum amplitude of those profiles was used to
derive a phasic VENG component (pVENG) which changed proportional to the
mean BP changes. It is concluded that the BP-VENGs and pVENG could
eventually be implemented in CL-VNS for epilepsy and BP control to monitor BP
changes and modulate on-demand VNS.

1 Introduction

Vagus nerve (VN) stimulation (VNS) has been used as a therapy for intractable
epilepsy since the mid ‘90s [1] and is presently tested in heart failure (HF) patients
[2]. In addition, there is evidence that VNS could be an option for treating
resistant hypertension (RH), too [3].
VNS for epilepsy is applied according to scheduled stimulation paradigms, e.g.
30 s stimulation every 5 min, 24 hours/day, 7 days/week. Whereas this stimulation
mode results in 50% seizure reduction in 50% of the implanted patients [1], there
is evidence that VNS can totally block seizures if applied prior to, or at the onset
of seizures [4]. This indicates that closed-loop VNS (CL-VNS) may be a better
option than scheduled VNS in epilepsy. However, CL-VNS for epilepsy requires a

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 717
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_100, © Springer International Publishing Switzerland 2014
718 C. Sevcencu, T.N. Nielsen, and J.J. Struijk

marker for at least early detection of seizures and a suitable marker for this
purpose is not available yet.
Besides epilepsy, CL-VNS would be ideal for HF and RH, too. This VNS mode
would avoid over-stimulation, which may lead to even cardiac arrest [5], or under-
stimulation, which may be ineffective. However, implantable CL-VNS for HF and
RH requires markers to monitor blood pressure (BP) changes and, as in the case of
CL-VNS for epilepsy, suitable markers for this purpose are not available yet.
Ideally, CL-VNS should be controlled by markers extracted from the VN
electroneurogram (VENG) itself. In this case, VENG recording and VNS could be
performed using one and the same electrode, allowing CL-VNS without
increasing the invasiveness of the therapy. As it is known that the VN conducts
BP-related afferent signals originating in aortic baroreceptors [6], such BP-related
signals could be extracted from VENG and used as markers in CL-VNS for HF
and RH. In addition, it is known that epileptic seizures are associated with cardiac
and BP changes, which often precede the onset of seizures [7]. Hence, extraction
of BP-related signals from VENG could lead to the development of markers for
seizures, too [8].
The BP-related VN signals have been recorded using hook, needle or glass
electrodes only [8;9], which are improper for implantable systems. If similar
signals could be recorded using e.g. cuff electrodes, the development of CL-VNS
systems for the mentioned applications would be possible. The present
experiments were performed in pigs to investigate if BP-related signals can be
extracted from the VENG recorded using cuff electrodes and if such signals can
be used to estimate BP changes.

2 Methods

2.1 Experimental Procedures


The present analysis was performed on data collected from 2 farm pigs weighing
45 and 47 kg. The pigs were anesthetized with sevoflurane during surgery and by
IV infusion of ketamine (20 mg/kg/hour) and xylazine (2 mg/kg/hour) during the
recordings. The left VN and the right carotid artery were exposed at a cervical level
through lateral neck incisions. The left VENG was recorded at a proximal and a
distal location using two tripolar ring cuff electrodes (2.4 mm inner diameter, 5 mm
center-to-center electrode spacing) which were placed 5 cm apart. The
electrocardiogram (ECG) was recorded using two surface electrodes to represent
lead II and the arterial BP was recorded using a catheter inserted in the right carotid
artery and connected to a pressure transducer (Edwards LifesciencesTM). After 5
min of baseline recording, a single bolus of adrenaline (0.5 µg/kg) was
administered in an auricular vein to induce BP increase. Following this procedure,
vagotomy was performed between the cuffs while recording the above mentioned
parameters. At the end of the experiments, the animals were euthanized by IV
administration of an anesthesia overdose.
A Blood Pressure-Related Profile Extracted from Pig Left Vagus Nerves 719

ECG 200
Vagotomy

sBP [mmHg]
150

140 PreVT
BP [mmHg]

PostVT
120 100

100 Pulse pressure

80 0.4

VENG [µV2]
BP-VENG [µV]

PreVT
2

0.4
Phasic 0.2 Prox
0.3
Tonic
Tonic
0.2 Phasic
0

0.4 Dist
]

VENG [µV2]
BP-VENG [µV

Prox
2

0.4 PostVT
Dist
0.3
0.2
0.2

0
-100 0 100 200 300 400 4 5 6 7 8 9
R-peak-related tim e [m s] Experimental time [min]

Fig. 1 An example of BP-VENG profiles and the derived phasic and tonic components in
relation to BP pulses (left) and sBP development (right) before and after vagotomy in Pig 1.
PreVT – before vagotomy; PostVT – after vagotomy; Dist – distal recording; Prox –
proximal recording.

All experimental procedures were approved by the Danish Animal Welfare


Committee.

2.2 Data Acquisition and Analysis


All signals were amplified (ECG = 2.5k-10k, VENG = 100k-1M, and BP = 50k
V/V) and filtered (ECG = 1-10 kHz, VENG = 10 Hz to 10 kHz and BP = DC-10
kHz) using AI402 SmartProbes and a CyberAmp 380 (Axon Instruments, Inc.) and
digitized at 16 bits and 50 kHz using a PCI-6251 DAQ (National Instruments®).
The data were analyzed off-line in MATLAB® (The MathWorks, Inc.).
The signals were further filtered in MATLAB (ECG = 2-150 Hz, VENG = 800-
10 kHz and BP = DC-150 Hz), the ECG and BP were down sampled to 1000 Hz,
and the VENG was squared to obtain the power of the signals. Diastolic BP (dBP)
and systolic BP (sBP) were calculated as the minimum and maximum BP,
respectively, within each BP pulse. The difference between sBP and dBP in each
BP pulse represents the pulse pressure.
VENG profiles were extracted from the general VENG (gVENG) as described by
Harreby et al [10], i.e. by ensemble averaging the gVENG activity relative to the R-
peaks followed by averaging the profiles into 10 ms bins. The maximum amplitude
of those VENG profiles was used to derive a phasic VENG component (pVENG)
and the minimum level of VENG at the base of those profiles was used to derive a
tonic VENG component (tVENG) (Fig. 1). The mean arterial BP (mBP, calculated
as 2/3 dBP + 1/3 sBP), gVENG, pVENG and tVENG were further normalized
relative to baseline and represented as a function of the experimental time (Fig. 3).
720 C. Sevcencu, T.N. Nielsen, and J.J. Struijk

1.8 Baseline
Adr: 0-30 s
1.6 Adr: 30-60 s
Adr: 60-90 s
1.4 Adr: 90-120 s
pVENG [µV2]

1.2

0.8

0.6

0.4

0.2
20 40 60 80 100 120
Pulse pressure [m m Hg]

Fig. 2 Maximum BP-VENG values (i.e. pVENG values) versus the pulse pressure values
recorded during baseline (black stars) and in consecutive intervals (colored stars) during the
adrenaline (Adr) induced BP increase in Pig 2

3 Results

The VENG profiles extracted as described were morphologically similar and in


phase with the BP pulses recorded from the carotid artery (Fig. 1, left). Therefore,
these VENG profiles are regarded as BP-related VENG profiles (BP-VENG). The
BP-VENGs preceded the corresponding BP pulses by 19 and 23 ms in Pig 1 and
Pig 2, respectively, because of differences in placement of the transducers and the
propagation velocities involved.
After vagotomy between the proximal and distal cuffs, the BP-VENGs
disappeared from the proximal VENG and increased slightly in the distal VENG
(Fig. 1, left). Mirroring this effect, the pVENG component derived from those
profiles dropped in the proximal VENG and increased in the distal VENG after
vagotomy (Fig. 1, right). As illustrated in the right upper trace of Figure 1, this
latter effect was associated with the sBP increase induced by vagotomy. As
compared to pVENG, tVENG decreased in both stumps after vagotomy and this
effect was more prominent in the proximal tVENG. The above mentioned changes
were similar in both pigs.
A Blood Pressure-Related Profile Extracted from Pig Left Vagus Nerves 721

3
Pig 1
mBP [AU]

2
Pig 2
1

0
gVENG [AU]

0
pVENG [AU]

0
4
tVENG [AU]

0
-4 -3 -2 -1 0 1 2 3 4 5
Tim e [m in]

Fig. 3 Development of the general VENG (gVENG) and of the phasic and tonic VENG
components (pVENG and tVENG, respectively) during the adrenaline induced BP increase.
The upper trace represents the mean arterial BP (mBP) calculated as described. Time “0”
represents the time of adrenaline administration.

Administration of adrenaline resulted in 45% and 100% increase of mBP in Pig


1 and Pig 2, respectively (Fig. 3), which was associated with a pulse pressure
increase. Plotting the maximum BP-VENG amplitudes as a function of the
corresponding pulse pressure values, measured prior and during that BP increase,
showed that the BP-VENG amplitude increased proportional with the pulse
pressure values. Such correlation between the pulse pressure values and the BP-
VENG amplitude was observed in both pigs and is illustrated in Figure 2 using the
plot from Pig 2.
The normalized mBP, gVENG, pVENG and tVENG as functions of time show
that pVENG increased 2.4 and 4 times in Pig 1 and Pig 2, respectively, consecutive
to the above mentioned mBP increase (Fig. 3). Similar but much smaller changes
were observed in gVENG and tVENG, too (Fig. 3).

4 Discussion
Our results showed that the BP pulses recorded using arterial catheters were
associated with phasic VENG profiles (i.e. BP-VENGs) which had an amplitude
proportional with the pulse pressure values. Thus, the present study demonstrates
that BP-related signals can be extracted from the left VENG recorded using cuff
electrodes and that information regarding pulse pressure values can be derived from
such signals.
722 C. Sevcencu, T.N. Nielsen, and J.J. Struijk

Studies with single fibers have shown that the left VN conducts afferent signals
from the aortic baroreceptors [6]. As illustrated by those studies, such fibers fire in
phase with BP pulses and proportional to the pulse pressure levels [6], which is in
line with our observations. Thus, the BP-VENGs extracted from VENG were
morphologically similar and in phase with the recorded BP pulses (Fig. 1), which
indicates that they consisted of signals related to pulse pressure levels. The fact that
the BP-VENGs disappeared from the proximal VN stump and persisted in the distal
VN stump after vagotomy (Fig. 1) suggests that those signals were afferent.
Consistent with this afferent and BP-related origin of the BP-VENGs, pVENG
derived from those BP-VENG profiles dropped in the proximal stump and
increased in the distal stump consecutive to the vagotomy-induced BP increase
(Fig. 1).
In addition to the above mentioned study on the activity of single baroreceptor
afferent fibers [6], studies with bundles of such fibers have demonstrated that those
fibers were recruited proportional to pulse pressure values [11]. In our study, the
amplitude of the BP-VENG was correlated with the pulse pressure values (Fig. 2),
which agrees with such a linear recruitment phenomenon. As such baroreceptor
recruitment depends on the pulse pressure and hence on dBP and sBP, changes in
the BP-VENG amplitude may indicate changes of either of those BP values. As
mBP is a combination of dBP and sBP, the correlation between the increase of
mBP and pVENG (Fig. 3) suggests that pVENG may serve as estimator of BP
changes.
Compared to pVENG, tVENG comprises large afferent and smaller efferent
content (Fig. 1) which seems less sensitive to BP changes (Fig. 3). This is
consistent with our previous studies which showed that 75% of the left VN activity
is afferent and primarily related to respiratory functions [8].
In a recent study, Plachta et al. have used cuff electrodes to record BP-related
signals from the left VN of rats [12]. Similar to the BP-VENGs described in the
present study, those BP-related signals reported by Plachta et al. were in phase with
BP pulses recorded using arterial catheters [12]. However, in contrast with our
results, the BP-related signals reported by Plachta et al. seemed morphologically
different in regard to the BP pulses and the mentioned authors did not report
whether or not information on BP values could be derived from those signals.
As the number of animals used in our study was limited, the present results
require validation in a larger study. In addition, whether or not this BP-related
information could eventually be used to detect the onset of seizures or drive CL-
VNS for BP control remains to be verified in experiments with pig models of
seizures and BP monitoring in various conditions.

5 Conclusion

The present work suggests that BP-related information can be extracted from the
left VENG recorded using cuff electrodes and that this information can be used to
estimate BP changes.
A Blood Pressure-Related Profile Extracted from Pig Left Vagus Nerves 723

Acknowledgment. This work was performed at the Biomedical Laboratory of Aalborg


Hospital, and supported by the Danish Agency of Science, Technology and Innovation. The
authors wish to thank Ole Sørensen, Torben Madsen and Jens Sørensen from The
Biomedical Laboratory of Aalborg Hospital for their help in performing the experiments.

References
[1] Ramani, R.: Vagus nerve stimulation therapy for seizures. J. Neurosurg.
Anesthesiol. 20(1), 29–35 (2008)
[2] De Ferrari, G.M., Crijns, H.J., Borggrefe, M., Milasinovic, G., Smid, J., Zabel, M.,
Gavazzi, A., Sanzo, A., Dennert, R., Kuschyk, J., Raspopovic, S., Klein, H.,
Swedberg, K., Schwartz, P.J.: Chronic vagus nerve stimulation: a new and promising
therapeutic approach for chronic heart failure. Eur. Heart J. 32(7), 847–855 (2011)
[3] Tosato, M., Yoshida, K., Toft, E., Nekrasas, V., Struijk, J.J.: Closed-loop control of
the heart rate by electrical stimulation of the vagus nerve. Med. Biol. Eng.
Comput. 44(3), 161–169 (2006)
[4] Morris III, G.L.: A retrospective analysis of the effects of magnet-activated
stimulation in conjunction with vagus nerve stimulation therapy. Epilepsy. Behav.
4(6), 740–745 (2003)
[5] Tatum, W.O., Moore, D.B., Stecker, M.M., Baltuch, G.H., French, J.A., Ferreira, J.A.,
Carney, P.M., Labar, D.R., Vale, F.L.: Ventricular asystole during vagus nerve
stimulation for epilepsy in humans. Neurology 52(6), 1267–1269 (1999)
[6] Andresen, M.C., Hofmann, M.E., Fawley, J.A.: The unsilent majority-TRPV1 drives
“spontaneous” transmission of unmyelinated primary afferents within
cardiorespiratory NTS. Am. J. Physiol. Regul. Integr. Comp. Physiol. 303(12),
R1207–R1216 (2012)
[7] Sevcencu, C., Struijk, J.J.: Autonomic alterations and cardiac changes in epilepsy.
Epilepsia 51(5), 725–737 (2010)
[8] Harreby, K.R., Sevcencu, C., Struijk, J.J.: Ictal and peri-ictal changes in cervical
vagus nerve activity associated with cardiac effects. Med. Biol. Eng. Comput. 49(9),
1025–1033 (2011)
[9] McAllen, R.M., Spyer, K.M.: The baroreceptor input to cardiac vagal motoneurones.
J. Physiol. 282, 365–374 (1978)
[10] Harreby, K.R., Sevcencu, C., Struijk, J.J.: Early seizure detection in rats based on
vagus nerve activity. Med. Biol. Eng. Comput. 49(2), 143–151 (2011)
[11] Angell James, J.E.: The effects of altering mean pressure, pulse pressure and pulse
frequency on the impulse activity in baroreceptor fibres from the aortic arch and right
subclavian artery in the rabbit. J. Physiol. 214(1), 65–88 (1971)
[12] Plachta, D.T.T., Espinosa, N., Gierthmuehlen, M., Cota, O., Herrera, T.C., Stieglitz,
T.: Detection of baroreceptor activity in rat vagal nerve recording using a multi-
channel cuff-electrode and real-time coherent averaging. Conf. Proc. IEEE Eng. Med.
Biol. Soc. 2012, 3416–3419 (2012), doi:10.1109/EMBC.2012.6346699
Patient Satisfaction of Using the ActiGait®
Drop Foot Stimulator System and Effect
of Treatment on Walking

Kaare Severinsen1,2,* Kurt Grey3, Anne Juhl4, Preben Soerensen5,


L. Oppel1, and P.T. Birgit Larsen6,**
1
Department of Neurology, Aalborg University Hospital
kaarseve@rm.dk
2
The Research Unit at Hammel Neurocenter,
Aarhus University Hospital
3
Department of Occupational Therapy and Physiotherapy,
Aalborg University Hospital
4
Department of Neurophysiology, Aalborg University Hospital
5
Department of Neurosurgery, Aalborg University Hospital
6
Department of Health, University College Nordjylland, Aalborg, Denmark

Abstract. In this case-control study of ten chronic stroke patients with drop foot
we report preliminary data on patient satisfaction, self- assessed changes in
walking performance, effect on walking speed as well as adverse effects after
surgical implantation of the ActiGait® drop foot stimulator in a clinical setting at
Aalborg University Hospital.
Using The Canadian Occupational Performance Measurement and a ten meter
walk test as well as standard neurophysiological measurements we demonstrate an
increase in self- assessed walking performance and patient satisfaction and an
apparent increase of walking speed after implantation of the ActiGait® drop foot
stimulator. The orthotic effect of ActiGait® stimulation on gait results in increased
walking speed. This is achieved without negative effects on nerve conduction
velocity as measured three months after surgical implantation. Measurements were
performed three, six and twelve months after implantation demonstrating an
increasing degree of patient satisfaction over time. Implementation of ActiGait®
in a daily clinical setting seems safe with high patient satisfaction whereas,
interpretation of the effect on walking speed must be performed with great care
due to the small population size, the case control design and the limitations of the
ten meter walk test in describing walking quality and safety.

1 Introduction
Drop foot as a result of paresis of the ankle dorsiflexor muscles, calf spasticity or
ankle stiffness is a common problem following stroke (1). Standard care of

*
Corresponding author.
**
B. Larsen was with Neurodan A/S, Aalborg, Denmark (during part of the study).

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 725
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_101, © Springer International Publishing Switzerland 2014
726 K. Severinsen et al.

treatment is the prescription of ankle foot orthosis (AFO), which provides stable
support of the ankle joint during the swing phase and initial contact during
walking. The disadvantages using AFO is that it limits normal ankle mobility
resulting in increased ankle stiffness and reduced adjustment of the foot to the
walking surface which may result in general inconvenience and therefore patients
may dislike and find the AFO unesthetic (2). An alternative to AFO is functional
electrical stimulation (FES) applied by surface electrodes above the common
peroneal nerve. Peroneal nerve stimulation activates the muscles of the lower leg
that dorsiflex and evert the foot which correctly timed ensures foot clearance
during swing and controlled heel strike during initial contact. FES of the common
peroneal nerve has been shown to provide an effective alternative to AFO (3, 4);
however, difficulties such as positioning the electrodes as well as skin irritation in
some patients (5,6) led to the development of partly implantable drop foot
stimulator systems (7,8). ActiGait®. that was CE-marked for the European market
in 2006 has shown to be a safe and effective walking tool in patients after stroke
(8) with high patient satisfaction (9). Since 2006 the ActiGait® has been
introduced in several European countries. This study presents the first results of
the implementation of ActiGait® as a commercially available treatment in drop
foot in Denmark. A clinical study was set up during the implementation of
ActiGait® at the first Danish Center of Excellence at Aalborg University Hospital.
The aims of the study were to verify patient satisfaction as well as effect and
safety during the first 10 implantations. Patient satisfaction was evaluated using
the The Canadian Occupational Performance Measurement (COPM) and effect of
stimulation was evaluated using preferred walking speed on a ten meter track and
distance in six minutes. Safety was evaluated by numbers and type of adverse
effects as well as an evaluation of changes in nerve conduction parameters of the
common peroneal nerve involved in the implantation procedure. This paper
presents the provisional results of the study.

2 Methods

2.1 ActiGait® Drop Foot Stimulator System


ActiGait® comprises a surgically positioned peroneal nerve stimulator, an
external heel switch and control unit and a software package. The implant consists
of the stimulator body, a cable and a nerve cuff electrode to be positioned around
the common peroneal nerve. The cuff electrode allows independent stimulation of
different fascicles within the nerve by four sets of electrodes. The heel switch that
is positioned in the shoe triggers the initiation and termination of stimulation
sequences with respect to the stride phase by a radio-link to the external control
unit, usually carried at the waist. A couple of weeks after implantation a trained
physiotherapist adjusts the stimulation sequence with respect to correct timing and
Patient Satisfaction of Using the ActiGait® Drop Foot Stimulator System 727

Fig. 1 The ActiGait® partly implantable drop foot stimulator system

movement of the ankle joint during gait by use of the software package connected
to the control unit. An antenna that is hard-wired to the control unit is positioned
on the skin above the stimulator body by which power and settings from the
control unit can be transferred to the implant. During use the control unit allows
the patient to switch on and off stimulation and increase/decrease stimulation
intensity within the clinical set range of intensities.

2.2 Participants
The study was designed as a manufacturer supported case control study including
the first ten patients receiving an ActiGait® implant during one year follow-up.
Selection of candidates followed the intended use, indications and contraindications
of ActiGait® (8), i.e. patients with hemiplegia including drop foot caused by
stroke, with a minimum time since stroke of six months. Patients were able to stand
with both heels touching the ground and a range of motion of the affected ankle
joint of at least 30 degrees. Patients had a reduced gait speed and surface peroneal
stimulation resulted in correction of the drop foot as measured by increased range
of motion, and an improvement of gait quality clinically evaluated by an
experienced physiotherapist (PT). Patients had no need of an AFO to ensure medio-
lateral stability of the ankle joint during loading phase and no other concomitant
medical or psychological diseases or stroke sequelae that might compromise
efficiency and safety in connection to the implantation or use of ActiGait®.
728 K. Severinsen et al.

2.3 Protocol and Outcome Measures


The ActiGait® implantation was carried out in general anaesthesia. After surgical
exposure of the common peroneal nerve the implant was positioned laterally on the
thigh and the cuff electrode sutured around the peroneal nerve just above the knee.
Two weeks after implantation patients were called in for activation of the
stimulator and again one week later for adjustment of the stimulation.
Subsequently, patients were offered five to eight hours of individually adjusted gait
training.
To investigate the long term effects of stimulation on walking speed and
endurance ten meter and six minutes gait tests at self-selected pace were applied
prior to implantation without stimulation and 6, 12, 26 and 52 weeks after
implantation with stimulation. During all assessments the ten meter gait test was
repeated three times, and the mean speed was used for further calculations. All
measurements of preferred walking speed after implantation were performed both
with and without ActiGait® stimulation to evaluate the orthotic effect, yet again,
three repetitions without and three repetitions with ActiGait® stimulation, the mean
being used for further calculations. The orthotic effect of stimulation was
investigated by comparing preferred gait speed on a ten meter walk test with and
without stimulation on the same day The patient was allowed to use his/her
preferred walking aid during testing, if needed, except for AFO. The six minute
gait test after implantation was only performed with stimulation once at each
follow-up., hence no estimation of orthothic effect was performed in regard to the
walking endurance.
The Canadian Occupational Performance Measurement (COPM) was applied in
order to verify if use of ActiGait® met patients’ expectations to their own set up
goals on the treatment. COPM is a validated tool that has previously been used to
document satisfaction of peroneal surface stimulation in patients with Multiple
Sclerosis (MS) (10). It is usually applied to identify problems in connection to
daily activities (ADL), plan exercise programs with individualized training of
activities of daily living, show patient’s prioritization of daily living problems and
assess performance and patient’s satisfaction with treatment or training in relation
to patient prioritized problem areas (11). The COPM was applied during the second
baseline measurement and at six and twelve weeks follow-up. The patient
identified their individual performance problems, within the categories A. self-care,
B. productivity and C. leisure that they encountered during the day. The patient
used the COPM scoring cards to prioritize the most important activities on a scale
from 1-10. The top five highest scored self-perceived problems were identified and
subsequently individually scored for performance and satisfaction on a scale from
1-10. The five highest scored items were re-assessed during six and 12 weeks
follow-up. A change in score of two or more is considered clinically significant
(10).
Nerve conduction velocity (NCV) of the peroneal nerve was measured before
and 12 weeks after implantation to assess if possible pull or pressure from the
implant might have compromised the nerve.
Patient Satisfaction of Using the ActiGait® Drop Foot Stimulator System 729

Study protocol was submitted to the local ethical committee who found that the
study was to be considered a quality follow-up study and application and ethical
approval therefore not required. Patients gave their written informed consent to
enter the study.

2.4 Statistical Analysis


The COPM were analyzed using Wilcoxons test with analysis of self-assessed
performance and self-assessed satisfaction.
Walking speed at baseline without stimulation was compared to post-operative
walking speed with stimulation i.e. long term effect, at every follow up. The paired
t-test was used for this analysis.
The orthotic effect of ActiGait® stimulation, i.e. difference in walking speed
with ActiGait® stimulation switched on and off during follow-up, was analysed
using a paired t-test, since the difference in walking speed with and without
stimulation was considered to be normally distributed.
In both Wilcoxons tests and the paired t-test a significance level of 0.05 was
adopted.

3 Results

Nine of the first ten patients receiving an ActiGait® implant at Aalborg Hospital
have finalized one year follow-up. Patient number ten has only completed three
months follow-up until now.
One patient who was infected after opening of the sutures above the knee, was
explanted 12 weeks after implantation and reimplanted 18 months later. Eight of
the nine patients that have finalized the one year follow-up patients used the
ActiGait® seven days a week.

Table 1 Shows the baseline demographic and performance data (median and (range))

n = 10 Results

Age (year) 55 (44; 68)


Gender 5/5
(male/female)
Affected side R/L 6/4
Walking speed 0.79 (0.25; 1.04)
(m/sec)
Walking speed 54.3 (15; 84)
(% of age and
gender norm)
Walking distance 259 (73; 306)
6 min walk (m)
730 K. Severinsen et al.

3.1 COPM
All patients scored three to five self-selected activities before implantation and
scored the same activites again 12 and 24 weeks after implantation. The median
score of self- assessed performance improved 12 weeks after implantation (p=
0.028), fig 2, and 24 weeks after implantation (p=0.015). Twelve weeks after
implantation patient scores of the performance of self-selected problems on daily
activities had improved or were unchanged in all patients except one.
In five out of nine patients an increase of the score above two indicated a clinical
relevant improvement. One patient, however, had a decrease in self- assessed
performance score three and six months after implantation.
Also median patient satisfaction score increased 12 and 24 weeks after
implantation (p=0.005 and p=0.011). Twelve weeks after implantation all patients
increased the scoring and seven out of nine patients increased the score with a
value of two or more (fig 2).

3.2 Gait Speed at 10 Meter Walk Test


The median baseline gait speed (before implantation) was 54 % of what would be
expected corrected for age and gender (12), reflecting a substantial reduction of
gait speed in the population compared with healthy individuals.
Gait speed at ten meter walk test without ActiGait® stimulation was unchanged
three, six and twelve months after implantation compared with baseline
measurements.
Mean long term effect of stimulation on walking speed three, six or twelve
months after implantation did not change significantly.
The orthotic effect of stimulation three, six and twelve months after
implantation, was investigated by comparing preferred gait speed on a ten meter
walk test with and without stimulation on the same day. Twelve weeks after
implantation there was an increase in gait speed in eight of nine patients and at six
and twelve months all patients had an increase in gait speed during stimulation
compared to no stimulation. The mean increase in walking speed, hence the
orthotic effect, was statistical significant at three (p=0.03), six (p=0.003) and
twelve months (p=0.03) after implantation although the actual change varied
considerably between patients.
In one patient the orthotic effect of stimulation was not tested due to instability
of the ankle joint without stimulation, and for another patient six and twelve
months follow-up has not yet been performed.

3.3 Six Minute Gait Test


All patients walked continuously during the six minute gait test before and after
implantation. There was a tendency toward an increase in walking distance over
time, however, mean values did not reach statistical significance twelve months
after implantation (p=0.21).
Patient Satisfaction of Using the ActiGait® Drop Foot Stimulator System 731

COPM (Performance)
9

6
COPM value

1
Baseline 3 months

COPM (Satisfaction)
9

6
COPM value

Fig. 2 COPM performance and satisfaction at baseline and 12 weeks. 24 week data are
incomplete and not reported.
732 K. Severinsen et al.

3.4 Neurophysiological Assessment


There were no changes in nerve conduction velocity of the common peroneal
nerve three months after ActiGait® implantation. The patient being explanted and
subsequently re-implanted, did not have any change in nerve conduction velocity
at subsequent measurement of conduction velocity.

3.5 Adverse Effects


In one patient the implant had to be removed due to infection. The patient was
treated with antibiotics and, subsequently re-implanted, with no side effects, and
no changes in nerve conduction velocity of the common peroneal nerve. No other
adverse effects were reported.

4 Discussion

In this case control study of ten chronic stroke patients with drop foot we present
preliminary data on safety of implementation of ActiGait® in a clinical setting and
data of self-assessed performance and satisfaction after ActiGait® implantation
three to twelve months after implantation. Furthermore, we present data on changes
in walking speed and the orthotic effect of ActiGait® stimulation.
The main results are following: 1) there are no negative effects of electrode
implantation on nerve conduction velocity of the common peroneal nerve; 2) there
is a significant increase of self-assessed performance and satisfaction after
ActiGait® implantation assessed by the COPM; 3) there are some indications of a
positive effect of ActiGait® stimulation on walking speed as measured by the
orthotic effect of stimulation during a ten meter gait test.
The present study reports preliminary data from a small case-control study on
clinical implementation of the ActiGait® implantable drop foot stimulator in
Denmark. Apparently implementation is safe and adverse effects are solely related
to surgical procedures, since no affection of the involved peripheral nervous system
components are observed.
In general patients self-assessed performance increased after implantation and
self-assessed performance and satisfaction continued to increase throughout the
follow-up period of six months. None the less, one patient decreased in the self-
reported COPM performance score, despite an actual increase in both walking
speed and COPM satisfaction. One patient stopped using the device during working
hours because he felt it changed his appearance, despite an increase in COPM
performance score. This indicates that acceptance of implanted devices can be
difficult in some patients. Furthermore, it emphasizes that a comprehensive
selection procedure is necessary prior to actual implantation.
The actual effect on preferred walking speed with ActiGait® stimulation must
be interpreted with great care because of the small number of patients; however,
Patient Satisfaction of Using the ActiGait® Drop Foot Stimulator System 733

there seems to be a tendency toward improvement. Whether the actual change of


walking speed with stimulation compared with no stimulation is of clinical
significance is less clear since the ten meter walk test is a short test, and may not
account for e.g. improved ability to change direction, improved obstacles avoidance
or other indicators of improved confidence during daily living activities as
indicated by patients’ own evaluation. A more detailed gait analysis using video or
three dimensional gait analyses would probably contribute with further information
as to the quality (7,13) and security of walking in a daily day environment.

5 Conclusion

One year follow-up of the first nine patients receiving an ActiGait® partly
implantable drop-foot stimulator at the first Danish ActiGait® Center of
Excellence has shown that the implementation of ActiGait® as a new treatment in
patients with drop foot following stroke is safe and patients’ satisfaction high. The
present results indicates that application of the commonly used outcome measure
–the six minute walk tests is insufficient to document patients satisfaction,
whereas, the ten meter walk test to some extent reflects self-assessed
improvements despite its obvious limitations in regard to walking quality and
stability during daily living activities.

Acknowledgment. This study was supported by Neurodan A/S, Denmark member of the
OttoBock GmbH group.

References
[1] Burridge, J.H., McLellan, D.L.: Relation between abnormal patterns of muscle
activation and response to common peroneal nerve stimulation in hemiplegia. J.
Neurol. Neurosurg. Psychiatry 69, 353–361
[2] Doğan, A., Mengüllüoğlu, M., Özgirgin, N.: Evaluation of the effect ankle-foot
orthosis use on balance and mobility in hemiplegic stroke patients
[3] Everaert, D.G., Stein, R.B., Abrams, G.M., Dromerick, A.W., Francisco, G.E.,
Hafner, B.J., Huskey, T.N., Munin, M.C., Nolan, K.J., Kufta, C.V.: Effect of a Foot-
Drop Stimulator and Ankle_Fooot Orthosis on Walking Performance After Stroke: A
Multicenter Randomized Controlled trial. Neurorehabil. Neural Repair 27(7), 579–
591 (2013)
[4] Kluding, P.M., Dunning, K., O’Dell, M.W., Wu, S.S., Ginosian, J., Feld, J., McBride,
K.: Foot Drop Stimulation versus Ankle Foot Orthosis After Stroke. Stroke 44(6),
1660–1669
[5] Taylor, P.N., Burridge, J.H., Dunkerley, A.L., Lamb, A., Wood, D.E., Norton, J.A.,
Swain, I.D.: Patients’ perception of the Odstock Dropped Foot Stimulator (ODFS).
Clinical Rehabilitation 13, 439–446 (1999)
734 K. Severinsen et al.

[6] van Swigchem, R., Weerdesteyn, V., van Duijnhoven, H.J., den Boer, J., Beems, T.,
Geurts, A.C.: near-Normal Gait Pattern With Peroneal Electrical Stimulation as a
Neuroprosthesis in the Chronis Phase of stroke: A Case report. Arch. Phys. Med.
Rehabil. 92 (2011)
[7] Kottink, A.I., Hermens, H.J., Nene, A.V., Tenniglo, M.J., van der Aa, H.E.,
Buschman, H.P., IJzerman, M.J.: A Randomized Controlled Trial of an Implantable 2-
channel Peroneal Nerve Stimulator on Walking Speed and Activity in Poststroke
Hemiplegia. Arch. Phys. Med. Rehabil. 88(8), 971 (2007)
[8] Burridge, J.H., Haugland, M., Larsen, B., Pickering, R.M., Svaneborg, N., Iversen,
H.K., Christensen, P.B., Haase, J., Brennum, J., Sinkjær, T.: Phase II trial to evaluate
the ActiGait implanted Drop-foot stimulator in established hemiplegia. J. Rehabil.
Med. 39(3), 212–218 (2007)
[9] Burridge, J.H., Haugland, M., Larsen, B., Svaneborg, N., Iversen, H.K., Christensen,
P.B., Pickering, R.M., Sinkjær, T.: Patients’ Perception of the benefits and problems
of using the ActiGait implanted drop-foot stimulator. J. Rehabil. Med. 40(10), 873–
875 (2008)
[10] Esnouf, J.E., Taylor, P.N., Mann, G.E., Barret, C.L.: Impact on activities of daily
living using a functional electrical stimulation device to improve dropped foot in
people with multiple sclerosis, measured by the Canadian Occupational Performance
Measure. Multiple Sclerosis 16(9), 1141–1147 (2010)
[11] Dedding, C., Cardol, M., Eyssen, I., Dekker, J., Beelen, A.: Validity of the Canadian
Occupational Performance Measure: a client –centered outcome measurement. Clin.
Rehabil. 18, 660–667 (2004)
[12] Bohannon, R.W.: Comfortable and maximum walking speed of adult aged 20-79
years: reference values and determinants. Age and Ageing 26(1), 15–19 (1997)
[13] Ernst, J., Grundey, J., Hewitt, M., Lewinski, F.V., Kaus, J., Schmalz, T., Rohde, V.,
Liebetanz, D.: Towards physiological ankle movements with the ActiGait implantable
drop foot stimulator in chronic stroke. Restor. Neurol. Neurosci. 31(5), 557–569
(2013)
Augmentative and Assistive Communication in
Patients of Locked-In Syndrome: A Case Report

F.A. Purva Sharma and S.B. Yash Jobanputra

RCSM Government Medical College,


Kolhapur, MH 416001 India
purva7sharma@gmail.com,
yash_joban@hotmail.com

Abstract. Locked-in syndrome (LIS) is a catastrophic condition caused most often


by ischemic stroke or hemorrhage, affecting the corticospinal, corticopontine, and
corticobulbar tracts in the brainstem. We present a case of a Locked-in
Syndrome patient who received communication training with augmentative and
alternative communication equipment. The patient was initially given a trial of the
basic Dynavox Assistive technology device after which she graduated to using
the Tobii C 12 device. The patient’s limited use of her right upper extremity in the
form of being able to operate a light writer switch with her thumb aided her use of
these devices. The patient was later introduced to the Mega-bee which eliminated
the use of a switch as it required only the use of eye-blinks to communicate. At the
end of her 2 month stay at the rehab facility she was able to efficiently use the
Mega-Bee device and improved tremendously in her communication.
Augmentative and alternative communication equipment helps patients of locked-
in syndrome to interact with their environment and plays a big role in their
recovery.

1 Introduction

Locked-in Syndrome (LIS) introduced by Plum and Posner in 1966, represents a


severe pontine infarction syndrome in which quadriplegia, lower cranial nerve
paralysis and mutism are caused by vertebral and basilar artery thromboses. The
LIS is a condition in which functions of consciousness and cognition are
maintained but there are defects of all movements other than eye blinks and
vertical eye movements. [1]
The diagnosis of Locked-in Syndrome is mainly done on the basis of presence
of retained alertness and cognitive abilities and at the same time paralysis of the
limbs and oral structures such that the individual cannot signal with the limbs or
speak.
The recent development of assistive technology has invited patients who cannot
conduct verbal communication to widen the options of augmentative and
alternative communication (AAC), whereby each of these patients can attempt to
satisfy his/her demands. [2]

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 735
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_102, © Springer International Publishing Switzerland 2014
736 F.A.P. Sharma and S.B.Y. Jobanputra

2 Case Report

A 66 year old woman with a history of obesity, hyperlipidemia and hypertension


with a remote left-sided cerebro-vascular accident in the past with no residual
functional deficits and who had previously been operated for bilateral total knee
replacement; first presented to Charlton Memorial Hospital, Boston, MA
complaining of dizziness and peri-orbital paraesthesias. A CT scan was done at
this point which showed a pontine infarct. However, the progressive worsening of
her symptoms indicated the need for further investigations and a MRI was ordered
which showed distal basilar occlusion. The patient was then transferred to
Massachusetts General Hospital where the diagnosis of locked-in syndrome was
made following which she received acute phase treatments (e.g. tracheostomy,
respirator and anticoagulation therapy).
The patient was subsequently transferred to a rehabilitation hospital. Her
hospital course at rehabilitation was complicated by a DVT in her left arm and an
E. coli urinary tract infection which were treated appropriately. Her neurological
examination showed that she was in a conscious state; however her cognitive and
perceptual abilities could not be determined due to difficulty in communicating
with her. The cranial nerve examination showed that her extra-ocular movements
were impaired and she was unable to direct conjugate gaze past her midline to her
right. She was able to smile with some assymetry and mild facial weakness was
observed on the left. She was also able to partly stick out her tongue, turn her head
to the right approximately 200 and the same degree to the left. The muscular
strength of the upper limbs was as follows: Right Upper Extremity (RUE) -2/5
elbow flexion and extension; 1/5 finger extension, 2/5 finger flexion. Left upper
extremity-no voluntary movement with Ashworth tone 3 at elbow flexors and
finger flexors. Similarly, that of the lower limbs was: Right lower extremity-
barely able to raise right leg off the bed, 1/5 dorsi and plantar flexion at right
ankle. Left lower extremity - no movement was seen.
The patient was also assessed in terms of rehabilitation care and the findings
noted were as follows: The physiotherapy evaluation showed that the patient
needed maximum assistance for bed mobility and transferring. However, she had
independent wheelchair management via buddy button or mini joy stick.
Occupational therapists noted that she needed moderate-maximum assistance
while using her right hand for bathing, dressing etc. Speech Language Pathology
and Cognition Evaluation found the patient’s auditory comprehension to be intact
for basic command and multi-unit Y/N questions. She demonstrated sustained and
selective attention to participate in basic auditory and visual tasks, was able to
shake her head in ‘yes’ or ‘no’, was able to cough and make sounds while crying
and was able to smile.
After this, a referral was made to Assistive Technology experts who on
evaluating the patient, concluded that use of low-tech Assistive and Augmentative
Communication (AAC) would help to convey simple messages, preferences and
needs of the patient and that she would identify 2-3 modes of AAC to
communicate with moderate cues.
Augmentative and Assistive Communication in Patients of Locked-In Syndrome 737

Table 1 Comparing patient's responses at onset and at time of discharge

Responses At onset At discharge (12


weeks)
Communicating One word at a 5-6 word sentences
messages time
Switch Slow; would Improved
operation miss out the dramatically,
rows while quicker
scanning
Eye blink and Slow at the Improved with
eye movement beginning slight increase in
head movement
towards right
Verbal Could make No improvement
communication sounds
Motor response Could only Started lifting her
(RUE): move her right arm off the
thumb bed.

The first device tried with the patient was the Dynavox after 3 weeks of her
stay at Spaulding Rehabilitation. She was initially given a game of tic-tac-toe,
starting with a 3x3 array of boxes and later moving on to the 5x5 one. The patient
was given a lightwriter switch in the thumb of her right hand and as the linear scan
of boxes started she would select the desired box by pressing the switch with the
movement of her thumb.
After giving her a trial of the device, she was then switched to a keyboard
layout in the following sessions. The patient successfully typed the word ‘mom’,
her son’s name and her husband’s name using the keyboard.
The next device used was the Tobii C-12. It uses a similar visual scanning
technique as the Dynavox AAC device. First a visual scanning of the rows starts,
and after an appropriate row is selected the scan then proceeds to the selected row;
the required letter is then selected in the given row. It comes with an in-built eye
gaze technology in which the infra-red rays from the eyes are reflected back using
in-built technology to scan the screen. The patient used this device better than the
Dynavox and improved considerably in typing words.
Various features of these devices such as different keyboard layouts(simple
abc, qwerty keypad), word-prediction, in-built phrases and greetings commonly
used in conversations and options like pre-storing messages for future use, made
communication much more efficient and quicker for the patient.
The patient was then given a trial of another AAC device called MegaBee™.
MegaBee™ is a simple-to-use assisted writing tablet to aid frequent
738 F.A.P. Sharma and S.B.Y. Jobanputra

communication. There is an LCD display on each side of the tablet, visible to


reader and writer. The tablet has been designed to require minimal learning both
for the reader and writer - letter selection is achieved by looking at the letter and
blinking, then looking at the block which is the same color as the selected letter.
For example the letter ‘K’ would be selected by looking first at the blue block
where the letter K is located and blinking (the reader then presses the blue button),
then, as the letter ‘K’ is black, the user looks at the black block and blinks. (The
reader presses the black button and the letter ‘K’ appears on the screen.)
The MegaBee™ is easy-to-use. It does not require calibration and
accommodates changes in head position or movement of the tablet. It requires
very little training and is learnt in minutes. It can also operate in a picture mode,
where pictures, photographs, symbols or drawings can be used as the
communication medium.
The regular training enabled the patient to express simple words like ‘home’,
her name etc. Further, it also enabled her to deliver some of her ideas and feelings
(e.g. "I love you," "When am I leaving the hospital?" etc.).

3 Discussion

According to the existing studies, the mortality of LIS patients is approximately


67% [3] and the survival rate of the patients who survived 5, 10 and 20 years is
83%, 83% and 40%, respectively.[4] The 19-month follow-up investigation of LIS
patients' functional recovery showed that only 21% of patients were able to
perform some activities of daily life and the other patients (79%) needed other
peoples' absolute help for living. [5]
LIS patients who survive with clear consciousness for a long time and whose
functional activity recovery is difficult need a communication method for living at
home and in society. Therefore, various types of devices and methods have
already been introduced and used. In 2001, the application of AAC was attempted,
which used the activities of thumbs, the chin, the head, and shoulders of 17 LIS
patients in Finland; of these, 9 patients were finally able to use a computer for
Internet access or for sending and receiving daily e-mails. [6] In addition, in
research carried out in the United States in 2003, 2 LIS patients diagnosed 11
years prior to 2003 returned to their position (i.e. lawyer and mathematics teacher)
by communicating with eye blinks and a mouse stick. [5]
LIS is classified into three categories according to whether or not physical
activities and communication can be performed. Classic LIS refers to the loss of
physical activities other than vertical eye movements, as defined by Plum and
Posner. Incomplete LIS represents a condition in which voluntary activity
functions except for vertical eye movements remain and total LIS refers to a
condition in which the functions of all physical activities are lost and
communication between the relevant patient and others is impossible. [7]
Augmentative and Assistive Communication in Patients of Locked-In Syndrome 739

Table 2 Patients performance with the various devices

Type of Progress made by the patient


Device used
Dynavox Switched from game mode to keyboard
layout; could successfully type 4-5 letter
words using switch
Tobii C-12 Used the scanning technique , improved
with row selection, could type sentences
using the special features of the device
Mega-Bee Used Eye-gaze and eye movements to
communicate, was faster and more efficient
in typing out words/sentences

The patient showed remarkable improvement with the use of these AAC
devices. With regular training, she demonstrated accurate timing of button
selection. Although there was a tendency to anticipate switch activation and select
a button too early in the scan, she got more efficient with row/column scanning
eventually.
During progressive sessions, the patient’s progress continued as she
successfully typed answers to questions in which the target word was unknown to
others. For example, “What is the color of your house?”
There are, however, a few drawbacks of AAC that need to be considered. To
begin with, the cost of the device is the biggest drawback. Apart from the money
involved, technical glitches are expected at some point. It needs a power source as
it runs on battery. At the same time, patient’s family needs to be educated about
the technical aspects of the device and how to customize it as per the patient’s
needs.
The interaction between the patient and the surrounding environment including
with other people is not only a human's basic desire but also an important factor
for improving the quality of life. We cannot completely replace normal language
or emotional communication with the system applied for the patient. However,
this AAC can form and express not only a patient's basic demands but also
personal decision-making or deeper ideas. We can consider the return of a patient
skilled in the system to his/her career. [2]
The rehabilitation of locked-in patients is a long process and requires close
cooperation of a specialized group of experts. It is a particularly demanding
process for the patient and his/her next of kin, requiring persistence, patience and
optimistic belief in a better future. When a person has lost practically all
capabilities for voluntary activity, it is of vital importance to do everything to
improve his/her life, however small the steps may be. [6]
Utilization of information technology in health care and rehabilitation requires
from the rehabilitation team enthusiasm and constant learning and updating. There
are many possibilities to choose from, but the expert training and know-how
740 F.A.P. Sharma and S.B.Y. Jobanputra

required for planning individual methods and programs need continuous


development. [6]
Therefore, this case study will provide the possibility and opportunity of
communication to LIS patients, and it will also contribute to the generalization of
the communication device and its actual use, for the relevant patients' return to
their family and society.

References
[1] Smith, E., Delargy, M.: Locked-in syndrome. BMJ 330, 406–409 (2005)
[2] Si-Woon Park, M.D., You-lim Yim, M.D., Sook-hee Yi, M.D., Hyun-young Kim,
O.T., Seung-min Jung, P.T.: Augmentative and Alternative Communication training
using eye-blink switch in a Locked-In Syndrome patient. Ann. Rebabil. Med. 36(2),
268–272 (2012)
[3] Patterson, J.R., Grabois, M.: Locked-in syndrome: a review of 139 cases. Stroke 17,
758–764 (1986)
[4] Doble, J.E., Haig, A.J., Anderson, C., Katz, R.: Impairment, activity, participation, life
satisfaction and survival in persons with locked-in syndrome for over a decade: follow-
up on a previously reported cohort. J. Head Trauma. Rehabil. 18, 435–444 (2003)
[5] Casanova, E., Lazzari, R.E., Latta, S., Mazzucchi, A.: Locked-in syndrome:
improvement in the prognosis after an early intensive multi-disciplinary rehabilitation.
Arch. Phys. Med. Rehabil. 84, 862–867 (2003)
[6] Söderholm, S., Meinander, M., Alaranta, H.: Augmentative and alternative
communication methods in locked-in syndrome. J. Rehabil. Med. 33, 235–239 (2001)
[7] Bauer, G., Gerstenbrand, F., Rumpl, E.: Varieties of the locked-in syndrome. J.
Neurol. 221, 77–91 (1979)
Validation and Test of a Closed-Loop
Tele-rehabilitation System Based on Functional
Electrical Stimulation and Computer Vision for
Analysing Facial Expressions in Stroke Patients

Daniel Simonsen1, Ramin Irani2, Kamal Nasrollahi2, John Hansen1,


Erika Geraldina Spaich1, Thomas B. Moeslund2, and Ole Kæseler Andersen1
1
Center for Sensory-Motor Interaction, Aalborg University, Denmark
dsim@hst.aau.dk
2
Visual Analysis of People Laboratory, Aalborg University, Denmark

Abstract. The aim of the present study was to validate and test a closed-loop tele-
rehabilitation system for training of hand function and analyzing facial
expressions in stroke patients. The paper presents the methods for controlling
functional electrical stimulation (FES) to assist hand opening and grasping. The
main outcome of the FES control was time differences in grip detections
performed by the automatic system and by analysis of the output from force
sensing resistors. This time difference was in the range of 0 to 0.8 s. Results from
analysis of facial expressions were very variable showing that subjects were
disgusted, happy and angry during the exercises, which were not in agreement
with the observations made during the experimental sessions.

1 Introduction

Stroke is a leading cause of disability worldwide [1]. Studies on stroke


rehabilitation have shown that stroke patients are capable of regaining motor
control to some extent by rehabilitative training, especially in the first months post
stroke [2, 3]. However, hand function often remains significantly affected [3].
Since proper motor function of the hand, i.e. hand opening and grasping, is related
to activities of daily living this has a major impact on the patient’s daily life.
Therefore, it is of great importance to exploit the time window for rehabilitation
post stroke, in order to maximize the outcome of rehabilitation, particularly in
relation to hand function. Generally, stroke patients receive intensive
rehabilitation subsequent to the acute treatment of the stroke, but the amount of
time spent on self-training by the patient in his or hers own home will most likely
increase. At home the patient is not supervised and supported by a therapist. This
might mean that the patient has an increased risk of performing the exercises
wrong or in some cases might not even be able to complete the exercises due to a
lack of sufficient motor function. Furthermore, training at distance without

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 741
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_103, © Springer International Publishing Switzerland 2014
742 D. Simonsen et al.

continuous supervision obviously makes it difficult for therapists to detect non-


spoken social cues (facial expressions/body language), which might provide
crucial information about how well the patient mentally complies with the
rehabilitation.
Reviews of tele-rehabilitation studies state that the current evidence is
insufficient to draw definite conclusions upon the effectiveness of tele-
rehabilitation of stroke patients [4, 5]. Common for the studies included in the
reviews is that the support given to the patients during self-training is either non-
existing or limited to visual feedback. As a consequence it will not make sense for
the patients to start using these systems before they can comply with the self-
training exercises. By combining a tele-rehabilitation system with a system that
can assist the patients in complying both physically and mentally with the self-
training exercises a broader range of patients can be targeted and rehabilitation
training in the patient’s own home might be more efficient.
Functional electrical stimulation (FES) of the muscles is a method for assisting
stroke patients in performing functional movements [6]. FES rehabilitation
systems are triggered by user input, often by surface electromyographic (EMG)
signals, or cyclically according to predefined settings. A meta-analysis by [7],
found no significant difference in rehabilitative outcome in stroke patients
between use of EMG-triggered FES and conventional care. Although studies show
that FES rehabilitation systems might be comparable to conventional care, they
are not designed as tele-rehabilitation systems and thus are not suited for use
during self-training in the patient’s own home. Furthermore, current FES
rehabilitation systems require some kind of direct user input for triggering the
assistive stimulation, which means that the user cannot solely focus on the
execution of the movements during training.
By use of a camera it is possible to monitor the patient’s movements during
training. By performing real-time analysis on the images captured by the camera it
is possible to control FES, thus eliminating the need for direct user input to trigger
the electrical stimulations. Furthermore, cameras can also be used for recording
facial expressions. Parameters derived from facial expressions are the most
effective ones in visual information as they provide clues to recognize the mental
state of a person. The majority of the methods reported in the literature use only
facial expressions for automatic emotional recognition. These works are mostly
based on Charles Darwin’s idea [8] which established general principles of
expressions and their meanings on the face of both human and animals. In 1978
Ekman [9] defined a new scheme named Facial Action Coding Scheme, which
involves 64 basic Action Units (AUs) and combination of AUs representing
movement of facial muscles.
In this paper a tele-rehabilitation system for assisting training of hand function
and recognizing facial expressions in stroke patients is presented. The system
controls FES in a closed loop by a Microsoft Kinect sensor, and records facial
expressions by a web camera.
Validation and Test of a Closed-Loop Tele-rehabilitation System 743

2 Methods

2.1 Subjects
Four subjects were included in the study. They were aged between 18 to 80 years,
previously diagnosed with a cerebrovascular stroke (verified by a MRI scan), had
decreased hand function, and were able to sit upright without support. Subjects
were excluded if they were pregnant, drug addictive (hash, opioids or other
psychedelic drugs), not able to understand the aim of the study and complete the
experiment due to cognitive or linguistic deficits, suffering from serious general
deterioration, had a pacemaker, or local infection at the stimulation sites. Written
informed consent was obtained from all subjects prior to participation and the
Declaration of Helsinki was respected. The study was approved by the local ethical
committee of the North Denmark Region (approval no. N-20130053).

2.2 Functional Electrical Stimulation


In the beginning of each experimental session, stimulation sites for delivering FES
to assist the subject with hand opening and hand grasping were identified. A total
of up to eight self-adhesive surface electrodes (Pals Platinum Round 3.2 cm,
Axelgaard Ltd., USA) were placed targeting the following muscle groups: m.
flexor digitorum profundus, m. flexor digitorum superficialis, and m. abductor
pollicis (hand grasping), m. extensor digitorum communis, m. extensor pollicis
longus, and m. abductor pollicis (hand opening). The stimulation consisted of a
pulse train with a frequency of 30 Hz and square pulse duration of 200 µs. The
intensity of each stimulation channel was set to the level where visible motor
activation occurred (motor threshold) plus 2 mA. The onset of stimulation assisting
hand opening and grasping was controlled by the system. The duration of the
stimulation assisting hand opening was set to 2.5 s, while the duration of
stimulation assisting hand grasping was controlled by the system.

2.3 Hand Function Exercise


A hand function exercise was performed by the subjects seated on a chair in front
of the table. The exercise involved lifting and moving a cylindrical object
in the sagittal plane between two squares (located ~70 mm apart) marked on the
table.
Two cylindrical objects (denoted as the “small-” and “large- cylinder”) were
used in the hand function exercise. The cylinders had grey colored sides, a green
colored lid, equal heights (100 mm) and weights (300 g). The diameters of the
small and large cylinder were 40 mm and 75 mm respectively.
744 D. Simonsen et al.

2.4 Monitoring of Grip Force


The small and large cylinder had two or four 38 mm square force sensing resistors
(Interlink Electronics FSR® 406) mounted on the side, respectively (Fig. 1).

Fig. 1 Illustration of the large cylinder with FSRs mounted on the side. A total of 4 FSRs
were mounted on the side of the large cylinder.

These FSRs provided a continuous measure of the grip force applied to the
cylinder during the hand function exercise (ranging from 0-10 V). Each FSR was
sampled at 1000 Hz and data were saved for offline analysis. The activity for all
FSRs was summed in the online analysis. A grip was considered to be established
when the summed FSR activity exceeded 0.2 V.

2.5 Monitoring of Hand and Cylinder Kinematics


A Microsoft Kinect sensor was used for recording and analyzing the kinematics of
the subject’s hand and the cylinder during the hand function exercise. The Kinect
sensor captured depth images and RGB images in a resolution of 640 x 480 pixels
at 30 frames per second [10]. The sensor was mounted on a tripod and positioned
85 cm above the table surface providing a top-down view of the table. The
position of the camera resulted in a distance between each pixel of approximately
1.5 mm.

2.6 Control of Functional Electrical Stimulation


The control of FES for hand opening once the hand was approaching the cylinder
was based on the distance between the cylinder and the hand. FES for hand opening
was triggered once the distance was between 200 mm and 30 mm (all distances are
Euclidian distances). The control of FES for hand opening once the cylinder was
placed in the target area (one of the two squares marked on the table) was based on
the distance between the table and the bottom of the cylinder. A distance less than
10 mm triggered FES for hand opening.
FES for hand grasping was triggered once a grip around the cylinder was
detected by the system (method for grip detection is described in section 1). FES
continued for each frame where grip was detected.
Validation and Test of a Closed-Loop Tele-rehabilitation System 745

2.7 Cylinder Detection


The detection of the cylinder was based on the RGB images. In each frame the
RGB image was filtered in order to extract green colored pixels. The identified
pixels were labelled as pixels representing the cylinder surface.

2.8 Hand Detection


Hand detection was based on both the RGB and depth image. Based on the depth
image pixels with depth values in the range of the table surface were excluded as
the majority of these pixels represented the table surface. Also the pixels
representing the cylinder were excluded. Finally, all connected pixels were grouped
(a pixel was considered to be connected to another pixel if it was located exactly on
top, below, left or right to the other pixel). Groups of less than 50 pixels were
excluded, since most of these were either pixels representing the cylinder or the
table. The remaining group(s) of pixels was labelled as pixels representing the
hand.

2.9 Grip Detection


In frames where the distance between the hand and the cylinder was less than 30
mm, the system would determine whether a grip around the cylinder had been
established. Initially a subset of the depth and RGB images for the present frame
was used. The dimensions of the quadratic image subset were equal to the diameter
of the cylinder plus 30 mm. The center of the quadratic image was matched with
the estimated centroid of the cylinder.
The hand labelled pixels in the upper left and lower right part of the image were
then used pairwise in a geometric calculation to determine whether the centroid of
the cylinder was located left to the line intersecting the combination of points (Fig.
2). This was one of two requirements that had to be fulfilled in one case or more for
a grip to be detected.
For each frame the mean of the distances of all hand labelled pixels to the
centroid of the cylinder was saved. Initially, a grip was detected if this mean
distance was less than the radius of the cylinder plus 15 mm. In the frames
following a frame where grip had been detected a grip was still detected only if the
mean distance of the present frame was less than the minimum mean distance
detected during the session.

2.10 Facial Expression Recognition


In order to analyze the emotional state of the patient during the experiment, a
Logitech webcam was used for capturing frontal facial images of the patient at 30
frames per second with a resolution of 640 x 480 pixels. Emotional states
were analyzed by a commercial facial expression recognition system, “Facereader
746 D. Simonsen et al.

Ver. 5.1”©, which recognizes six basic expressions: sadness, disgust, happiness,
anger, surprise, fear, and neutral. This system is based upon the Active appearance
model (AAM), which is typically used for facial emotion recognition [11].

3 Results

3.1 Differences in Grip Detections by FSRs and System


The absolute mean time differences in grip detection based on the FSRs and the
Kinect output ranged from 0.18-0.27 s (Fig. 3).

Fig. 2 On the left the subset of the RGB image is shown in greyscale. The image on the
right side shows the pixels representing the hand (the dots mark the centroid of the small
cylinder)

The average number of grips detected under the different conditions is summed
up in Table 1.

Table 1 Average number of detected grips (±standard deviations)

C_S F_0 C_L F_0 C_S F_1 C_L F_1


10.0±10.9 9.0±11.5 13.8±11.5 14.8±9.9

3.2 Subjects’ Emotional Expression


It can be seen from Table 2 that subject 1 is mostly disgusted, subject 2 is mostly
happy, subject 3 is mostly neutral, and subject 4 is mostly angry during the
exercises.
Validation and Test of a Closed-Loop Tele-rehabilitation System 747

Fig. 3 Mean time differences and 95 % CI. “C_S”: small cylinder, “C_L”: large cylinder.
“F_0”: FES not applied, “F_1” FES applied.

Table 2 Subjects’ emotional expression in percentage

Subject Fear Sadness Surprise Disgust Happy Anger Neutral


1 <1% <1% <1% 52% 10% <1% 43%
2 <1% <1% 2% <1% 57% 8% 41%
3 <1% <1% <1% <1% 4% 25% 72%
4 <1% <1% <1% <1% 45% 70% 20%

4 Discussion

4.1 Functional Electrical Stimulation


In two out of four subjects, it was not possible to increase the intensity of FES to a
sufficient level to elicit motor responses without causing pain. Therefore, the
intensity of FES given to these subjects during the experiment was below motor
threshold meaning that the subjects did not experience any assistance in hand
opening and grasping.

4.2 Monitoring of Grip Force


The method for monitoring grip force during the experiment was based on FSRs
placed on the side of the cylinders. In cases where the position of the subjects
hand during grasping was on the edge of the FSRs, the force recorded by the FSRs
was close to zero. For that reason some of the grasps performed by the subjects
had to be excluded from the analysis. Grasps were also excluded in cases where
the subject used the other hand to establish the grasp.
748 D. Simonsen et al.

4.3 Control of Functional Electrical Stimulation


This study used a fixed duration of 2.5 s of FES for assisting hand opening, and as
a result of this the subjects had to wait for the stimulation to finish before grabbing
the cylinder. Not all subjects had enough patience to wait for the stimulation to
finish and consequently they grabbed the cylinder while getting stimulation
assisting hand opening.
The onset of FES assisting hand grasping, i.e. facilitating the grip, relied on the
ability of the system to detect when a grip was present. When comparing the time
for grips detected by the system and the FSR sensors on the objects, an absolute
mean difference less than 0.3 s was found. Similarly, another study using the
Kinect sensor for detection of hand closing postures compared the difference
between detections of movement onset by the Kinect sensor with onset of EMG
activity in the hand flexor muscles and found a mean difference less than 0.25 s
[12].

4.4 Object Detection


The method used for detection of the cylinders was solely based on the color of
the lid of the cylinder. Therefore, the detection of the cylinder was sensitive to
changes in the background light. This is a common issue for all the methods
including analysis of RGB images. The method is also sensitive to objects with a
color similar to that of the cylinder in case that this object is located too close to
the cylinder or is larger than the cylinder. This problem might be solved by
combining the existing method with estimation of the size of the detected objects
from the depth images. Then objects that are too small or too large compared to
the size of the cylinder can be excluded.
The method for detection of the hand of the subject was based on both the
depth and RGB image. It would have been preferable to detect the hand from the
depth image alone. However, this was not possible for the frames where
the subject had established a grasp around the cylinder. In these frames the depth
information of parts of the fingers was not available most likely due to a
shadowing effect caused by the cylinder (the infrared beams from the Kinect
sensor were reflected by the cylinder before they reached the fingers located closer
to the table surface). Therefore these parts of the hand could not be detected.
The clinical value of the system is highly dependent on the precision of the
captured kinematics, but the present study has not validated the precision of the
object detection. A previous study has shown that the Kinect sensor can be used
for detection and tracking of finger joints angles with an average absolute error
ranging from 2.4 to 4.8 degrees [13].
Validation and Test of a Closed-Loop Tele-rehabilitation System 749

4.5 Facial Expression Recognition


Our own observations and questioning of the subjects showed that in most cases
they were actually neutral even though results from the facial expression
recognition yielded that three out of four subjects were mainly non-neutral. The
difference between the results of Facereader and our own observations might be
due to the insufficient facial muscle control of the patients. In addition to the facial
analysis of the patients during the exercises we asked one of the patients to express
the six mentioned basic facial expressions in the end of the experimental session
(each facial expression was maintained for approximately 15 seconds). We
observed that it was very hard for the subject to do that though she tried her best.
Even though she was not able to show her emotion at all, Facereader was still
detecting wrong emotional states, clearly indicating a shortage in the classification
approach.

5 Conclusion

In this study, it has been shown that it is possible to control FES assisting hand
opening and grasping by a Microsoft Kinect sensor. When comparing the time for
grips detected by the system and the FSR sensors on the objects, an absolute mean
difference of less than 0.3 s was found. Such a difference would be functionally
useable.
The results from the study also suggest that present facial expression recognition
systems are not reliable for recognizing patients’ emotional states especially when
they have difficulties to control/move their facial muscles. For addressing these
issues, one may train facial expression recognition systems with facial images
captured directly from patients and then combine the results with physiological
signals of facial images, similar to our previous work at [14]. Combining the
system with proper facial expression recognition would make it possible for the
system to provide the patient different kinds of feedback, e.g. changing the level of
difficulty of the task when the patient has been detected as being bored.
Acknowledgment. The research council for Technology and Production supported the
study. Træningsenheden, Aalborg Municipality, assisted with the clinical validation studies.

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[4] Laver, K.E., Schoene, D., Crotty, M., George, S., Lannin, N.A., Sherrington, C.:
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[6] Schuhfried, O., Crevenna, R., Fialka-Moser, V., Paternostro-Sluga, T.: Non-invasive
neuromuscular electrical stimulation in patients with central nervous system lesions:
an educational review. J. Rehabil. Med. 44, 99–105 (2012)
[7] Meilink, A., Hemmen, B., Seelen, H., Kwakkel, G.: Impact of EMG-triggered
neuromuscular stimulation of the wrist and finger extensors of the paretic hand after
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en-us/kinectforwindows/discover/features.aspx
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emotion recognition for human–machine interaction. In: Emotion-Oriented Systems,
Pt. 2, pp. 133–159. Springer (2011)
[12] Scherer, R., Wagner, J., Moitzi, G., Müller-Putz, G.: Kinect-based detection of self-
paced hand movements: Enhancing Functional Brain Mapping paradigms. In: 34th
Annual International Conference of the IEEE EMBS (2012)
[13] Metcalf, C.D., Robinson, R., Malpass, A.J., Bogle, T.P., Dell, T.A., Harris, C.,
Demain, S.H.: Markerless Motion Capture and Measurement of Hand Kinematics:
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[14] Irani, R., Nasrollahi, K., Moeslund, B.: Improved Pulse Detection from Head Motions
Using DCT. In: 9th International Conference on Computer Vision Theory and
Applications, Lisbon (2014)
Gait Orthosis Lokomat Combined with
Functional Electrical Stimulation for Foot Drop
Correction: A Feasibility Study

Erika Geraldina Spaich1, Mette F. Bøg1, Ema Erkocevic1, Anne Smidstrup1,


Ole Kæseler Andersen1, and Jørgen Feldbæk Nielsen2
1
Aalborg University, Aalborg, Denmark
espaich@hst.aau.dk
2
Hammel Neurorehabilitation and Research Center, Hammel, Denmark
joerniel@rm.dk

Abstract. The purpose of this study was to investigate the feasibility of combining
Lokomat based gait training with functional electrical stimulation (FES) to correct
foot drop. An individual who suffered a stroke and two healthy subjects
participated in the experiment. Transcutaneous functional electrical stimulation of
the common peroneal nerve was synchronized to Lokomat to support dorsiflexion
of the foot during the swing phase of the gait cycle. The results showed a lift of
the foot in the hemiparetic side of the patient during the swing phase, with a
significant increase of the mean ankle angle when training in Lokomat with FES
compared to training in Lokomat without FES (p<0.001). The system combining
Lokomat and FES for correcting foot drop proved to function as expected and
supported a functional gait.

1 Introduction

People who have suffered a stroke often present a compromised gait pattern with
diverse spatiotemporal and kinematic deviations from normal gait, among them
the difficulty to dorsiflex the ankle joint during the swing phase. This is known as
foot drop [1]. It has been suggested that a neuroplastically determined time
window is present, where the greatest gain can be achieved through rehabilitation
in the early phase post injury [2]. Hence, an early and intense rehabilitation
process is desirable after neurological stabilization.
Gait orthoses with body weight support have made early rehabilitation possible
even when the locomotion skills of the patient are very limited [3]. One such
system is the gait orthosis Lokomat (Hocoma AG, Volketswill, Switzerland).
Lokomat consists of an exoskeleton that guides the patient while walking on a
treadmill [4;5]. Improved cardiovascular fitness and gait function have been
shown in stroke patients after training with Lokomat [4-6]. Although Lokomat
assists the patient in regaining a symmetrical gait pattern [5;7], it does not provide
an active mobilization of the ankle joint [8].

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 751
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_104, © Springer International Publishing Switzerland 2014
752 E.G. Spaich et al.

The use of functional electrical stimulation (FES) to correct foot drop is widely
documented, also when combined with other training techniques to improve the
therapeutic effect [3;9-11].
Combining Lokomat training with FES to correct foot drop would provide the
possibility of an early and intensive intervention with consistent and repetitive
movements including an active training of the ankle joint. The aim of the current
study was therefore to investigate the feasibility of combining Lokomat and FES
for the rehabilitation of gait, with focus on the restoration of dorsiflexion of the
ankle.

2 Methods

2.1 Participants
This study included a 79 years old female subject who suffered a stroke two weeks
prior to the experiment and presented moderate foot drop. Additionally, two
healthy subjects (mean age: 24.5 years old) participated in the study to provide
control recordings of walking assisted by Lokomat.
The study was conducted according to the Declaration of Helsinki and was
approved by the local Ethics Committee (ESDH 1-10-72-135-12). All participants
gave their written informed consent prior to enrollment.

2.2 Lokomat
A gait orthosis Lokomat was used in the experiment. To keep the foot in neutral
position, the spring-strap system of Lokomat was used. Lokomat provided output
signals consisting of a square pulse (duration: 200 ms and amplitude: 5 V)
indicating the beginning of the stance phase of each leg.

2.3 Functional Electrical Stimulation


A computer controlled, constant current stimulator was used to deliver the
electrical stimulation (frequency: 30 Hz, pulse duration: 300 µs, amplitude: 23
mA). The stimulation electrodes were placed on the hemiparetic side of the stroke
subject, the cathode (Pals Platinum Round 3.2 cm, Axelgaard Ltd., USA) was
placed above the peroneal nerve close to the fibular head, while the anode (Pals
Platinum Oval 4.0x6.4 cm, Axelgaard Ltd., USA) was placed on the proximal
aspect of the tibialis anterior muscle.
The duration of the electrical stimulation train was controlled by the output
signals from Lokomat. Stimulation was started when triggered by the ascending
edge of the pulse indicating the beginning of the stance phase of the contralateral
leg. Stimulation was stopped when triggered by the descending edge of the pulse
Gait Orthosis Lokomat Combined with Functional Electrical Stimulation 753

indicating the beginning of the stance phase of the ipsilateral leg. With this
approach, stimulation was delivered approximately during the entire push-off and
swing phases of the ipsilateral, hemiparetic leg.

2.4 Experimental Protocol


An experienced therapist placed the subjects in Lokomat and set the necessary
parameters of the gait orthosis (Table 1). Prior to starting the actual experiment,
subjects were given time to get used to the gait pattern imposed by Lokomat at the
set treadmill speed. Afterwards, the stroke subject walked for four minutes
without receiving FES (woFES), had a resting break, and walked for four more
minutes while receiving FES synchronized with the gait pattern determined by
Lokomat (wFES). The healthy subjects walked without receiving FES.

Table 1 Parameter settings in Lokomat

Healthy Healthy
Parameter Stroke subject
subject #1 subject #2
Body weight
27 17 19
support (kg.)
Treadmill
1.3 1.5 1.5
speed (km/h)
Patient
0.41 0.44 0.45
coefficient
Guidance
100% 100% 100%
force

2.5 Outcome Measures


The movement of the ankle joint in the sagittal plane was measured with a
goniometer (SG110/A, Biometrics Ltd., Gwent, UK). The output signals from
Lokomat indicating the beginning of the stance phase of both legs were also
recorded and stored for later offline analysis.

2.6 Data Analysis


The goniometric signals were low-pass filtered (no phase lag Butterworth filter, 4th
order, 10 Hz), segmented according to the step cycle using the output signals from
Lokomat, and normalized to 100% of the gait cycle. The mean ankle angle
trajectory (±SEM) was calculated for all steps wFES and woFES.
Three measures of ankle angles were obtained: 1) swing angle, the mean ankle
angle during the swing phase, defined as 62-95% of the gait cycle [12]; 2) peak
plantarflexion, peak to peak amplitude from heel-off to peak plantarflexion; and 3)
peak dorsiflexion, peak to peak amplitude from peak plantarflexion to peak
dorsiflexion before heel-strike.
754 E.G. Spaich et al.

2.7 Statistical Analysis


T-test was used to study differences in the measures of ankle angles of the stroke
subject walking in Lokomat wFES and woFES. Homogeneity of variances was
tested using Levene test. If homogeneity was not present, the Welch-Satterthwaite
method was used to compensate for this violation. A significance level of 0.05
was considered.

3 Results

The mean ankle angle trajectories for the stroke subject walking in Lokomat
wFES and woFES and for the two healthy subjects walking in Lokomat woFES
are shown in Fig. 1. Walking assisted by Lokomat and FES provided a lift of the
foot of the stroke subject during the entire swing phase. This resulted in
maintaining the foot at an ankle angle close to neutral, achieving an ankle angle
trajectory similar to that of one of the healthy subjects.

Fig. 1 Mean ankle angle trajectories for all gait cycles of the stroke subject walking wFES
and woFES and for the two healty subjects walking woFES. The grey areas represent the
SEM.

Walking wFES caused a significant change of the swing angle of the stroke
subject (p<0.001) that changed from an average of -5.8 degrees to -0.31 degrees
(Fig. 2). Furthermore, decreased peak plantarflexion and peak dorsiflexion were
measured when walking wFES (p<0.001 for both).
Gait Orthosis Lokomat Combined with Functional Electrical Stimulation 755

Fig. 2 Mean ankle angle measurements of the stroke subject walking woFES and wFES.
The error bars are 95% confidence intervals of the mean. The asterisk indicates a significant
difference (p<0.001).

4 Discussion

The decrease in both peak plantarflexion and dorsiflexion observed when walking
with FES can be interpreted as an earlier start of the take-off and swing phases.
The foot did not reach the degree of plantarflexion achieved when walking
without FES due to the electrical stimulation. Furthermore, the induced
dorsiflexion was kept almost constant, thus stabilizing the ankle joint in neutral
position. This cleared the foot from the ground and supported a more functional
gait. This was also supported by the fact that the trajectory achieved after heel-off
seemed similar to that of a healthy subject walking without FES.
When combining FES with Lokomat, it was possible to use the output signals
from Lokomat to synchronize the stimulation without needing to use any
additional sensors. Dohring and Daly [13] used the signal from Lokomat to trigger
a predefined stimulation train that needed to be adjusted to the walking speed. In
the present study, FES was both initiated and terminated by the output signals
from Lokomat, thereby automatically adapting the duration of the stimulation train
to the walking speed set by Lokomat. This setup resulted in a functional response
that induced dorsiflexion with the right timing. A possible improvement of the
system would be to implement a delay in the onset of the stimulation in order to
allow for some push-off before the ankle dorsiflexors are activated.
The synchronization with Lokomat that does not require further sensors and the
use of a single FES channel makes this paradigm easy to implement in the clinical
environment. Placing the stimulation electrodes in order to achieve the desired
ankle movement is, however, a critical aspect and a common problem when using
surface FES [14].
756 E.G. Spaich et al.

5 Conclusion

The system combining Lokomat and FES for correcting foot drop proved to
function as expected, supported a functional gait and kept the ankle joint in neutral
position during the swing phase. Future studies should include several stroke
individuals and investigate the therapeutic effect of such an intervention.

Acknowledgment. The authors would like to thank physiotherapist Brian Hangaard for his
assistance during the experiments.

References
[1] Olney, S.J., Richards, C.: Hemiparetic gait following stroke. Part I: Characteristics.
Gait & Posture 4(2), 136–148 (1996)
[2] Murphy, T.H., Corbett, D.: Plasticity during stroke recovery: from synapse to
behaviour. Nature Reviews Neuroscience 10(12), 861–872 (2009)
[3] Belda-Lois, J.M., Mena-del, H.S., Bermejo-Bosch, I., Moreno, J.C., Pons, J.L.,
Farina, D., Iosa, M., Molinari, M., Tamburella, F., Ramos, A., Caria, A., Solis-
Escalante, T., Brunner, C., Rea, M.: Rehabilitation of gait after stroke: a review
towards a top-down approach. J. Neuroeng. Rehabil. 8, 66–84 (2011)
[4] Husemann, B., Muller, F., Krewer, C., Heller, S., Koenig, E.: Effects of locomotion
training with assistance of a robot-driven gait orthosis in hemiparetic patients after
stroke: a randomized controlled pilot study. Stroke 38(2), 349–354 (2007)
[5] Westlake, K.P., Patten, C.: Pilot study of Lokomat versus manual-assisted treadmill
training for locomotor recovery post-stroke. J. Neuroeng. Rehabil. 6, 18 (2009)
[6] Chang, W.H., Kim, M.S., Huh, J.P., Lee, P.K., Kim, Y.H.: Effects of robot-assisted
gait training on cardiopulmonary fitness in subacute stroke patients: a randomized
controlled study. Neurorehabil. Neural Repair 26(4), 318–324 (2012)
[7] Stoller, O., Waser, M., Stammler, L., Schuster, C.: Evaluation of robot-assisted gait
training using integrated biofeedback in neurologic disorders. Gait Posture 35(4),
595–600 (2012)
[8] McCabe, J.P., Dohring, M.E., Marsolais, E.B., Rogers, J., Burdsall, R., Roenigk, K.,
Pundik, S., Daly, J.J.: Feasibility of combining gait robot and multichannel functional
electrical stimulation with intramuscular electrodes. J. Rehabil. Res. Dev. 45(7), 997–
1006 (2008)
[9] Liberson, W.T., Holmquest, H.J., Scot, D., Dow, M.: Functional electrotherapy:
stimulation of the peroneal nerve synchronized with the swing phase of the gait of
hemiplegic patients. Arch. Phys. Med. Rehabil. 42, 101–105 (1961)
[10] Sabut, S.K., Sikdar, C., Kumar, R., Mahadevappa, M.: Improvement of gait & muscle
strength with functional electrical stimulation in sub-acute & chronic stroke patients.
Conf. Proc. IEEE Eng Med. Biol. Soc. 2011, 2085–2088 (2011)
[11] Lindquist, A.R., Prado, C.L., Barros, R.M., Mattioli, R., da Costa, P.H., Salvini, T.F.:
Gait training combining partial body-weight support, a treadmill, and functional
electrical stimulation: effects on poststroke gait. Phys. Ther. 87(9), 1144–1154 (2007)
[12] Whittle, M.W.: Gait analysis - An introduction, 4th edn. (2007)
Gait Orthosis Lokomat Combined with Functional Electrical Stimulation 757

[13] Dohring, M.E., Daly, J.J.: Automatic synchronization of functional electrical


stimulation and robotic assisted treadmill training. IEEE Trans. Neural Syst. Rehabil.
Eng. 16(3), 310–313 (2008)
[14] Lyons, G.M., Sinkjaer, T., Burridge, J.H., Wilcox, D.J.: A review of portable FES-
based neural orthoses for the correction of drop foot. IEEE Trans. Neural Syst.
Rehabil. Eng. 10(4), 260–279 (2002)
Learning Effect of the Nintendo Wii Agility Test
in Community-Dwelling Older Adults

Erika Geraldina Spaich1, Nicolas B. Hansen1, Alberto L.R. Perez2,


and Martin G. Jørgensen3
1
Aalborg University, Aalborg, Denmark
espaich@hst.aau.dk, nicolas@sejlsport.dk
2
Bispebjerg Hospital, Copenhagen, Denmark
alberto.luis.rodriguez.perez.01@regionh.dk
3
Aalborg University Hospital, Aalborg, Denmark
martin.joergensen@rn.dk

Abstract. The purpose of the study was to characterize the learning effect of the
Nintendo Wii Agility test as performed repetitively by a population of
community-dwelling older people with no recent history of falls. 35 older adults
participated in this study and each performed 10 trials of the Agility test, with rest-
periods of 30 seconds between tests, in a single session. Results showed that to
achieve an estimation error of ≤5% in the Agility test at least five repetitions were
needed. Additionally, the minimum effect size that could be measured using the
Agility test was determined for the number of repetitions in the test. The test is
easy to perform, inexpensive, and is feasible to implement in a clinical setting.

1 Introduction
Impaired postural balance is a major risk factor for fall accidents among elderly
people and individuals with neuromuscular diseases [1-3]. Fall related injuries are
associated to increased morbidity and mortality [4;5] with the consequent costs for
the health care system. Assessment of postural balance is therefore a key element
in the process of identifying potential fallers, and evaluating the effect of
treatments to prevent and decrease the number of falls.
The Nintendo Wii Fit gaming system (Nintendo Corporation, Kyoto, Japan)
consisting of the Nintendo Wii Balance Board (NWBB), the Wii console, and ad
hoc software has received considerable interest from researchers since it allows
assessing balance and training balance skills with a relatively inexpensive system
[6].
Within the Wii Fit Plus software two tests seem relevant for measuring postural
balance: the Stillness and the Agility Test. The reproducibility of the test scores
was studied in a population of community-dwelling older adults and showed that
while the Stillness test had no intra-day test-retest differences, the Agility test had
a systematic test-retest effect. The scores produced by repeating the Agility test
showed a learning effect that needs to be characterized, should the test be used to
assess postural balance. [7]

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 759
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_105, © Springer International Publishing Switzerland 2014
760 E.G. Spaich et al.

It is unknown how fast the learning effect occurs when the Agility test is
repeated various times during a single session. The purpose of this study was
therefore to characterize the learning effect by performing multiple trials of the
Agility test in a population of community-dwelling elderly people with no recent
history of falls.

2 Methods

2.1 Participants
The study included 35 older adults (27 women, 8 men) recruited at senior society
organizations in and around Copenhagen, Denmark (Table 1). Inclusion criteria
were: at least 65 years or older, a minimum score of 27 in the mini-mental state
examination, ability to ambulate independently with or without use of a cane, no
severe hearing and vision impairments, and no history of fall accidents within the
last 12 months.

Table 1 Demographics of the participants

Characteristics Mean - [range]

Age (yr.) 70.5 – [65-86]


Weight (kg) 68.6 – [44-124]
Height (cm) 169.8 – [153-183]

The study was conducted according to the Declaration of Helsinki and was
reported to the Danish Data Protection Agency. All participants gave their written
informed consent prior to enrollment.

2.2 Wii Agility Test


The Agility test is a 30 second biofeedback postural balance test with an outcome
score ranging from 0 to 30 levels (0 being the worst score). The objective of the
test is to move a red dot representing the Center of Pressure towards squares
displayed at different geometric locations on a TV as quickly as possible. The
levels of the Agility test are gradually more challenging, starting with only one
stationary tile, continuing with two and three stationary tiles, and finalizing with
moving targets (Fig. 1).
Participants performed 10 successive trials (separated by 30 seconds of rest) of
the Agility test standing on a NWBB, which was connected to the Nintendo Wii
console and a Samsung 40 inch LCD color television. The NWBB was placed
three meters away from the television screen. Participants were instructed to stand
with their feet placed at hip-width. Prior to testing, the Agility test was introduced
and demonstrated by an investigator.
Learning Effect of the Nintendo Wii Agility Test in Community 761

Fig. 1 Screenshoots of the Agility test (level 1 and 12) and outcome score indicated

2.3 Data Analysis


To characterize the learning effect, the scores were averaged using one to ten
repetitions of the test for each subject and the 95% confidence intervals for the 10
means were calculated across subjects.
To determine the minimum number of trials needed for obtaining a reliable
Agility test score, the estimation error was calculated as the difference between
the score calculated using all ten trials and the scores calculated using one to ten
repetitions for each subject. The error was expressed as a percent of the score
based on ten trials.
A paired t-test was used to compare the outcome of the Agility test after the
first trial to the mean of the ten trials. The significance level was set to 5%.

3 Results

Across subjects, the mean Agility test score after the first trial was 11.91±0.33
(mean±SEM), while the average after 10 trials was 12.83±0.18 (Fig. 2), indicating
an overall improvement in performance when repeating the test 10 times and using
the 10 individual scores to obtain a measure of performance (p<0.001, paired t-
test).
The 95% confidence intervals for the determination of the Agility test scores
based on the averaging of 1-10 trials are presented in Table 2 indicating a measure
of the precision of the calculated score.
Increasing the number of averaged trials in the calculation of the Agility test
score resulted in a decreased estimation error (Fig. 3). Averaging 5 or more
trials resulted in the entire 95% CI of the mean to be below the error threshold
of 5%.
762 E.G. Spaich et al.

Fig. 2 Mean Agility test score as a function of the number of trials averaged. Black circles
represent mean values and error bars represent the upper part of the 95% confidence
interval.

Table 2 Width of the 95% confidence interval for the different number of averaged trials
(1-10)

1 2 3 4 5 6 7 8 9 10

0.23 0.17 0.14 0.14 0.14 0.13 0.14 0.13 0.13 0.13

Fig. 3 Estimation error of the Agility test score as a function of the number of trials
averaged. The stippled line indicates an error of 5%. Black circles represent mean values
and error bars represent the upper part of the 95% confidence interval.
Learning Effect of the Nintendo Wii Agility Test in Community 763

4 Discussion

This study presented for the first time a characterization of the learning effect
observed while performing the Agility test repeatedly. The results showed that by
repeating the test, the performance measured by the Agility test score improved. It
was shown that by defining an arbitrary estimation error of the outcome score, it
was possible to determine the minimal amount of trials necessary to obtain a
reliable result.
The width of the confidence intervals of the means calculated averaging
different number of trials provides a tool to determine the minimum effect size
that could be measured using the Agility test. The minimum detectable effect size
would, according to our results, depend on the number of trials being averaged.
Combining this information, with the estimation error, and knowledge about the
physical ability of the subjects and the limits of fatigue would also be useful to
determine the number of trials to include in an experimental protocol.
In a previous study, no indication of ceiling or floor effects were observed for
the Agility test when used by a heterogeneous group of community-dwelling older
adults suggesting that the test could be used to assess a large range of older adults
[7].
To reduce the learning effect, the use of a familiarization period, in which the
subjects could perform the test a number of times, could be studied. This solution
has however, the potential undesired effect of tiring the subjects, especially
considering that a familiarization period of six trials seemed to show this effect
[7], which might be a considerable amount of trials for some older adults. In future
studies, it would be interesting to also characterize the inter-day learning effect.
In conclusion, this study showed a clear learning effect in the Nintendo Wii
Agility test when performing one to 10 trials during a single session. The number
of trials to repeat in an experimental protocol before most of the learning effect
has been eliminated could be determined using an estimation error, e.g. 5 trials for
a 5% estimation error. Also, the precision of the measured score depended on the
number of trials, which can be used to define the minimum effect size that could
be detected using a certain number of trials.

Acknowledgment. We would like thank Lone Schaadt, Physiotherapist at department of


geriatrics Bispebjerg Hospital, Copenhagen, for her help when running the experiment.

References
[1] Campbell, A.J., Spears, G.F., Borrie, M.J.: Examination by logistic regression
modelling of the variables which increase the relative risk of elderly women falling
compared to elderly men. J. Clin. Epidemiol. 43(12), 1415–1420 (1990)
[2] Teasell, R., McRae, M., Foley, N., Bhardwaj, A.: The incidence and consequences of
falls in stroke patients during inpatient rehabilitation: factors associated with high risk.
Arch. Phys. Med. Rehabil. 83(3), 329–333 (2002)
764 E.G. Spaich et al.

[3] Gray, P., Hildebrand, K.: Fall risk factors in Parkinson’s disease. J. Neurosci.
Nurs. 32(4), 222–228 (2000)
[4] Cummings-Vaughn, L.A., Gammack, J.K.: Falls, osteoporosis, and hip fractures. Med.
Clin. North Am. 95(3), 495–506 (2011)
[5] Ayoung-Chee, P., McIntyre, L., Ebel, B.E., Mack, C.D., McCormick, W., Maier, R.V.:
Long-term outcomes of ground-level falls in the elderly. J. Trauma Acute. Care
Surg. 76(2), 498–503 (2014)
[6] Goble, D.J., Cone, B.L., Fling, B.W.: Using the Wii Fit as a tool for balance
assessment and neurorehabilitation: the first half decade of “Wii-search”. J. Neuroeng.
Rehabil. 11(1), 12 (2014)
[7] Jorgensen, M.G., Laessoe, U., Hendriksen, C., Nielsen, O.B., Aagaard, P.: Intra-Rater
Reproducibility and Validity of Nintendo Wii Balance Testing in Community-
Dwelling Older Adults. J. Aging Phys. Act. (May 2013)
Functionality of the Contralateral Biceps
Femoris Reflex Response during Human
Walking

Andrew J.T. Stevenson1, Svend S. Geertsen2, Thomas Sinkjær3,


Jens B. Nielsen2, and Natalie Mrachacz-Kersting1
1
Center for Sensory-Motor Interaction, Aalborg University, Denmark
{ajts,nm}@hst.aau.dk
2
Department of Nutrition, Exercise and Sports,
and
Department of Neuroscience and Pharmacology,
University of Copenhagen, Denmark
ssgeertsen@ifi.ku.dk, jbnielsen@sund.ku.dk
3
Danish National Research Foundation, Copenhagen, Denmark
ts@dg.dk

Abstract. In this study we examined the functionality of the contralateral biceps


femoris (cBF) reflex response following ipsilateral knee extension joint rotations
during the late stance phase of the gait cycle [1]. Stevenson et al. [1] proposed that
the cBF reflex acts to slow the forward progression of the body in order to
maintain dynamic equilibrium during walking. Therefore, we hypothesized that if
we suddenly slowed the treadmill participants were walking on, the cBF reflex
would be inhibited because the necessity to break the forward progression of the
body would be decreased. Conversely, if we suddenly sped up the treadmill, the
breaking requirement would be greater and the cBF reflex would be larger. We
found this to be the case when the treadmill velocity was suddenly changed either
100 ms or 50 ms prior to the onset of the ipsilateral knee perturbations. The cBF
reflex was unchanged when the treadmill velocity was altered concurrently or 50
ms after knee perturbation onset. These results, together with the finding that the
cBF reflex response is under some cortical control [1], strongly suggest a
functional role for the cBF reflex during walking that is adaptable to the
environmental situation.

1 Introduction

Human walking displays an impressive ability to adapt to external perturbations


which may threaten dynamic stability. Interlimb reflexes have been proposed to
play a functional role in human locomotion [2, 3]. Contralateral reflex responses
have recently been demonstrated in the knee flexors during the late stance phase
of human gait [1]. Following unexpected extension perturbations to the ipsilateral

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 765
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_106, © Springer International Publishing Switzerland 2014
766 A.J.T. Stevenson et al.

knee joint at 50% of the gait cycle, the contralateral biceps femoris (cBF) muscle
was strongly facilitated at a latency of about 76 ms. Furthermore, the response was
found to be mediated in part by a transcortical pathway [1].
Stevenson et al. [1] hypothesized that the cBF reflex response may be a
preparation of the contralateral leg for early load bearing, slowing the forward
progression of the body in order to maintain dynamic equilibrium during walking.
This is consistent with the brief reflexive braking reaction observed in the cBF
muscle, among others, when the walking surface of the ipsilateral foot was
unexpectedly lowered at ipsilateral heel contact [4].
The objective of the present study was to investigate the functionality of the
cBF reflex response. We hypothesized that if we unexpectedly decreased the
speed of the treadmill participants were walking on, the cBF reflex would be
inhibited due to less slowing of the forward progression of the body being
required. On the contrary, if we unexpectedly increased the speed of the treadmill
participants were walking on, the cBF reflex would be facilitated due to the
forward progression of the body needing to be slowed further.

2 Methods

2.1 Participants
Six participants (three female) aged 20-34 years (24.3 ± 5.2, mean ± S.D.)
provided written informed consent to take part in this study. At the time of the
study, all participants were free of any known physical or neurological disorders.
Approval for the study was given by the scientific ethics committee for
Nordjylland (Reference Number: N-20110076). The study was performed in
accordance with the declaration of Helsinki.

2.2 Apparatus and Instrumentation


The knee perturbator used in this study was a semi-portable device that could
induce unexpected knee joint rotations (see [1, 5] for further details). The
functional joint consisted of a two-link joint connected to a powerful actuator by
Bowden wires. The actuator was positioned next to the treadmill that the
participant walked on. The motor was regulated by position feedback from the
joint in such a way that it followed the movement of the knee joint without
influencing the gait pattern. The perturbator was programmed to randomly apply
knee extension joint rotations at 50% of the gait cycle. The perturbations had a
ramp and hold of 200 ms, a constant velocity of 250-350°/s and amplitude of 6-
10° (see [1, 6]). During walking, the weight of the portable stretching apparatus
added an extra load of approximately 2 kg to the left leg. This has previously been
shown not to change the normal walking pattern compared to when participants
walked without the device [7].
Functionality of the Contralateral Biceps Femoris Reflex Response 767

During this study, participants walked on a split-belt treadmill (Split


70/157/ASK, Woodway GmbH, Weil am Rhein, Germany). The treadmill was
used to influence the participants’ gait by rapid changes in velocities at different
points in the gait cycle; relative to knee perturbation onset at 50% of the gait cycle
(-100 ms, -50 ms, 0 ms, and +50 ms), and at ipsilateral heel strike (0% of the gait
cycle). The main purpose of this study was to look at the effects of the initial
velocity change, which was to either speed up (+velocity trials) or slow down (-
velocity trials) the treadmill. During +velocity trials, the treadmill velocity
increased from the initial velocity by 0.56 m/s, then decreased by 1.12 m/s, then
increased by 1.12 m/s. During –velocity trials, the treadmill velocity decreased
from its initial velocity by 0.56 m/s, then increased by 1.12 m/s, then decreased by
1.12 m/s. Each of the velocity changes lasted for 500 ms, thus the whole treadmill
perturbation lasted for 1.5 seconds. The velocity changes occurred with an
acceleration of ± 5 m/s2.
Bipolar surface electrodes (Medicotest 720-01-K, AMBU A/S, Ballerup,
Denmark) were used to record electromyographic (EMG) activity of the ipsilateral
biceps femoris (iBF) and contralateral biceps femoris (cBF) muscles. The EMG
signals were amplified and band-pass filtered at 20 Hz – 2 kHz and rectified. A
flexible electrogoniometer (XM180 series, Biometrics Ltd., Cwmfelinfach,
Newport, UK) was used on two participants to trace the right knee joint angle. A
pressure sensitive trigger was placed under the left heel of the participants’ shoe
and used to trigger the sampling to the computer. A custom-made PC system
controlled the acquisition of the signals from the position-feedback channels and
the surface EMGs. All data were collected at a sampling frequency of 2 kHz.

2.3 Experimental Procedures


During the experiment, participants walked at a self-selected velocity between
0.83 and 1.11 m/s (mean velocity: 1.07 ± 0.05 m/s). Before testing, participants
walked for five minutes to become accustomed to the selected walking velocity
and the semi-portable device attached to the left leg. Following this, 20 steps were
recorded to establish the non-perturbed walking profile of each participant. From
the walking profile, 50% of the gait cycle of the ipsilateral leg was calculated. The
gait cycle percentage was defined as one ipsilateral leg heel contact
(corresponding to 0% of the gait cycle) to the next ipsilateral leg heel contact
(corresponding to 100% of the gait cycle). If the participants began to vary from
their initial stride time (±50 ms), they were verbally asked to increase or decrease
their stride time (necessary in three experimental sessions). All data were analyzed
off-line.
Following gait profile assessment, one of the following 11 conditions were
administered randomly every four to six steps:
1. Normal gait: no ipsilateral knee extension joint rotations and no treadmill
perturbations (60 trials).
768 A.J.T. Stevenson et al.

2. iKnee (ipsilateral knee) perturbation only: ipsilateral knee extension joint


rotations delivered at 50% of the gait cycle (60 trials).
3. Treadmill only –100 ms: treadmill perturbations delivered 100 ms prior to
50% of the gait cycle (30 +velocity trials and 30 –velocity trials).
4. iKnee & Treadmill –100 ms: a combination of conditions 2 and 3 (30
+velocity trials and 30 –velocity trials).
5. Treadmill only –50 ms: treadmill perturbations delivered 50 ms prior to 50%
of the gait cycle (30 +velocity trials and 30 –velocity trials).
6. iKnee & Treadmill –50 ms: a combination of conditions 2 and 5 (30
+velocity trials and 30 –velocity trials).
7. Treadmill only 0 ms: treadmill perturbations delivered at 50% of the gait
cycle (30 +velocity trials and 30 –velocity trials).
8. iKnee & Treadmill 0 ms: a combination of conditions 2 and 7 (30 +velocity
trials and 30 –velocity trials).
9. Treadmill only +50 ms: treadmill perturbations delivered 50 ms following
50% of the gait cycle (30 +velocity trials and 30 –velocity trials)
10. iKnee & Treadmill +50 ms: a combination of conditions 2 and 9 (30
+velocity trials and 30 –velocity trials).
11. Control trials: treadmill perturbations at 0% of the gait cycle in order to
decrease adaptation to the above treadmill perturbation timings (60 +velocity
trials and 60 –velocity trials).

There were a total of 720 trials. Participants were allowed to rest every 100
recorded steps, and were able to pause the experiment any stage if they reported
fatigue.

2.4 Data Analysis


A typical response from one participant in the cBF following iKnee only trials
(condition 2) is shown in Fig. 1D. The vertical dashed line in Fig. 1 indicates the
onset of the ipsilateral knee extension joint rotations.
Data for each individual participant were averaged across conditions and
quantification of responses was performed on these averaged trials. A window
commencing from the onset of the cBF reflex response until 120 ms following
iKnee onset was individually specified for each participant to determine the initial
reflex amplitude of the cBF response. The root mean square (RMS) of the cBF
EMG in the specific time window for each participant was extracted for each
condition, and for conditions 3-10 the RMS amplitude was extracted separately for
each treadmill velocity change. For each corresponding treadmill perturbation
timing (-100 ms -50 ms, 0 ms, +50 ms) and direction (+velocity, -velocity), the
cBF RMS value for the combined iKnee & Treadmill condition was compared to
the algebraic sum of the iKnee only and Treadmill only conditions. Background
activity (normal gait cBF RMS value) was subtracted from these trials before
comparison.
Functionality of the Contralateral Biceps Femoris Reflex Response 769

Fig. 1 Mean data from one participant for either normal gait (black lines) or following
ipsilateral knee extension joint rotations (grey lines) during the late stance phase (0%) of
the gait cycle (0-100%). (A) Ipsilateral knee angle; (B) mean rectified ipsilateral biceps
femoris electromyography (EMG); (C) contralateral knee angle; and (D) mean rectified
cBF EMG. Perturbation onset is represented by the vertical dashed line. The upward
pointing arrows below (D) represent the onset of treadmill velocity changes relative to
perturbation onset (-100, -50, 0 and +50 ms). Note the period of facilitation in the cBF
EMG following iKnee only trials, beginning about 73 ms after perturbation onset.

3 Results

The cBF reflex response was observed in all participants following ipsilateral knee
extension joint rotations applied at 50% of the gait cycle, with a mean onset
latency of 80 ± 11 ms. Mean data from one representative participant are shown in
Fig. 1 (30 normal gait steps and 30 iKnee perturbation steps).

3.1 Effects of Sudden Changes in Treadmill Velocity on the cBF


Reflex Response
Results from the same participant as in Fig. 1 are shown in Fig. 2 (sudden
increases in treadmill velocity) and Fig. 3 (sudden decreases in treadmill velocity).
The RMS window for this participant was between 73 and 120 ms following
iKnee perturbation onset. When the treadmill velocity was suddenly increased 100
ms and 50 ms prior to the onset of the iKnee perturbation, the combined iKnee &
Treadmill condition resulted in larger cBF reflex responses than the algebraic sum
770 A.J.T. Stevenson et al.

of the iKnee only and treadmill only conditions (Fig. 2A and 2B). Conversely,
when the treadmill velocity was suddenly decreased 100 ms and 50 ms prior to the
onset of the iKnee perturbation, the combined iKnee & Treadmill condition
resulted in smaller cBF reflex responses than the algebraic sum of the iKnee only
and treadmill only conditions (Fig. 3A and 3B). When the sudden changes in
treadmill velocity (+velocity or –velocity) occurred at the same time or 50 ms
after the onset of the iKnee perturbation, the cBF reflex response of the combined
iKnee & Treadmill condition was the same size as the algebraic sum of the iKnee
only and treadmill only trials (Fig. 2C, 2D, 3C, and 3D).
Fig. 4 shows the mean data across all participants for the combined conditions
when the sudden treadmill velocity changes occurred 100 ms, 50 ms, at (0 ms), or
50 ms after the onset of the iKnee perturbation. Due to the low sample size in this
pilot study, no attempt at statistical comparisons was made on these data.

Fig. 2 Mean rectified cBF EMG for one participant depicting either the combined iKnee
perturbation and treadmill velocity change condition (grey lines), or the summation of the
iKnee perturbation only and treadmill velocity change only conditions (black lines)
following sudden increases in treadmill velocity at -100 ms (A), -50 ms (B), 0 ms (C) and
+50 ms (D) relative to iKnee perturbation onset (vertical dashed line). The onset of the
treadmill velocity increase is represented by the black arrows. The participant is the same as
in Fig. 1. Note the extra facilitation of the cBF reflex in (A) and (B).
Functionality of the Contralateral Biceps Femoris Reflex Response 771

Fig. 3 Mean rectified cBF EMG for one participant depicting either the combined iKnee
perturbation and treadmill velocity change condition (grey lines), or the summation of the
iKnee perturbation only and treadmill velocity change only conditions (black lines)
following sudden decreases in treadmill velocity at -100 ms (A), -50 ms (B), 0 ms (C) and
+50 ms (D) relative to iKnee perturbation onset (vertical dashed line). The onset of the
treadmill velocity decrease is represented by the black arrows. The participant is the same
as in Fig. 1 and Fig. 2. Note the inhibition of the cBF reflex in (A) and (B).

However, when the sudden treadmill velocity changes occurred 100 ms or 50 ms


prior to iKnee perturbation onset, the cBF reflex response was either facilitated
(increase in treadmill velocity) or inhibited (decrease in treadmill velocity)
compared with the algebraic sum of the iKnee only and treadmill only conditions,
while no such effect was observed when the sudden treadmill velocity changes
occurred at the same time or 50 ms after iKnee perturbation onset.

4 Discussion

We examined the functionality of the cBF reflex response following ipsilateral


knee extension joint rotations during the last stance phase (50%) of the gait cycle.
In the six participants investigated, we observed a decrease in the initial cBF
772 A.J.T. Stevenson et al.

Fig. 4 Mean amplitude of the initial reflex component of the cBF response following a
combination of iKnee perturbations delivered at 50% of the gait cycle, and sudden changes
in treadmill velocity at four different timings relative to iKnee perturbation onset. Data are
expressed as a percentage of the algebraic sum of the iKnee perturbation only and sudden
treadmill velocity change conditions. The horizontal dashed line represents 100%. Filled
circles represent sudden increases in treadmill velocity, while open circles represent sudden
decreases in treadmill velocity. Error bars represent standard error.

reflex amplitude when the treadmill velocity was suddenly decreased 100 ms and
50 ms prior to the onset of the iKnee perturbation. Conversely, we observed an
increase in the initial cBF reflex amplitude when the treadmill velocity was
suddenly increased 100 ms and 50 ms prior to the onset of the iKnee perturbation.
The main results are consistent with the proposal by Stevenson et al. [1] that the
cBF reflex response may be a preparation of the contralateral leg for early load
bearing, slowing the forward progression of the body in order to maintain dynamic
equilibrium during walking. When the walking surface was slowed, the cBF reflex
did not need to be as large in amplitude because there was less breaking of the
body’s forward progression required. When the walking surface was sped up,
more breaking of the body’s forward progression was required, thus requiring a
larger cBF reflex.
Because the cBF reflex response has been shown to be mediated by a
transcortical pathway, it may allow for more adaptable responses than purely
spinally mediated reflexes due to integration with other sensory input at a cortical
level, such as afferent information arising from the contralateral leg [8, 9].
However, there must be sufficient time for this sensory integration to occur. When
the treadmill velocity was suddenly altered at the same time as, or 50 ms after, the
iKnee perturbation onset the cBF response was unchanged.

5 Conclusion

In conclusion, these preliminary results strongly suggest a functional role for the
cBF reflex response. A greater knowledge of the functionality of such interlimb
reflexes is important in understanding the neural control of human walking,
Functionality of the Contralateral Biceps Femoris Reflex Response 773

particularly from a rehabilitation perspective. In addition to investigating more


participants, we are also currently investigating how responses in other
contralateral leg muscles are influenced by the unstable walking environment
created by the multiple unexpected changes to the velocity of the treadmill given
that intra- and interlimb reflexes are modulated by the level of postural threat
during walking [10, 11].

Acknowledgments. This study was supported by grants from Det Obelske Familiefond and
SparNord Fonden. We also thank L. C. Aarestrup, A. L. N. Hansen, L. S. Hansen, A. Skou,
A. T. Thanning, and K. Thorsteinsson for assistance with data collection, and K. Larsen for
programming assistance.

References
[1] Stevenson, A.J.T., Geertsen, S.S., Andersen, J.B., Sinkjær, T., Nielsen, J.B.,
Mrachacz-Kersting, N.: Interlimb communication to the knee flexors during walking
in humans. J. Physiol. 591, 4921–4935 (2013)
[2] Stubbs, P.W., Nielsen, J.F., Sinkjær, T., Mrachacz-Kersting, N.: Phase modulation of
the short-latency crossed spinal response in the human soleus muscle. J.
Neurophysiol. 105, 503–511 (2011)
[3] Zehr, E.P., Collins, D.F., Chua, R.: Human interlimb reflexes evoked by electrical
stimulation of cutaneous nerves innervating the hand and foot. Exp. Brain Res. 140,
495–504 (2001)
[4] van der Linden, M.H., Marigold, D.S., Gabreels, F.J., Duysens, J.: Muscle reflexes
and synergies triggered by an unexpected support surface height during walking. J.
Neurophysiol. 97, 3639–3650 (2007)
[5] Andersen, J.B., Sinkjær, T.: Mobile ankle and knee perturbator. IEEE Trans. Biomed.
Eng. 50, 1208–1211 (2003)
[6] Mrachacz-Kersting, N., Grey, M.J., Sinkjær, T.: Evidence for a supraspinal
contribution to the human quadriceps long-latency stretch reflex. Exp. Brain Res. 168,
529–540 (2006)
[7] Mrachacz-Kersting, N., Lavoie, B.A., Andersen, J.B., Sinkjær, T.: Characterisation of
the quadriceps stretch reflex during the transition from swing to stance phase of
human walking. Exp. Brain Res. 159, 108–122 (2004)
[8] Christensen, L.O., Andersen, J.B., Sinkjaer, T., Nielsen, J.: Transcranial magnetic
stimulation and stretch reflexes in the tibialis anterior muscle during human walking.
J. Physiol. 531, 545–557 (2001)
[9] Zuur, A.T., Christensen, M.S., Sinkjær, T., Grey, M.J., Nielsen, J.B.: Tibialis anterior
stretch reflex in early stance is suppressed by repetitive transcranial magnetic
stimulation. J. Physiol. 587, 1669–1676 (2009)
[10] Haridas, C., Zehr, E.P., Misiaszek, J.E.: Context-dependent modulation of interlimb
cutaneous reflexes in arm muscles as a function of stability threat during walking. J.
Neurophysiol. 96, 3096–3103 (2006)
[11] Haridas, C., Zehr, E.P., Misiaszek, J.E.: Postural uncertainty leads to dynamic control
of cutaneous reflexes from the foot during human walking. Brain Res. 1062, 48–62
(2005)
Rehabilitation Following Targeted Muscle
Reinnervation in Amputees

Agnes Sturma1, Malvina Herceg3, Birgit Bischof4,


Veronika Fialka-Moser3, and Oskar C. Aszmann1,2
1
Christian Doppler Laboratory for Bionic Reconstruction at the
Medical University of Vienna, 1090 Vienna, Austria
{agnes.sturma,oskar.aszmann}@meduniwien.ac.at
2
Division of Plastic Surgery, Department of Surgery at the
Medical University of Vienna, 1090 Vienna, Austria
3
Department of Physical and Rehabilitation Medicine at the
Medical University of Vienna, 1090 Vienna, Austria
{malvina.herceg,veronika.fialka-moser}@meduniwien.ac.at
4
Otto Bock Health Care Products GmbH, 1070 Vienna, Austria
birgit.bischof@ottobock.com

Abstract. Targeted Muscle Reinnervation (TMR) provides an opportunity to


improve prosthesis control for patients with high upper limb amputations. During
surgery, nerves of the arm are rerouted to muscles of the stump region thus
yielding additional myo-signals which can be used to control prosthesis more
intuitively. This study reveals a new protocol for successful prosthetic training of
these patients, the so-called “TechNeuroRehabiliation”. It is initiated after surgery
and takes about 1.5 years, depending on the level of amputation. During this time,
the patient has to learn how to control his new neuro-muscular interface. This
rehabilitation process can be divided into 4 stages: 1) reinnervation i.e. wound
healing following surgery; 2) signal training: the patient has to learn to control and
separate signals; 3) prosthetic fitting if the patient can already reliably control
sufficient signals; and 4) follow ups and further training. In this process stage 2
requires maximum therapeutic effort and is highly cognitive. After finishing stage
3, the patient should be capable of using the prosthesis in daily life.

Keywords: selective nerve transfer, upper limb amputation, prosthetic training.

1 Introduction

Basic myoelectric prostheses for upper limb amputees are usually operated by
using two myosignals generated from muscles via surface electrodes. Although this
allows a fairly good prosthetic function, it is still limited to few degrees of freedom
(in high amputations at least movements of the elbow, the wrist and the hand are
required), in speed of combined movements and does not allow intuitive control
over the device. In the past few years new possibilities have been found to improve

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 775
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_107, © Springer International Publishing Switzerland 2014
776 A. Sturma et al.

prosthetic control. A special kind of selective nerve transfer ‘Targeted Muscle


Reinnervation’ (TMR) provides the amputee with up to six signals for intuitive
prosthetic control. In surgery, the residual nerves from the amputated limb are
transferred onto alternative muscle groups that are not functional anymore since
they are no longer attached to the missing arm. [1]
After nerve regeneration and a long-lasting phase of motor learning the
reinnervated muscles serve as biological amplifiers for the motor command to the
prosthetic arm. TMR thus provides physiologically appropriate EMG control
signals that are related to previous functions of the lost arm.
After surgery and nerve healing, the patients have to discover a new
neuromuscular interface and have to learn how to control their prostheses. This
requires complex motor learning. Because of this a long term rehabilitation
program is needed. This so-called ‘TechNeuroRehabilitation’ procedure takes
about 1.5 years depending on the level of amputation. [2-3]

Fig. 1 Example for nerve transfers in a glenohumeral amputee

2 Methods
The presented rehabilitation protocol was developed based on literature research
and clinical experience of the Christian Doppler Laboratory for Bionic
Reconstruction, Medical University of Vienna and of Otto Bock Health Care
Products GmbH. The Christian Doppler Laboratory was founded in January 2012
and since then 10 TMR surgeries (5 glenohumeral, 1 bilateral and 4 transhumeral
amputees) were performed. Experts of the multidisciplinary team which takes care
of the patient (surgeons, PMR specialists, therapists, technicians,...) were involved
Rehabilitation Following Targeted Muscle Reinnervation in Amputees 777

in developing the rehabilitation program described below. It aims to guide the


rehabilitation team through the process, but cannot cover the precise content of the
training sessions.

3 Results

The TechNeuroRehabilitation is a long-term process and requires both a motivated


patient and a multidisciplinary center with dedicated and skilled team members.
Within the rehabiliation process a few milestones need to be achieved. This
includes the reinnervation of the muscles after surgery, gaining the ability to
selectively activate the reinnervated muscles and the prosthetic fitting. On the basis
of those milestones the TechNeuroRehabiliation can be divided into the following
stages:

3.1 Stage 1: Regeneration (0-3 Months after Surgery)


After surgery and wound healing it takes about 3 to 6 months until the transferred
nerves reach their targets and the first contractions can be registered either by
surface or needle electrodes. During this time it is important for cortical
representation and stimulation to start facilitating the reinnervation process by
motor imagery. This means that the patient should think of different movements of
the non-existing arm/hand[4-5]. They are selected depending on the transferred
nerves and the movements they are usually responsible for. Also bilaterally gross
movement patterns can be used for facilitating first motor activity.
Another focus lies on pain and oedema control as well as on trunk stability and
body symmetry. Furthermore attention is paid on restoration of range of motion of
the existing joints. [6]

3.2 Stage 2: Signal Training (About 3-15 Months after Surgery)


As soon as the first EMG signals can be recorded the aim of rehabilitation is the
improvement of neuromuscular control. [7] Movement patterns according to the
ones typical for the transferred nerves are then being tested and trained to find
the movements which elicit the most powerful and best separated signals. Since the
precise control of the signals is of utmost importance for later prosthetic use,
additional attention should be paid on this stage. To support the patient in learning
how to activate the new reinnervated muscles, the use of EMG-biofeedback is
advised. Using this tool, activation of one single muscle without another and the
application of different contraction forces are trained.
As soon as the signals can be controlled fairly well using EMG-biofeedback, a
training with a prosthesis mounted on a desk is recommended. Thus the patient can
learn how to control the different movements of a real prosthesis.
778 A. Sturma et al.

3.3 Stage 3: Prosthetic Fitting (About 12-18 Months after


Surgery)
Once the signals are well established the final prosthesis can be fitted. Up to 6
electrodes have to be embedded in the socket. Thus an experienced prosthetist is
needed. For defining the final positions of the electrodes the collaboration of
surgeons, PMR specialists, therapists, technicians and prosthetists is recommended.
After fitting, the control of the prosthesis needs to be trained again. We recommend
starting with prosthetic movements without objects and then going on doing easy
grasp/release tasks with different objects. [3] In the end activities of daily living
should be trained. Finally, the patient receives the prosthesis to use it in daily life.

3.4 Stage 4: Follow-Ups (6, 12 and 24 Months after Final


Fitting)
While using the prosthesis at home, some problems may occur or changes in the
stump may lead to the necessity of socket changes. Since the muscle reinnervation
can continue after final fitting also the optimal electrode positions can change over
time. Thus it is very important to stay in contact with the patients after final fitting
and regularly assess their function, pain and quality of life. An assessment of these
areas before TMR surgery, during TechNeuroRehabilitation and frequently after
the prosthetic fitting ensures constant monitoring of our patients' progress as well
as a quality check of our efforts.

4 Conclusion

The presented process is a summary of literature reviews and clinical experience.


It is under evaluation by using several outcome measures to get a proof of
concept. Priliminary results show an increase in prosthetic function due to TMR
and the TechNeuroRehabilitation. Furthermore, it seems to be associated with a
reduction of phantom limb pain.
With advances in technology (as virtual reality training systems) or changes in
the surgical procedure (as using implanted electrodes) also the rehabilitation
process needs to be adapted. We hope to improve the therapeutic outcome
(especially for patients from abroad) with our recommendations for interventions
after targeted muscle reinnervation.

Acknowledgment. The scientific work of the Christian Doppler Laboratory for Bionic
Reconstruction is sponsored by the Christian Doppler Gesellschaft, Boltzmanngasse 20,
1090 Vienna, Austria.
A.S. thanks Michael Krutzler and Esther Baliko for their support.
Rehabilitation Following Targeted Muscle Reinnervation in Amputees 779

References
[1] Kuiken, T.A., Dumanian, G.A., Lipschutz, R.D., Miller, L.A., Stubblefield, K.A.: The
use of targeted muscle reinnervation for improved myoelectric prosthesis control in a
bilateral shoulder disarticulation amputee. Prosthet. Orthot. Int. 28(3), 245–253 (2004)
[2] Aszmann, O.C., Dietl, H., Frey, M.: Selective nerve transfers to improve the control of
myoelectrical arm prostheses. Handchir. Mikrochir. Plast. Chir. 40(1), 60–65 (2008)
[3] Stubblefield, K.A., Miller, L.A., Lipschutz, R.D., Kuiken, T.A.: Occupational therapy
protocol for amputees with targeted muscle reinnervation. J. Rehabil. Res. Dev. 46(4),
481–488 (2009)
[4] Dickstein, R., Deutsch, J.E.: Motor Imagery in Physical Therapist Practice. Physical
Therapy 7, 942–953 (2007)
[5] Jackson, P.L., Lafleur, M.F., Malouin, F., Richards, C., Doyon, J.: Potential role of
mental practice using motor imagery in neurologic rehabilitation. Arch. Phy. Med.
Rehabil. 8, 1133–1141 (2001)
[6] Esquenazi, A., Mayer, R.H.: Rehabilitation in Limb deficiency.4. Limb Amputation.
Arch. Phy. Med. Rehabil. 77, 18–28 (1996)
[7] Novak, C.: Rehabilitation Following Motor Nerve Transfers. Hand Clin. 24, 417–423
(2008)
Centre of Pressure Assessment in Subjects with
Incomplete Spinal Cord Injury: Preliminary
Data of Reliability, Validity and Effectiveness

Federica Tamburella1, Giorgio Scivoletto2, Marco Iosa3, and Marco Molinari2


1
Spinal Cord Unit - IRCCS S. Lucia Foundation
via Ardeatina 306 - 00179 Rome, Italy
{f.tamburella,m.iosa}@hsantalucia.it
2
Clinical Movement Analysis and Research Laboratory - Spinal Cord Unit,
IRCCS Santa Lucia Foundation, Rome, Italy
3
Clinical Laboratory of Experimental Neurorehabilitation
Fondazione Santa Lucia I.R.C.C.S.
{g.scivoletto,m.molinari}@hsantalucia.it

Abstract. Impairments in balance are highly predictive of functional recovery in


patients with spinal cord injury (SCI) and thus merit evaluation. An objective
balance evaluation can be implemented by analyzing center of pressure (COP)
parameters using stabilometric platforms (SPs). Specifically, concerning subjects
with SCI, no studies addressed reliability, validity, or responsiveness of this
measure. The objective of the serial cross-sectional study was to analyze the
reliability, validity, and responsiveness of COP parameters under various
conditions in 23 incomplete SCI subjects, examined 111 times for 1 year. Each
session comprised: Berg Balance scale, Tinetti and WISCI scale, stabilometry
performed under various sensory conditions (open and closed feet (OF – CF);
open and closed eyes (OE – CE). COP parameters analyzed (L: path length; V:
velocity, VAP and VLL: anteroposterior and laterolateral velocity, A: ellipse area,
SA1 and SA2: x and y-axis of A). V and arithmetically related measures had the
highest reliability, validity, and effectiveness scores. Of all test conditions, OE-OF
was the most valid, whereas CE-OF was the most responsive. The assessment of
balance in SCI subjects can be reliable, valid, and effective on acquisition of V
data, based on OF-OE and OF-CE conditions and heel distance values.

1 Introduction
Balance is usually defined as preservation of the vertical projection of the body’s
center of mass (COM) onto the support area that is formed by the feet [1]. Human
balance is typically modeled as an inverted pendulum, in which the body is
controlled as a single rigid segment that supports a single mass point—the
COM—which rotates around the ankle joint. The inverted pendulum is regulated
through the development of ground-reaction forces, the vector sum of which is
applied to a point that is defined as the center of pressure (COP) [2].

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 781
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_108, © Springer International Publishing Switzerland 2014
782 F. Tamburella et al.

The body’s equilibrium is maintained by the central nervous system, which


fixes the COM around a specific point—a goal that is under constant challenge by
continuous perturbations to the COM by factors, such as breathing, heart rate, and
muscle activity [3]. Postural sway, such as spontaneous shifts in the COP during
quiet standing, represents the integrated output of complex interactions between
systems [4]. Many systems contributing to postural control have been identified.
The postural control system depends on the unimpaired ability to correctly
perceive the environment through peripheral sensory systems, as well as to
process and integrate vestibular, visual and proprioceptive inputs at the central
nervous system (CNS) level [4].
Of the postural control systems, the spinal centers have a significant function,
explaining the clinical relevance of postural control deficits in SCI [5;6].
Despite the availability of many technical instruments to assess balance, the
most common clinical tools remain observational scales, such as the Tinetti and
Berg balance scales. Nevertheless, these scales are hampered by a lack of
sensitivity and objectivity and limited by floor-ceiling effects [7;8].
To overcome these drawbacks, stabilometric platforms (SPs), consisting of a
rigid plate that is supported by force transducers, and COP analyses have been
introduced in clinical settings [4]. Only two recent studies assessed balance in
SCI, examining the recovery after visual biofeedback rehabilitation by COP
analysis [5;6]. Impaired balance is a significant limitation to overground
ambulation in patients with SCI [8], and impairments in balance are predictive of
gait recovery [9], thus meriting evaluation [6].
Despite the growing interest in balance, the standardization of COP parameters,
with regard to measurements and the related quality domains [10;11] (ie,
reliability, validity, and responsiveness) [12] is poor [13] and is absent from the
SCI population. COP measurements have been examined in healthy elderly
individuals [4;14] and in patients with Parkinson [15] and orthopedic diseases
[16]. Data from healthy subjects can inflate the reliability estimates, because
measurements can be made in them more easily than in patients [4].
Measurement errors, and hence the reliability of a measure, are not fixed but
depend on the study population [17] and can vary by test conditions [4]. Thus,
measurement properties must be specified for the study population and test
conditions.
No study has examined the properties of COP parameters by SP in subjects
with SCI. Our serial cross-sectional study aimed to determine the reliability,
validity, and responsiveness of COP parameters under various test conditions and
define the protocol parameters that are suitable for specifically assessing balance
in subjects with incomplete motor SCI.

2 Methods
2.1 Population
This serial cross-sectional study included 23 subjects with incomplete motor SCI.
The inclusion criteria comprise traumatic and nontraumatic etiology, subacute and
Centre of Pressure Assessment in Subjects with Incomplete Spinal Cord Injury 783

chronic AIS D motor incomplete SCI lesions, and the ability to maintain a standing
position unsupported for at least 52 s. The exclusion criteria were the presence of
cognitive impairments and any orthopedic or neurological pathology that could
influence the assessment of balance. Neurological status was scored per American
Spinal Injury Association (ASIA) standards, including the Impairment Scale (AIS)
[18].

2.2 Balance Assessment


Enrolled patients were assessed repeatedly. In particular, 6 patients were assessed 1
time, and the remaining 17 patients were assessed 2 to 12 times for 1 year, with 2
weeks between sessions. Overall, 111 evaluation sessions were analyzed, all of
which employed clinical and instrument-based assessments of balance. The local
ethics committee approved this study.
Clinical assessment of balance: For each evaluation, the Berg Balance scale
(BBS) and Tinetti scale (TS) were used to assess balance clinically, and the
Walking Index for Spinal Cord Injury (WISCI) [19] was used to determine the
functional level of ambulation.
Instrument-based stabilometric assessment of balance: Stabilometric parameters
were analyzed using a 320-cm by 75-cm (length x width) static force platform
(Platform BPM 120, Physical Support Italia, Italy). The signals were amplified and
acquired using dedicated software (Physical gait Software Vv. 2.66, Physical
Support Italia, Italy). In assessing static stability, patients stood barefoot in a
natural and relaxed position with their arms by their sides and with both heels lined
up [4], under 2 sensory conditions: eyes open (OE) and facing a target 1.5 m away,
and eyes closed (CE). The feet were placed with the forefoot open to 30 degrees
and the heels in 2 positions: together (FT) or apart at a comfortable distance (FA).
For the FA condition, heel distance (HD) was measured manually by the operator
and fixed for the FA-OE and FA-CE conditions during the recordings. For each
evaluation, 4 conditions (FT-OE, FT-CE, FA-OE, and FA-CE) were tested. Under
each condition, measures were recorded 3 times, per Ruhe [4], and the recording
time was 51.2 s., as indicated in the platform handbook. We considered the
following quantitative COP parameters:
- Length indicators: path length (L, mm), mean velocity (V, L divided by the
trial duration), anteroposterior (VAP) and laterolateral (VLL) velocities
(mm/s), mean position of COP along the planar laterolateral (X) and
anteroposterior (Y) coordinates on the platform (mm)
- Surface indicators: area of the ellipse encompassing 90% of COP samples (A,
cm2) and length of its semiaxes (SA1, SA2, cm).

2.3 Data Analysis


The influence of demographic features on COP parameters was analyzed using the
Pearson correlation coefficient, applied to data from the first session of each
subject.
784 F. Tamburella et al.

Measurement of COP parameters between test conditions, was assessed by


means of reliability, validity and responsiveness domains. The reliability domain
contains various measures for continuous data [10]: test-retest and intrarater
reliability. Test-retest reliability has been assessed by means of Coefficient of
Variation (CV), intrarater reliability by means of Intraclass Correlation Coefficient
– ICC. The validity domain refers to the degree to which an instrument measures
the construct that it purports to measure [10] and is evaluated, based on criterion
and construct validity. Validity has been investigated by means of correlation
coefficient between COP parameters and clinical scales. Responsiveness domain
reflects the sensitivity to changes and is frequently measured by effect size (ES)
[20]. ES was calculated for patients who participated in at least 2 sessions (17
patients) with regard to clinical and instrumental data.
The optimal sensory conditions for balance assessment were analyzed by
analysis of variance (ANOVA), with vision and support base as the main factors.
Further, Spearman correlation between HD and clinical scales was analyzed to
determine the influences of HD on balance in SCI subjects.
Statistical analyses were performed using SPSS for Windows (version 9.0,
Chicago, IL). Data were considered significant at p<0.05. Correlation analyses
were performed per Munro’s classification [17]: 0.00–0.25: little, if any correlation;
0.26–0.49: low correlation; 0.50–0.69: moderate correlation; 0.70–0.89: high
correlation; and 0.90–1.00: very high correlation.

Table 1 Results of mean (sd) values of CV, ICC and ES between conditions for each COP
parameter
COP Parameter CV ICC ES
A 45.7 (2.2) 0,79 (0,17) 1.60 (0.55)
L 13.4 (0.3) 0,87 (0,08) 2.16 (0.68)
SA1 25.3 (2.1) 0,83 (0,04) 1.63 (0.98)
SA2 26.7 (1.2) 0,68 (0,22) 1.48 (0.84)
V 13.4 (0.4) 0,87 (1,13) 2.16 (0.68)
VLL 13.4 (0.6) 0,88 (0,03) 2.29 (0,97)
VAP 15.8 (1.9) 0,79 (0,1) 2.36 (0.66)

3 Results

Not all subjects were tested under each sensory condition; subjects with more
severe damage were unable to perform the most challenging tasks; CF or CE
conditions. Overall, 111 OF-OE, 96 OF-CE, 83 CF-OE, and 73 CF-CE
evaluations were performed.
By Spearman correlation analysis, no significant correlations between COP
parameter and demographic features (age, height, weight, gender) were recorded
for any sensory condition (OE, CE, OF, CF). Of the COP parameters, V, VAP,
VLL and L had the highest reliability, validity, and effectiveness scores (Table 1
and Table 3). Of all test conditions, OE-OF was the most valid, whereas CE-OF
was the most responsive (Table 2 and Table 3).
Centre of Pressure Assessment in Subjects with Incomplete Spinal Cord Injury 785

Table 2 Results of mean (sd) values of CV, ICC and ES between COP parameters for each
sensory condition

Table 3 Validity of COP paramaters (p<0.05:*, p<0.005:**, p<0.001:***). The mean


values of absolute values of these coefficients between conditions are in last column.

Considering the data above, the effects of sensory conditions were examined,
focusing on V, the most sensitive, reliable, and valid COP parameter. Overall, feet
position had little effect on V, whereas vision affected V significantly. By ANOVA
of V values, with vision and support base as the main effects, only vision had a
significant effect [F(1.346)=76.10; vision: p<0.001, support base: p=0.535,
interaction not significant: p=0.445.]

4 Conclusion

Reliability, validity, and responsiveness are the key components of determining


the suitability of a measurement; these parameters can vary by characteristic of the
target population [17]. Our data allow us to define the COP parameters and
assessment conditions that are suitable in evaluating postural balance in subjects
with incomplete SCI. Overall, our findings implicate V as a valid parameter in
assessing balance in SCI subjects. The higher responsiveness was recorded for V
and the related L, VLL, and VAP measures. Furthermore taking into account the
V data, OF-OE is the most valid condition and OF-CE is the most responsive
condition, suggesting that both should be implemented in testing SCI subjects.
The comparison of reliability and responsiveness between the V value of COPs
in the OF-OE and OF-CE conditions and the balance scales merits further
786 F. Tamburella et al.

examination. Because BBS is the reference standard, the V results only


approximate the BBS ICC data. Yet, greater changes in V versus BBS in patient
balance are required to obtain improvements that are not due to instrument error.

Acknowledgment. This work was supported by the Italian Ministry of Health (RC08G), by
the European commission in the Seventh Framework Program ICT-2013- 611626
SYMBITRON.

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valid and reliable? Injury 42, 236–240 (2011)
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health status measures in the design of randomized and cluster-randomized trials.
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measures of postural stability in healthy older adults: effects of postural task difficulty
and cognitive load. Gait Posture 33, 651–655 (2011)
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injury and functional ankle instability. Gait Posture 29, 460–464 (2009)
[17] Domholdt, E.: Rehabilitation research: principles and applications. Elsevier Saunders,
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Classification of Spinal Cord Injury (rev), pp. 1–23. American Spinal Injury
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[19] Ditunno, P.L., Dittuno Jr., J.F.: Walking index for spinal cord injury (WISCI II): scale
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[20] Portney, L.G., Watkins, M.P.: Responsiveness to change. Foundations of Clinical
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Jersey, pp. 104–105 (2000)
A Functional Muscle Synergy for Forward
Reaching

Denise Taylor1 and J. Greg Anson2


1
Health & Rehabilitation Research Institute,
Auckland University of Technology, Auckland, New Zealand
denise.taylor@aut.ac.nz
2
University of Auckland, Auckland, New Zealand
g.anson@auckland.ac.nz

Abstract. There is increasing interest in the development of devices to assist


rehabilitation. Functional electrical stimulation has the capacity to enhance muscle
activation and timing during functional tasks. Identifying principal muscles may
assist developers in designing operating parameters of these devices. In this study
electromyography (EMG) and kinematic measures were taken from the affected
and unaffected arms of stroke patients and both arms of healthy age-matched
control participants. Three muscles (anterior deltoid, biceps and wrist extensors)
were identified as forming a functional muscle synergy and are nominated as
principal muscles for forward reaching. In control participants the three principal
muscles were active prior to the start of movement in all trials. Activation was
delayed in the affected arm of the participants with stroke. Facilitating appropriate
activation of the principal muscles for reaching may enhance outcomes for people
following stroke.

1 Introduction
Damage to the central nervous system (CNS) following stroke frequently results
in deficits in the ability of patients to make smooth and accurate reaching
movements of the contralateral limb. Recovery of arm function after stroke is
limited with few patients regaining useful function of the upper limb [1]. Reach to
grasp is a fundamental and frequently used movement of the upper limb
commonly focused on in rehabilitation. Successful reaches can be achieved using
a variety of joint angles and muscle actions due to large redundancy within the
system. There is increasing evidence that the brain controls this redundancy by
functionally coupling elements of the movement system and uses sets of muscle
synergies that have spatial and temporal coupling, to simplify the computational
demand on the system. [2,3,4,5,6] Some of this functional coupling occurs prior to
the onset of movement and is considered part of a pre-programmed, or pre-
planned response. [7] At a minimum, the initial 100ms of a movement is
considered to be under central control unaltered by feedback and inferred as
reflecting a centrally driven motor program. [7] Changes in movement related

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 789
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_109, © Springer International Publishing Switzerland 2014
790 D. Taylor and J.G. Anson

parameters following this initial early phase of the movement are likely to be
related to feedback mechanisms providing online correction, via visual or
proprioceptive feedback. Successful recovery of upper limb function requires the
stroke patient to relearn control over multiple joints and produce co-ordination
activity of muscles in appropriate synergistic sets and responds appropriately to
sensory feedback to correct movement parameters if necessary.
There are exciting developments in the area of brain computer interface devices
and electrical stimulation devices that can assist rehabilitation of reaching.
[8,9,10] One of the fundamental questions for developers working with electrical
stimulation in particular, is which muscles should be stimulated when assisting
reaching into forward space. Knowledge of muscle activity behavior during
forward reaching tasks in healthy individuals will be useful for engineers
developing systems aimed at rehabilitating or assisting reaching based movements
in people with CNS lesions.
The aim of the study was to identify the principal muscles used in forward
reaching tasks in normal control participants and to compare this to stroke
participants. It was assumed that if a muscle behaved as a principal element in a
reaching synergy it would be active on all reaches in the control group. We
hypothesized that there would be a clear functional synergy identified in control
participants but not in the affected arm of the stroke participants. We further
hypothesized that muscles that were consistently active prior to the start of the
movement would be a part of a pre-programmed motor plan. The Southern
Regional Health Authority Ethics Committee (New Zealand) granted ethics
approval.

2 Method

2.1 Participants and Measures


Stroke participants were recruited from a geriatric day hospital and a rehabilitation
center. Healthy control participants were recruited from posters displayed in the
hospitals and university precincts. All stroke participants had sustained a first ever
stroke at least 6 months prior to the study, demonstrated a unilateral motor
impairment of the upper limb and scored between 15 and 60 on the upper limb
section of the Fugl-Meyer Motor Assessment. [11] Participants were excluded in
they had a brainstem or cerebellar stroke, severe contracture of the hand, reduced
passive range of motion at the elbow, less than ¾ range of pain-free passive
supination at the radioulnar joint, or pain on passive movement of the shoulder.
The upper limb section of the Fugl-Meyer Motor Assessment was used to
measure motor performance and is scored out of 66. The modified Ashworth Scale
was used as an indicator of spasticity, with 1 indicating mild spasticity and 5
indicating severe spasticity. Muscle activity was recorded with electromyography
(EMG) using silver-silver chloride electrodes. The signals were sampled at
A Functional Muscle Synergy for Forward Reaching 791

1000Hz, pre-amplified and then relayed to Quantic EMG amplifiers and stored off-
line. Signals were smoothed using a 4th order Butterworth filter with a frequency
response between 10Hz and 5000Hz. A 50 Hz notch filter was used to reduce
electrical noise. EMG activity was recorded from trapezius, anterior, middle and
posterior deltoids, pectoralis major, triceps, biceps, and wrist extensor muscles. A
MotionAnalysisTM system was used to collect kinematic data at a frequency of
60Hz. Fifteen calibration and tracking adhesive markers were used to define the
trunk segment, the upper arm segment, forearm segment and mid hand location.

2.2 Experimental Design


A between groups, within participants repeated measures design was used. Each
participant completed 15 reaches into each of two directions with each arm. The
order of arm and task was randomized by coin toss prior to the participant arriving
at the laboratory. For each trial EMG and kinematic measurements were recorded.
Movement A required shoulder flexion with abduction and Movement B required
shoulder flexion with adduction. Participants were seated on a stool with their hand
on their lap and were asked to pick up a cup that was placed on a table at arms
length.
The start of movement was defined as the point at which the X-axis value of the
metacarpophalangeal marker exceeded 2 standard deviations of the resting baseline
value. The end of the movement was defined as the point at which the
metacarpophalangeal marker reached 100mm from the cup center. The onset of
muscle activity was defined as the point at which the signal exceeded 3 standard
deviations (the threshold level) above the resting baseline value for at least 20ms.
Muscle offset was the point at which the signal fell below the threshold level for at
least 50ms. To represent relative muscle activity patterns onsets and offsets were
normalized as a percentage of movement time.

3 Results
Ten stroke and 5 healthy control participants were recruited with a mean age of 64
(sd 11) years and 61 (sd 12) years respectively. There were 8 male and 2 female
participants in the stroke group, with 5 right-sided and 5 left-sided strokes. These
participants had a mean time since stroke of 17 months with a range of 6-39
months. The mean Fugl-Meyer Motor Assessment score was 30 (sd 10). Scores on
the modified Ashworth Scale ranged from 1-3 with 5 participants scoring 1. Data
from the right and left limbs of healthy control participants were pooled to create a
dataset of 10 control limbs.
Three muscles were identified as being principal muscles for the reaching task
and forming a consistent functional synergy. Anterior deltoid, biceps and wrist
extensors were active for all trials in the control dataset in both Movement A and
Movement B. This did not hold for the stroke participants with either arm (see
Table 1).
792 D. Taylor and J.G. Anson

In the control dataset the three principal muscles become active prior to the start
of movement and remain active throughout the movement. Trapezius also becomes
active prior to the start of movement but is not active on all trials.

Table 1 Identification of Principal Muscles


A) Movement A

Proportion of trials in which muscles were active


Muscle Contro Unaffa Affb
Trapezius 0.85 0.98 0.96
Anterior deltoid 1.00 1.00 0.96
Middle deltoid 0.92 1.00 1.00
Posterior deltoid 0.34 0.91 0.88
Pectoralis Major 0.70 0.71 0.59
Biceps 1.00 0.99 0.92
Triceps 0.69 0.83 0.60
Wrist extensors 1.00 1.00 0.82

B) Movement B

Proportion of trials in which muscles were active

Muscle Contro Unaffa Affb


Trapezius 0.90 0.89 0.89
Anterior deltoid 1.00 1.00 1.00
Middle deltoid 0.92 0.94 0.89
Posterior deltoid 0.19 0.54 0.75
Pectoralis Major 0.68 0.73 0.68
Biceps 1.00 1.00 0.99
Triceps 0.46 0.56 0.36
Wrist extensors 1.00 1.00 0.89
a b
Unaffected limb, Affected limb

Fig. 1 illustrates the timing and order of onset of the muscles in the control and
affected limb of the stroke participants. It can be seen that other muscles, such as
triceps, pectoralis major, posterior deltoid and middle deltoid are active after the
onset of muscle activity, but not in every trial, as is the case for the principal
muscles. This may indicate that these other muscles are active in response to
A Functional Muscle Synergy for Forward Reaching 793

feedback, either from visual or proprioceptive inputs, as error correction


mechanisms, thus accounting for the variability in onset frequency and timing.
The timing of onset of the three principal muscles prior to the start of
movement supports the premise that activation of the principal muscles represents,
at least part of, a pre-planned motor program for reaching in a forward direction.
For stroke participants when reaching with their affected arm there was a delay in
activation of many of the muscles and difficulty in consistently recruiting the most
distal of the muscles, the wrist extensors.

Fig. 1 Timing of muscle activity in Movement A

4 Conclusion

That the three principal muscles are active prior to the initiation of movement may
indicate that they are constituents of a pre-programmed muscle synergy for
forward reaching. When considering rehabilitation strategies for forward reaching
in people following stroke it would be valuable to consider the action of the
principal muscles for this task, both in terms of which muscles are
794 D. Taylor and J.G. Anson

active and their relative timing. This knowledge could be useful in the
development of functional electrical stimulation devices, ensuring appropriately
timed muscle contraction of the anterior deltoid, biceps and wrist extensor
muscles. There are some interesting complexities with biceps that need to be
considered. Biceps is a complex multi-joint muscle that is active eccentrically to
control the position of the forearm during forward reaching into free space.
Further research investigating the ability of functional electrical stimulation
devices to include activation of the three principal muscles is required.

References
[1] Langhorne, P., Coupar, F., Pollock, A.: Motor recovery after stroke: a systematic
review. Lancet Neurology 8, 741–754 (2009)
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A Brain-Machine Interface
Architecture to Control an Upper
Limb Rehabilitation Exoskeleton

Andrés Úbeda1 , Daniel Planelles1 , Enrique Hortal1 , Francisco Resquı́n2 ,


Aikaterini D. Koutsou2 , José Marı́a Azorı́n1, and José Luis Pons2
1
Brain-Machine Interface Lab, Miguel Hernández University of Elche,
Av. de la Universidad S/N, 03202, Elche, Spain
{aubeda,dplanelles,ehortal,jm.azorin}@umh.es
2
Bioengineering Group, National Research Council (CSIC),
Carretera Campo Real, km 0.200, 28500, Madrid, Spain
{aikaterini.koutsou,jose.pons}@csic.es, franresquin@gmail.com

Abstract. The combination of Brain-Machine Interfaces (BMIs) with as-


sistive technologies has seen a rapid development during the last few years.
Regarding post-stroke rehabilitation, the BMI could be combined with other
sensors to assist movements performed by the patient by attaching an ex-
oskeleton to the affected arm. To that end, the patient’s arm movement in-
tentions can be obtained by processing the brain information and generating
suitable output commands to control the exoskeleton kinematics. In this pa-
per, we propose an architecture that combines a Brain-Machine Interface
with an upper limb exoskeleton. Two different experimental setups based on
flexion/extension movements of the arm are proposed.

1 Introduction
Brain-Machine Interfaces (BMIs) are an alternative communication method
for people with a severe motor disability as they allow generating control
commands with the only help of the thoughts [1, 2]. Therefore, people with
motor disabilities, who can not control traditional devices like a mouse or a
keyboard, can interact with their environment. Non-invasive BMIs, although
having a lower spatial resolution, avoid the risks of surgical intervention and
have been used in all sorts of applications, such as the control of a robot arm
[3, 4] or to assist mobility by controlling a wheelchair [5, 6]. Alternatively,
BMIs are a very useful complement to motor rehabilitation procedures of
people that suffer movement limitations due to a cerebro-vascular accident
(CVA) or stroke. In those cases, the recovery of the arm movement is cru-
cial in order to perform activities of the daily life, so the assistance during
rehabilitation may be a key factor of improvement [7].
The combination of BMIs with assistive technologies has seen a rapid de-
velopment during the last few years. According to recent literature [8], a BMI

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 795
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_110,  c Springer International Publishing Switzerland 2014
796 A. Úbeda et al.

should be considered as an additional channel of the assistive system (hybrid


BMI), as it cannot manage all the assistive process alone. This means that
BMIs are usually combined with sensors and artificial intelligence to obtain
a proper control of the assistive device. Regarding post-stroke rehabilitation,
the BMI could be combined with other sensors to assist movements per-
formed by the patient by attaching an exoskeleton to the affected arm. To
that end, the patient’s arm movement intentions can be obtained by pro-
cessing the brain information and generating suitable output commands to
control the exoskeleton kinematics. This will serve as a reinforcement of the
rehabilitation process.
In this paper, we propose an architecture that combines a Brain-Machine
Interface with an upper limb exoskeleton. This architecture, whose main goal
is to act as a post-stroke rehabilitation tool, will be capable of decoding
movement intention and assist rehabilitation in patients who have a limited
mobility by completing arm movements or even carry out the whole move-
ment in those patients who suffer from a total loss of motor function. To
illustrate the applicability of the architecture, we show two different exper-
imental setups which take advantage of several BMI approaches to decode
movement intention.

2 Experimental Setup
The system architecture is composed of the Brain-Machine Interface that
commands the exoskeleton, the Inertial Measurement Units (IMUs) and the
Functional Electrical Stimulation (FES) that induces flexion/extension move-
ments (see fig.1).

2.1 Brain-Machine Interface


Brain signals are acquired using the commercial amplifier g.USBamp of the
g.Tec company with the g.GAMMAcap, which has active electrodes to reduce
signal/noise ratio. The acquisition of EEG signals is done using 16 electrodes
with a sampling frequency of 1200 Hz. The electrodes are placed over the scalp
with the following distribution: FC5, FC1, FC2, FC6, C3, Cz, C4, CP5, CP1,
CP2, CP6, P3, Pz, P4 , PO3 and PO4, according to the International System
10/10. This distribution has been chosen to cover all the relevant surface of
the scalp and, particularly, the regions were motor activity and Event-Related
Desyncronization (ERD) occurs. The EEG signals are internally band-pass
filtered between 0.5 and 100 Hz and a 50 Hz Notch filter is applied to remove
the power line interference.
A Brain-Machine Interface Architecture 797

Fig. 1 Experimental environment (top): the subject sits in front of a computer with
the exoskeleton attached to the right arm. Additionally, inertial measurement units
are used to measure the joint angles and functional electrical stimulation induces
flexion/extension arm movements. Inertial Measurement Unit (A). Inertial Mea-
surement HUB (B). Functional Electrical Stimulation Electrodes (C). Functional
Electrical Stimulation HUB (D).
798 A. Úbeda et al.

2.2 Upper Limb Exoskeleton: ARMEO Spring


The Armeo Spring1 is one of the most popular upper limb rehabilitation ex-
oskeletons commercialized by Hocoma. It consists of a passive orthosis (with-
out robotic actuators), with 6 degree-of-freedom (3 in the shoulder, 2 in the
elbow, 1 in the wrist). It has a spring mechanism to allow variable level of
gravity support, according to the patient capabilities. 3D arm segments po-
sitions can be determined by the in-build joints sensors position. The Armeo
has been used for rehabilitation after stroke [10, 9], spinal cord injury [11, 12],
and multiple sclerosis [13].

2.3 Functional Electrical Stimulation (FES)


Functional Electrical Stimulation(FES) is applied on biceps brachii and tri-
ceps brachii in order to obtain elbow flexion and extension respectively. The
FES system consists of the INTFES stimulator (Tecnalia S.L.) and tradi-
tional superficial electrodes (Axelgaard S.L.). The INTFES stimulator is an
one-channel constant current stimulator. INTFES stimulator in combination
with 4 demultiplexers can deliver asymmetric exponentially decreased bipha-
sic electric pulses of the same frequency and different pulse width and am-
plitude to up to 64 channels [14]. FES parameters are adjusted to 40 Hz of
stimulation frequency and 350 μs of pulse width. Pulse amplitude is adjusted
for each subject separately.

2.4 Inertial Measurement Units


An inertial sensors system is used in combination with the Armeo spring,
because it is not possible to obtain the direct joint angles from the Armeo
software. The capture of forearm movements is achieved by using two inertial
sensors (Technaid S.L). Two inertial sensors are needed in order to capture
the movement of the forearm in relation with the arm (elbow joint). There-
fore, one inertial sensor is placed on the posterior compartment of the forearm
next to the elbow and the other on the posterior compartment of the arm
next to the elbow. Both sensors are aligned regarding the same axis. Joint
angles are calculated based on Euler angles and using the orientation data of
the sensors. Orientation data are acquired through a HUB that is connected
to the PC USB port. Data acquisition frequency is 50Hz.

3 Proposed Experimental Procedures


Two experimental procedures have been designed based on flexion/
extension movements of the arm. The main goal is to control arm motion by
1
http://www.hocoma.com/products/armeo/armeospring/
A Brain-Machine Interface Architecture 799

executing, either volitive brain commands or detecting brain potentials re-


lated to movement onset. As a consequence, the first experimental setup
consists of controlling flexion/extension movements by performing volitive
commands generated from the classification of two motor imagery mental
tasks. On the other hand, the second experimental setup makes use of the
detection of actual movement intention before the flexion/extension is per-
formed. To that end, two different methodologies are proposed: the detection
of ERD events that indicate movement onset and the decoding of movement
intention from EEG low frequency components. Five healthy subjects will
perform the experiments.

3.1 Spontaneous BMI to Control Flexion/Extension


Movements
The spontaneous BMI is based on the classification of two mental tasks:
open/close left hand movements and recite the alphabet. These two output
commands are used to command flexion/extension movements through a hi-
erarchical menu displayed on a screen in front of the subject. The hierarchical
menu presents two options: rest and movement. The movement performed is
alternatively switched between flexion and extension depending on the cur-
rent state. The subject has the arm initially flexed. As a consequence, the first
menu to appear is the rest/extension menu. A cursor is moved left or right
by performing each of the mental tasks and the subject can easily select one
of the options in a minimum time of 7 seconds. When a flexion (or extension)
movement is selected it provokes the activation of FES and the arm moves
to the desire state. Each subject will perform a set of 4 training runs with a
visual feedback similar to the one shown in [15]. Afterwards, 4 real-time runs
will be performed to generate the flexion/extension movements.
The methodology followed to classify the EEG data has been previously
applied in [15]. First, the signal is band-pass filtered between 5 to 40 Hz.
Afterwards, a laplacian filter is applied over the 16 signals. This method is
used to enhance the signal quality. Lastly, an estimate of the spectral density
of the signal is applied using the periodogram [16]. The classifier is a Support
Vector Machine (SVM) with a (Radial Basis Function) RBF kernel. This kind
of kernel has 2 important parameters to configure: the regulation parameter
(C) and γ, which determines the size of the kernel. In this case, the values
are C=512 and γ=0,002.

3.2 Decoding Flexion/Extension Movements from


EEG Signals
The experimental procedure followed to decode movement intentions is based
on the measurement of EEG signals and elbow angles during the performance
of flexion/extension movements (Fig. 2). To that end, subjects will be asked
800 A. Úbeda et al.

Fig. 2 Joint measurements obtained from the IMUs. Elbow angles (top) and an-
gular velocities for the elbow (bottom).

to perform flexion and extension arm movements in runs of 2 minutes (ap-


proximately 10 flexion/extension movements per run). The complete session
will consist of a total number of 5 runs. The recorded data will be analyzed
to obtain the movement intention. To that end, we propose two alternatives:

3.2.1 Decoding Flexion/Extension Onset Using Event Related


Desynchronization (ERD)
To detect ERD potentials, EEG data are preprocessed and then classified.
The output of the classifier will be the current intention of the subject: rest
or flexion/extention onset. First, an 8th order Butterworth filter is applied
between 5 Hz and 40 Hz. Afterwards, a Laplacian filter is applied for all the
electrodes to smooth the signals. To extract the EEG features, the data are
processed with a Fast Fourier Transform (FFT) to know the spectral power.
The features are the sums of three frequency bands, 8-12 Hz, 13-24 Hz and 25-
30 Hz per each electrode which represents mu and beta bands, so 48 features
define the class. Finally, several classifiers will be tested to detect movement
onset such as Support Vector Machine SVM, K Nearest Neighbour (KNN),
Naive Bayes or Linear Discriminant Analysis (LDA).
A Brain-Machine Interface Architecture 801

3.2.2 Decoding Flexion/Extension Movements from EEG Low


Frequency Components
To decode the kinematics of the arm, a multidimensional linear regression
will be applied according to the formula (for further details refer [17]):


N 
L
x [t] = a + bnk Sn [t − k] (1)
n=1 k=0

Where x[t] is the kinematics state (elbow angle) at time t and Sn is the
voltage measured at electrode n. L are the number of lags and N the number
of channels. a and b, are the decoding parameters. Previously, EEG signals
and hand kinematics are filtered below 2 Hz (low frequency components) and,
afterwards, EEG data from each electrode is standardized by subtracting, for
each time sample (t), the mean (V̄ ) of the signal and dividing the result by
the standard deviation (SDV ).

4 Conclusion
In this paper, we propose an architecture that combines a Brain-Machine
Interface with an upper limb exoskeleton. Two different experimental se-
tups based on flexion/extension movements of the arm are proposed. The
first experimental setup consists of controlling flexion/extension movements
by performing volitive commands generated from the classification of two
motor imagery mental tasks. On the other hand, the second experimental
setup makes use of the detection of actual movement intention before the
flexion/extension is performed. This work contributes to existing knowledge
of neurorehabilitation robotics by providing a promising tool in future post-
stroke rehabilitation procedures. In the future, the recorded data will be stud-
ied by applying the different methodologies proposed. The main goal is to
obtain a reliable and fast instrument to decode arm movement intention and
will be eventually tested in patients that suffer from movement limitations
due to a stroke or paralysis.

Acknowledgment. This research has been funded by grant DPI2011-27022-C02-


01 and grant DPI2011-27022-C02-02 of Ministerio de Economı́a y Competitividad of
Spain as part of the project Brain2Motion, by Conselleria d’Educació, Cultura i Es-
port of Generalitat Valenciana of Spain through grant VALi+d ACIF/2012/135 and
through grant CSD2009-00067 (HYPER) of the Spanish CONSOLIDER-INGENIO
2010 Program.
802 A. Úbeda et al.

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learning control and 3D robotics reduces motor impairment in chronic stroke.
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arm orthosis used in spinal cord injury rehabilitation. Journal of Neuroengi-
neering and Rehabilitation 9(1), 1–8 (2012)
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A Brain-Machine Interface Architecture 803

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Transcranial Direct Current Stimulation
Enhances Propulsion during Walking

Edwin H.F. van Asseldonk

Department of Biomechanical Engineering,


MIRA, University of Twente, Enschede, The Netherlands
e.h.f.vanasseldonk@utwente.nl

Abstract. Transcranial direct current stimulation (tDCS) has been shown to


improve force generation and control in single leg joints in healthy subjects and
stroke survivors. However, it is unknown whether these effects also result in
improved force production and coordination during walking. Here we investigated
the effect of tDCS using different electrode configurations on the coordinated
motor output during walking. In a randomized double-blinded crossover design,
10 healthy subjects walked on an instrumented split-belt treadmill before and after
10 minutes of either uni-hemispheric (standard configuration), dual-hemispheric
(one electrode over each hemisphere) or sham primary motor cortex (M1) tDCS.
We found that tDCS enhanced the coordinated output during walking as reflected
in an increased propulsive impulse. Although increases were observed in both legs
only the increase in the leg contralateral to the hemisphere receiving anodal
stimulation was significant. These results show that tDCS can improve force
generation and coordination during walking. Future studies need to investigate
whether tDCS can improve the coordinated output of the paretic leg of stroke
survivors and in doing so its contribution to propulsion during walking.

1 Introduction

Transcranial direct current stimulation (tDCS) is a non-invasive, painless and easy


to apply cortical stimulation technique that modulates the excitability of the
corticospinal pathway from the cortex to the muscles (corticomotor excitability)
and may induce improved cortical plasticity [1-3]. Studies in chronic stroke
survivors have demonstrated that 10-20 minutes of anodal tDCS aimed at
upregulation of the excitability of the affected hemisphere results in a 10 %
improvement of motor tasks that mimic activities of daily living [4-6].
Hitherto, research on the clinical effectiveness has mainly addressed recovery of
motor function in the upper extremity. However, tDCS could also promote
corticomotor excitability and recovery in the lower limb. Its potential in the lower
extremities has recently been shown in healthy subjects and stroke survivors.
Anodal tDCS applied to the leg motor cortex resulted in an average increase of
corticomotor excitability of 30% [7] and increased pinch force generation in

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 805
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_111, © Springer International Publishing Switzerland 2014
806 E.H.F. van Asseldonk

healthy subjects [8]. For chronic stroke survivors anodal stimulation of the lesioned
hemisphere resulted in increased paretic knee extensor force generation [9] and
improved learning of a motor skill task with the paretic ankle [10]. All these studies
focused on changes occurring at the level of a single joint. We do not yet know
whether tDCS can also improve force generation and coordination between
different joints to improve walking.
One approach to further enhance the effects of tDCS is to optimize the electrode
configuration. The electrode configuration influences the electric field strength and
direction in the targeted area. In the standard protocols one electrode is placed over
the area of interest and the other over the forehead. Recent experimental studies
have demonstrated that effects are enhanced when placing one electrode over the
target area and the other electrode over the same area on the contralateral side, so
called dual-hemispheric stimulation. Modeling studies have shown that placing the
electrodes on opposite sides of the target area increases the target field strength
[11]. For stimulation of the leg area, placing electrode on opposite sides of the
target area would be similar to using a dual-hemispheric configuration.
The aim of this paper was to assess the effect of tDCS using different electrode
configurations on coordinated motor output during walking in healthy subjects. To
quantify the contribution of the coordinated output of the muscles to forward
propulsion, we used the anterioposterior ground reaction forces [12].

2 Methods

2.1 Subjects
Ten subjects participated in this double-blinded, crossover study. All participants
gave written informed consent. The study was approved by the medical ethical
research committee of the Medisch Spectrum Twente (Enschede, The Netherlands)
and conformed to the Declaration of Helsinki.

2.2 Design
Subjects participated in three experimental sessions separated by at least 1 week
and occurring around the same time of the day. In each session subjects received
tDCS with different configurations being uni-hemispheric (UNI), dual-hemipheric
(DUAL) or sham stimulation (SHAM). Each experiment consisted of a baseline
measurement (BASE) of treadmill walking, tDCS and two post measurements of
treadmill walking after approximately 20 (POST1) minutes and 50 minutes
(POST2).

2.3 Transcranial Direct Current Stimulation


Direct current stimulation was deliverd using a Magstim DC-Stimulator PLUS
through 2 saline-soaked sponge electrodes (5x7 cm). For UNI tDCS the anode was
Transcranial Direct Current Stimulation Enhances Propulsion during Walking 807

placed over the non-dominant hemisphere (contralateral to the non-dominant leg)


with the long edge of the rectangle aligned with the mid-sagittal fissure and the
cathode over contralateral supraorbital region. For DUAL tDCS the anode was
again placed over the non-dominant hemisphere but the electrode was shifted
laterally 1 cm, whereas the cathode was placed similarly over the contralateral
hemisphere. So the inter electrode distance was 2 cm and electrodes were
positioned on opposite sides of the target. For UNI and DUAL tDCS the motor
cortex was simulated for 10 minutes with 2 mA. For SHAM tDCS the electrode
configuration was randomly assigned to participant (either UNI or DUAL) and was
balanced across the subjects. For SHAM the current was ramped down after it was
being ramped up and held at 2 mA for 30 s.

2.4 Measurement of Ground Reaction Forces


In each of the sessions, subjects walked on an instrumented split-belt treadmill (Y-
mill, Forcelink, Culemborg, The Netherlands) during baseline and post
measurements for 3 minutes at 2.5 km/h (SLOW) and for 2 minutes at 5 km/h
(NORMAL). Each belt was equipped with force sensors that allowed measurement
of the 6 DoF ground reaction forces (GRF) and torques. These forces were sampled
with 1000 Hz and stored for offline analysis.

2.5 Data Analysis


As a measure for the coordinated motor output we calculated the total propulsive
and breaking impulse for every step from the anterioposterior GRF. First we used
the vertical ground reaction forces to detect heel strike and toe off and used these
gait events to split up the data in separate strides. Second we calculated the
propulsive impulse as the time integral for all positive anterioposterior GRF
(Impprop), see Fig. 1. For each trial we calculated an average value and expressed
this value as a fraction of the baseline value for that session.
From the detected gait events we also calculated the single stance duration and
the cycle time and also expressed these as fractions of the baseline values.

2.6 Statistics
To assess the effect of the applied tDCS we performed a linear mixed model
analysis with stimulation (UNI, DUAL, SHAM), speed (2.5 km/h and 5.0 km/h)
and time (POST1 and POST2) as fixed factors for each dependent variable. To
account for the correlation between the repeated measurements within a subject,
different intercepts were assumed for each subject by including the factor subject as
random factor into the analysis.
808 E.H.F. van Asseldonk

3 Results

DUAL and UNI tDCS resulted in longer stance duration and larger peaks in the
anterioposterior GRF for the representative subject depicted in Fig. 1. On a group
level, the propulsive impulse significantly increased in the non-dominant leg
(DUAL=1.042±0.014 [mean±SEM], UNI=1.029±0.014, SHAM=0.989±0.014,
F(2,99)=6.862 p<0.002) whereas it did not significantly increase for the dominant
leg (F(2,99)=1.581, p=0.211) (see Fig. 2 and Table 1). tDCS mainly influenced the
impulse for the slower walking speed as there was a significant SPEED x
SIMULATION interaction effect (F(2,99)=3.747, p=0.027) and post hoc analysis
turned out that there was no effect for walking at 5 km/h. For walking slowly UNI
and DUAL were both significantly different from SHAM (DUAL =1.070±0.017,
UNI=1.039±0.017, SHAM=0.976±0.017, DUAL vs SHAM: p<0.001, UNI vs
SHAM: p=0.010) but were not significantly different form each other (DUAL vs
UNI: p=0.454).
The increased propulsion was accompanied by a significantly increased stance
duration (DUAL =1.02±0.006, UNI=1.002±0.006, SHAM=1.000±0.006,
F(2,99)=7.176, p=0.001) and cycle time (DUAL =1.02±0.006, UNI=1.002±0.006,
SHAM=1.000±0.006, F(2,99)=7.295, p=0.001). As the walking speed was kept
constant, the latter result indicates that subjects made larger strides after they
received DUAL stimulation.

Table 1 Summary of statistical results

STIM STIM UNI vs UNI vs DUAL


x DUAL SHAM vs
SPEED SHAM
Non dominant p=0.002 p=0.027 p=1.000 p=0.027 p=0.002
Impprop
Dominant p=0.211 p=0.198
Imppropa
Non dominant p=0.001 p=0.181 p=0.008 p=1.000 p=0.003
stance duration
Dominant p=0.009 p=0.356 p=0.110 p=1.000 p=0.008
stance duration
Cycle time p=0.001 p=0.143 p=0.007 p=1.000 p=0.002
a
No post hoc tests were performed as there was no main effect of STIMULATION.
Transcranial Direct Current Stimulation Enhances Propulsion during Walking 809

e
in

t1

t2
el
s

s
Ba

Po

Po
UNI
DUAL
SHAM
2.5 km/h 5 km/h
80 150
propulsive
60
anterioposterior

40 impulse 100
force [N]

20 50
UNI

0 0
−20
−50
−40
−60 −100

80 150
60
anterioposterior

100
40
force [N]
DUAL

20 50
0 0
−20
−40 −50
−60 −100

80 150
60
anterioposterior

100
40
force [N]
SHAM

20 50
0 0
−20
−50
−40
−60 −100

0 0.2 0.4 0.6 0.8 1 0 0.2 0.4 0.6


Time [s] Time [s]

Fig. 1 Representative example of average anterioposterior ground reaction forces as a


function of time fot the non-dominant leg for a single subject
Non Dominant Dominant
2.5 km/h 5 km/h 2.5 km/h 5 km/h
propulsive
impulse

1.10
1.0 1 1 1 1

0.9
0.8
duration

1.10
stance

1.0 1 1 1 1

0.9
0.8
e

2
in

st

st
st

st
in
l
Po

Po

l
Po

Po
se

se
cycle time

Ba

Ba

1.10
1.0 1 1

0.9
DUAL
0.8 UNI
SHAM
e

t1

t2

t1

t2
lin

lin
s

s
Po

Po

Po

Po
se

se
Ba

Ba

Fig. 2 Group averages for the outcome variables expressed as fraction of the baseline values
for the different experimental conditions. Error bars indicate standard error of the mean.
810 E.H.F. van Asseldonk

4 Discussion and Conclusion

In this study we assessed the effect of tDCS using different electrode


configurations on the coordinated motor output during walking. We demonstrated
that tDCS increased the propulsive impulse for slow walking but not for walking at
normal speed. Effects were largest for dual-hemispheric stimulation but these
effects did not significantly differ from uni-hemispheric stimulation. Remarkably,
also in the leg ipsilateral (dominant leg) to the hemisphere receiving anodal tDCS
we observed facilitation of the motor output. This was even the case for the dual-
hemisperic stimulation, where the hemisphere contralateral to the dominant leg
actually received cathodal (down-regulating) stimulation. Here, based on the
opposite polarity of the stimulation of both hemispheres one would have expected
opposite sign modulation of the propulsive forces in the different legs.
The observed effects were modest and there was considerable variability
between subjects. For instance, for the condition that showed the largest
improvement (dual hemispheric stimulation and slow walking), 5 out of 10 showed
a marked increase of the propulsive impulse of more that 10%, 2 showed an
increase of approximately 5% and 3 subjects even showed a decrease of
approximately 5%. Similar variability in responses was observed for other
conditions. Other studies have also reported large variability in response to tDCS.
Madhavan and colleagues [13] showed that up-regulating stimulation resulted in
increased corticomotor excitability only in 60% of the cases and decreased in 18%.
These inter individual differences could be explained by individual differences in
the electrical properties of the superficial brain structures [13] and slight
differences in the placement
Previous studies did already show that tDCS can improve force generation and
control in single leg joints [8-10] We showed that it also facilitates multi-joint force
generation and coordination such that propulsion is increased. Therefore, tDCS has
potential to increase the impaired contribution of the paretic leg to propulsion in
stroke survivors [12]. Future studies need to investigate the effect of tDCS on the
paretic propulsion.

Acknowledgment. This study was supported by a VENI grant (grant nr: 91610143) from
The Netherlands Organisation for Scientic Research. The author wants to thank Stan
Verwer for his help in collecting the data.

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Design of a Subject-Specific EMG Model
for Rehabilitation Movement

Michele Vivian1 , Luca Tagliapietra1, Monica Reggiani1 ,


Dario Farina2 , and Massimo Sartori2
1 Department of Management and Engineering, University of Padua,
Stradella San Nicola 3, 36100 Vicenza, Italy
vivian@gest.unipd.it
2 Department of Neurorehabilitaion Engineering, University Medical Center Göttingen
Georg-August University, Von-Siebold-Str. 4, 37075 Göttingen, Germany

Abstract. In the latest years, robotics technologies have been increasingly intro-
duced in rehabilitation with the objective of cost reduction and speed up the re-
covery process. While with most of the devices the patient is passive, the current
challenge is to build devices able to understand patient’s intention and adapt ac-
cordingly, forcing his/her active involvement. A way to understand the patient is
to use EMG-driven neuromusculoskeletal model able to compute muscle dynamics
and joint torques from the electromyography (EMG) signals. While the approach
is quite promising, collecting EMG data is still not a simple task as placement of
electrodes requires professional skills and EMG data can be affected by electric and
magnetic noise.
This work proposes a model that builds upon a reduced experimental database
of EMG data from a common rehabilitation movement to develop the capability of
predicting EMG values for the same movement executed at arbitrary speed. The
reported experimental results are promising, showing a good accuracy in EMG
prediction thus enabling the possibility of their use as input for EMG-driven neu-
romusculoskeletal models. Model applicability, even if limited to repetitive move-
ments, can simplify the use of active rehabilitation devices and still keeping their
possibility to be driven by patient.

1 Introduction
Nowadays, an increasing number of people is affected by alteration in locomotions
due to population aging and neurological disorders or injuries, such as spinal cord
trauma and strokes [1, 2]. Rehabilitation treatments can restore functionalities but
their efficacy is often dependent on their personalization based on the anatomical,
physiological, and neurological characteristics of the patient [3, 4, 5]. Traditional
rehabilitation relies on therapists to personalize the treatment. Despite the effective-
ness of this approach, it has usually high cost depending on the required number of
therapists and sessions. Beside the cost, the achievable results and recovery time are
often highly dependent on the therapists skills.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 813
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_112,  c Springer International Publishing Switzerland 2014
814 M. Vivian et al.

In the latest years, robotics technologies have been increasingly introduced in


rehabilitation to assist the patient in the repetition of exercises with the objective of
decreasing the cost and speeding up the recovery process. Examples are automated
treadmill assisting the gait rehabilitation through pre-programmed gait patterns [6,
7] or orthoses that support over-ground locomotion with the objective of relearning
gait [8, 9, 10].
The current research challenge is to move from passive to active devices, able to
understand patient’s intention and adapt to the current state of the specific subject. A
promising approach is the use of electromyographic (EMG) signals to drive a neuro-
musculoskeletal model able to compute muscle dynamics and joint torques [11, 12].
Recent advancements could allow their use for real time estimation of joint mo-
ments and the control of a device [13] based on subject’s movement intention. EMG
signals also provide important information about metabolic energy consumption,
muscles activities and compliance in the muscles and joints. However, collection
of EMG data is still not a simple task as placement of electrodes requires profes-
sional skills and EMG data can be affected by electric and magnetic noise. It would
be much easier to skip the direct measurement and predict EMG values based on
other external observable variables and then use these predicted EMG data to drive
the neuromusculoskeletal model. Albeit this prediction would be usually impossi-
ble for the complex relation between muscle activations and resulting movement,
it could be instead feasible for the simpler, repetitive movements that are used in
rehabilitation treatments.
This paper presents a first effort to investigate the possibility to predict EMG val-
ues during plantar-dorsiflexion (P-DF) cyclic movements, often used to rehabilitate
a gait pathology known as drop foot [14]. Based on an experimental database of
EMG data collected when a subject performs P-DF movements at three different
speeds, an EMG model was developed to predict electromyographic data for P-DF
movements executed at arbitrary speeds. The presented results are a step in the di-
rection of investigating the accuracy and reliability of EMG prediction for its use
in driving neuromusculoskeletal models. Despite its applicability limited to repeti-
tive movements it would greatly simplify the use of rehabilitation devices and still
keeping their possibility to be driven by patient’s intention.

2 Methods

2.1 Participants
Five voluntary subjects (3 males and 2 females) participated in this experiment.
Their age was 26±1.22 years (mean pm STD), their body weight was 66±12.83 kg,
and their height was 1.7 ± 0.089 m. The participants had no neurological or muscu-
lar disorders that could influence their movements. Participants provided written
informed consent prior to participation.
Design of a Subject-Specific EMG Model for Rehabilitation Movement 815

(a) (b)

Fig. 1 Experimental Setup: (a) Markers and EMG electrodes placement (b) All the subjects
performed the P-DF movement sitting on a bar stool without any ground contact

2.2 Equipments and Set-Up


EMG signals were collected with a Wave wireless EMG system (Cometa srl, Milan,
Italy) at a sample rate of 2000 Hz from the following muscles: Gastrocnemius Lat-
eralis (GASL), Gastrocnemius Medialis (GASM), Soleus (SOL), Peroneus Longus
(PER), Tibialis Anterior (TIB). Bipolar electrodes sites were determined following
the SENIAM [15] recommendation.
Plantar-dorsiflexion movement of the ankle was recorded using an A1000-30fc
industrial camera (Basler, Ahrensburg, Germany) with a sample rate of 30 Hz. Cir-
cular markers were placed at three anatomical points: head of the fibula, tip of the
medial malleolus, and head of 5th metatarsus. A trigger signal was used to synchro-
nize the acquisitions from the two systems.
A picture of the set-up is shown in Figure 1.

2.3 Experimental Procedure


The entire procedure was carried out in an experiment room. Participants were asked
to sit comfortably on a bar stool with the feet not touching the floor. Before the
collection of the experimental data, they were shortly instructed on the procedure
and they practiced on plantar-dorsiflexion movements with the right leg already
instrumented.
Then, they were asked to perform plantar-dorsiflexion movements of the right
ankle for a total number of nine complete series, each one including at least three
P-DF movement. Subjects were instructed to repetitively span the whole range of
motion, starting at the maximum plantarflexion angle, reaching the maximum value
for dorsiflexion and then going back to the starting position.
816 M. Vivian et al.

In the first three series, each subject was asked to move slowly. Subsequently,
the test was repeated and the subject was asked to move at medium and then fast
speed. Tests were executed with a target cadence audio feedback (generated using a
miniature metronome) to allow a better control of the ankle movement minimizing
the effect of flexion-to-flexion variance within the same series. In the following we
will refer to the three cadence as: 1) Low Cadence (LC) with the metronome set
at 40 beats per minute (BPM), 2) Medium Cadence (MC), at 80 BPM, 3) High
Cadence (HC), at 120 BPM. At the same cadence, each subject was moving at a
different speed as each participant has a different range of motion. The collection of
the movement data at different cadences was aimed at obtaining an subject-specific
EMG model covering the whole wide variability of the ankle movement during
rehabilitation exercises.
Additional series of plantar-dorsiflexion ankle movements were performed to col-
lected data to validate the model. At least three additional series of movement for
each cadence (LC, MC, and HC) were collected. Finally, additional series of plantar-
dorsiflexion ankle movements were performed by each subject at a cadence between
medium and fast speed (100 BPM). This additional cadence (AC in the future sec-
tion) was used for the validation of the EMG model.

2.4 Data Processing


Raw EMG signals were processed by high-pass filtering, rectification, and low-pass
filtering [16]. The resulting EMG linear envelopes were then normalized. The max-
imum EMG peak for each muscle was identified extracting the maximum instanta-
neous value within all the recorded trials of the same subject.
Ankle angles were extracted using a C++ custom-software based on the OpenCV
library [17]. Ankle angles values were then used to estimate the ankle rotation speed
for each series and to automatically identify start and stop frame of each plantar-
dorsiflexion cycle.
Three consecutive P-DF cycles were automatically extracted from each series.
EMG data and ankle plantar-dorsiflexion of nine cycles for each LC, MC, HC were
used to build the model. The same data from three additional cycles for each cadence
(LC, MC, HC, and AC) during other acquisition sessions were used to validate the
model.

2.5 EMG Model


The objective of the proposed EMG model is to use only the plantar-dorsiflexion
mean speed to predict muscle EMG values during the cyclic ankle movement.
For each participant, a subject-specific EMG model was built based on the data
from the cycles at three different cadences (LC, MC, and HC). For each cadence and
muscle, an average EMG mean curve was first computed. Then, for each muscle, the
three curves at different cadences were time warped over 1000 samples, releasing
the speed dependance, to allow the computation of a single average curve.
Design of a Subject-Specific EMG Model for Rehabilitation Movement 817

Table 1 Mean value and standard deviation of R2 evaluated at cadences used to build the
model

GASL GASM PER SOL TIB


R2 ± ST D R2 ± ST D R2 ± ST D R2 ± ST D R2 ± ST D
S01 0.637 ± 0.238 0.770 ± 0.097 0.188 ± 0.127 0.667 ± 0.161 0.456 ± 0.430
S02 0.799 ± 0.141 0.754 ± 0.183 0.725 ± 0.235 0.795 ± 0.147 0.859 ± 0.074
S03 0.744 ± 0.135 0.770 ± 0.111 0.824 ± 0.095 0.625 ± 0.139 0.822 ± 0.149
S04 0.911 ± 0.054 0.823 ± 0.133 0.948 ± 0.026 0.902 ± 0.068 0.934 ± 0.044
S05 0.774 ± 0.196 0.801 ± 0.156 0.519 ± 0.276 0.808 ± 0.111 0.893 ± 0.076
Mean 0.773 ± 0.099 0.784 ± 0.028 0.641 ± 0.298 0.759 ± 0.112 0.793 ± 0.193

These curves, one for each muscle, can then be used to estimate EMGs at the
cadences required in the rehabilitation treatment. Starting from the time required to
execute a complete P-DF (input of the model), for each muscle the average EMG
curve previously computed is un-warped to match the current task speed thus gen-
erating a prediction of EMG signals.

2.6 EMG Model Validation


Fitting accuracy tests examined the ability of the EMG model to reproduce EMGs
collected from the subjects in validation trials, not used to build the model. Curves of
EMGs from the five muscles were further compared using the square of the Pearson
product moment correlation (R2 ) and the root mean squared error (RMSE).
The first test aimed at assessing the accuracy at the same cadence values (LC,
MC, and HC) used to collect EMG inputs to build the model.
The second test aimed at assessing the prediction accuracy for EMGs collected
from movements at a cadence (AC) not used to build the model.

3 Results
The first test evaluates the accuracy on the prediction of EMG values at the cadence
values used to train the model. For each subject, a set of nine cycles at LC, MC, or
HC were selected from acquisition sessions not used to build the EMG model.
Tables 1 and 2 show the obtained R2 and RMSE values of the normalized EMG
signals for the five participants. The overall R2 is equal to 0.750 showing that pre-
dicted curves are correlated with the experimental ones, and the average RMSE is
0.088 ± 0.022.
818 M. Vivian et al.

Table 2 Mean value and standard deviation of RMS error evaluated at cadences used to build
the model

GASL GASM PER SOL TIB


RMSE ± ST D RMSE ± ST D RMSE ± ST D RMSE ± ST D RMSE ± ST D
S01 0.040 ± 0.022 0.112 ± 0.051 0.121 ± 0.048 0.132 ± 0.034 0.164 ± 0.038
S02 0.067 ± 0.026 0.085 ± 0.036 0.122 ± 0.056 0.120 ± 0.045 0.091 ± 0.020
S03 0.064 ± 0.025 0.071 ± 0.025 0.082 ± 0.032 0.103 ± 0.038 0.100 ± 0.028
S04 0.043 ± 0.019 0.033 ± 0.012 0.063 ± 0.019 0.061 ± 0.022 0.065 ± 0.017
S05 0.105 ± 0.046 0.077 ± 0.032 0.081 ± 0.037 0.105 ± 0.044 0.090 ± 0.033
Mean 0.064 ± 0.026 0.076 ± 0.028 0.094 ± 0.026 0.104 ± 0.027 0.102 ± 0.037

Performance across the subjects are quite similar but for the subject S01 that
shows a reduced performance on Peroneous Longus and Tibialis Anterior that re-
quires further investigation. Performance across the different muscles shows also
good correlation and low average errors. The highest average error of Tibialis Ante-
rior can be motivated by its central role (and therefore high EMG values) in plantar-
dorsiflexion without ground contact. Model performance across the three cadence
values were also examined showing a higher accuracy at medium cadence (R2 = 0.8)
and a good accuracy for the worst cadence (LC) (R2 = 0.647).
The second test evaluated prediction of cycles at a cadence (AC) not used to build
the EMG curves of the model. Tables 3 and 4 reports, respectively, the correlation
coefficient R2 and the RMS errors obtained by the EMG Model estimation. Once
againg, R2 and RMSE values across all the participants and their muscles, allow to
assess the reliability and accuracy of the proposed EMG model. Results are quite
similar to the ones obtained with the previous test with poor results only shown by
two muscles of the subject S01 (possibly due to an incorrect placement of EMG
sensors).
Fig. 2 compares the estimated EMG behavior of each muscle with the measured
EMG signals averaged on the nine cycles at AC cadence. Plots refer to subject S04
but similar behavior are obtained with the other subjects.
Design of a Subject-Specific EMG Model for Rehabilitation Movement 819

Fig. 2 Comparison between estimated EMG signals and measured ones for each muscle
of subject S04 reported as a percentage of the P-DF cycle. Gray areas reports the ± STD
intervals of the reference.
820 M. Vivian et al.

Table 3 Mean value and standard deviation of R2 evaluated through all cycles recorded for
the additional cadence

GASL GASM PER SOL TIB


R2 ± ST D R2 ± ST D R2 ± ST D R2 ± ST D R2 ± ST D
S01 0.745 ± 0.269 0.851 ± 0.044 0.048 ± 0.024 0.807 ± 0.082 0.887 ± 0.036
S02 0.728 ± 0.214 0.693 ± 0.215 0.755 ± 0.181 0.762 ± 0.173 0.863 ± 0.057
S03 0.552 ± 0.199 0.623 ± 0.186 0.690 ± 0.157 0.519 ± 0.207 0.781 ± 0.105
S04 0.898 ± 0.056 0.897 ± 0.064 0.902 ± 0.056 0.907 ± 0.064 0.885 ± 0.046
S05 0.880 ± 0.040 0.854 ± 0.064 0.610 ± 0.164 0.897 ± 0.048 0.925 ± 0.037
Mean 0.760 ± 0.139 0.783 ± 0.119 0.601 ± 0.327 0.778 ± 0.157 0.868 ± 0.054

Table 4 Mean value and standard deviation of RMS error evaluated through all cycles
recorded for the additional cadence

GASL GASM PER SOL TIB


RMSE ± ST D RMSE ± ST D RMSE ± ST D RMSE ± ST D RMSE ± ST D
S01 0.037 ± 0.016 0.098 ± 0.033 0.100 ± 0.023 0.092 ± 0.017 0.171 ± 0.019
S02 0.064 ± 0.031 0.080 ± 0.032 0.114 ± 0.028 0.100 ± 0.030 0.089 ± 0.019
S03 0.061 ± 0.011 0.074 ± 0.016 0.071 ± 0.016 0.078 ± 0.016 0.091 ± 0.024
S04 0.044 ± 0.016 0.031 ± 0.015 0.085 ± 0.036 0.071 ± 0.021 0.074 ± 0.011
S05 0.086 ± 0.024 0.067 ± 0.015 0.082 ± 0.015 0.078 ± 0.031 0.078 ± 0.017
Mean 0.059 ± 0.019 0.070 ± 0.025 0.091 ± 0.017 0.084 ± 0.012 0.100 ± 0.040

4 Conclusions
This study presented a first implementation of a subject-specific model able to pre-
dict EMG signals of five muscles during the plantar-dorsiflexion ankle movement,
often used in rehabilitation treatments. The quite promising results presented in this
work on five different healhty subjects underline the importance to calibrate a spe-
cific model for each subject. This led us to expect a successful application also for
ill-conditioned patients since the model will be calibrated considering their own
EMG signals.
The good accuracy shown by the experimental results is promising for the future
steps of this research. We aim at developing a robotic orthosis for ankle-foot reha-
bilitation able to adapt to real patient’s physiological motion capability while still
simple enough to be used by untrained users. The possibility to use the predicted
EMG as input for an EMG-driven neuromusculoskeletal model, that could be used
to develop physiological control strategies, removes the need of trained personnel
Design of a Subject-Specific EMG Model for Rehabilitation Movement 821

for the placement of EMG sensors. In this context, future work will focus on com-
paring neuromusculoskeletal model outputs obtained using as input the predicted
EMGs or the directly measured signals. The final system will be validated compar-
ing the estimated ankle flexion extension (AFE) moment with the net AFE moment
experimentally measured with a Biodex (Biodex, Corp., Shirley, NY).

Acknowledgements. This research has been partially supported by EU-F7 grant BioMot
(project no. 611695) and by the ERC Advanced Grant DEMOVE (project no. 267888).
The authors would like to thank Stefano Ghidoni of the IAS-Lab (Univ. of Padua) for the
assistance with the camera data processing.

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A Pilot Study on Clinical and Neurological
Effects of Neurofeedback Training for
Treatment of Central Neuropathic Pain

Aleksandra Vuckovic1, Muhammad A. Hasan1,2, Matthew Fraser3,


Bernie Conway4, and David B. Allan3

1 Biomedical Engineering Research Division,


School of Engineering, University of Glasgow,
James Watt Building (South), Glasgow, G12 8QQ, UK
aleksandra.vuckovic@glasgow.ac.uk,
m.hasan.1@research.gla.ac.uk
2
Department of Biomedical Engineering,
NED University of Engineering and Technology, Karachi, Pakistan
3
Queen Elizabeth National Spinal Injuries Unit, Southern General Hospital,
1345 Govan Rd, Glasgow, G51 4TF, Glasgow
{Matthew.Fraser,Spinal.Unit}@ggc.scot.nhs.uk
4
Department of Biomedical Engineering,
University of Strathclyde,Wolfson Centre,
106 Rottenrow, Glasgow, G4 0NW, UK
b.a.conway@strath.ac.uk

Abstract. The aim of the study was to investigate the effect of neurofeedback
training on central neuropathic pain in patients with chronic paraplegia. Patients
EEG activity was modulated from the central areas of the cortex, electrode
location C3/Cz/C4. Training consisted of reducing EEG power in theta (4-8 Hz)
and higher beta (20-30 Hz) frequency ranges and increasing power in the higher
alpha range (9-12 Hz). Patients received 20-40 neurofeedback treatment and four
out of five patients reported clinically significant reduction of pain (>30%). EEG
during neurofeedback revealed a wide spread modulation of power in all three
frequency bands accompanied with changes in the coherence. LORETA analysis
of EEG before and after neurofeedback therapy revealed general reduction of
power in all frequency bands, most notably in 12-15 Hz and 20-30 Hz bands.
Areas with reduced power included the Anterior Cingulate Cortex and the Insular
Cortex, known to be involved in processing of chronic pain. Further studies on
larger number of patients will be needed to confirm clinical relevance of
neurofeedback therapy for treatment of central neuropathic pain.

1 Introduction

Central neuropathic pain (CNP) is caused by an injury to the somato-sensory


system with a prevalence of 8% in the general population [1]. Its symptoms don’t

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 823
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_113, © Springer International Publishing Switzerland 2014
824 A. Vuckovic et al.

respond well to medication and the drugs used are often associated with significant
adverse effects [2]. This has generated interest in nonpharmacological treatment
methods based on neurostimulation, such as repetitive Transcranial Magnetic
Stimulation (rTMS) [3] and transcranial Direct Current Stimulation (tDCS) [4].
Both rTMS and tDCS achieved the best results when applied over the primary
motor cortex, which is not part of the conventional pain matrix. However, recent
fMRI studies confirmed increased activation of the motor cortex in patients
suffering from CNP [5] which might explain the effectiveness of rTMS and tDCS
[3,4].
Neurofeedback is similar to rTMS and fDCS, in that it is also a neuromodulation
technique. It is however based on self-induced rather than externally evoked
modulation of brain activity that can be learned and practiced when needed.
Neurofeedback has been successfully used for some other types of chronic pain,
such as migraine and complex regional pain syndrome [6]. Results of
neurofeedback studies for CNP are inconclusive, using neurofeedback protocols
that do not target the motor cortex [7].
Results of EEG studies on CNP patients have shown that these patients have
dominant alpha frequency shifted towards the lower values and have increased
EEG power [8,9].
In this study we present a novel neurofeedback protocol for treatment of CNP
inspired by the results of neurostimulation techniques [3,4] and based on
measurement of EEG activity in patients with CNP [8]. We tested our protocol on
paraplegic patients suffering from CNP.

2 Methods

2.1 Patients
Seven chronic patients with paraplegia (age 50±4, 6 males, 1 female) having CNP
in their legs and the abdomen were recruited for the study. All patients had pain
level at 5 or higher on the Numerical Rating Scale (NRS). Patients were also
recruited in another study of our group in which baseline EEG activity of
paraplegic patients with CNP was compared with the EEG activity of paraplegic
patients with no pain and of able bodied volunteers [9]. The study confirmed that
patients with CNP had significantly higher power of EEG signal and significantly
lower dominant alpha frequency than the other two groups.

2.2 EEG Offline Recording and Analysis


EEG was recorded from 61 channels (Synamp2, Neuroscan, USA) in the relaxed
open-eye state with electrodes placed according to standard 10-10 locations using
an ear-linked reference and AFz as ground. Sampling frequency was 250 Hz and
impedance was kept below 5kΩ. EEG was recorded in three 2 min sessions. After
A Pilot Study on Clinical and Neurological Effects of Neurofeedback Training 825

removing sections with extensive noise (>100 µV) at least 3 min of recording was
analysed.
The sLORETA [10] (estimated current density) cortical map/image was
computed for 6239 voxel partitions of intracerebral volume at 5 mm spatial
resolution. Brodmann areas are reported using the Montreal Neurological Institute
(MNI) space with correction to the Talairach Space.

2.3 EEG On-Line Recording and Neurofeedback Protocol


During NF patient’s EEG was recorded with up to 16 electrodes (F3, Fz, F4, T7,
C3, Cz, C4, T8, Cp3, CPz, C4, P4, P3, O1, Oz and O2), using Usbamp, (Guger
technologies, Austria). Sampling frequency was 256 Hz and electrode impedances
were below 5kΩ. On-line neurofeedback was provided to a patient from one
electrode at the time for each NF training session. On each training day, before and
after NF session, patient’s EEG was measured in relaxed open-eye and closed-eye
state for 2 min. In the eyes-open state, EEG power was calculated in 4-40 Hz band
and in theta (4-8 Hz), alpha (9-12 Hz) and high beta (20-30) Hz bands. Relative
power was calculated for each frequency band by dividing the power of the
frequency band with the power of 4-40 Hz band. In the eyes-closed state relative
EEG power was calculated for 6-10 Hz band from the occipital area (Oz).
A session always started with audio neurofeedback training provided from Oz
with patients having their eyes closed. Patients listened to relaxing music which
had two levels: quieter when the power of EEG signal was above the ‘threshold’
and louder when the EEG power was under the threshold. The threshold was set to
110% of the baseline value and patients were trained to increase EEG power. Each
patient received two 3 min long audio neurofeedback sub-sessions. The main
reason for practicing audio neurofeedback was relaxation and patients were not
expected to experience reduction of pain.
Following audio NF training, patients practiced visual NF in order to reduce
pain. We trained patients to reduce (down-regulate) the relative energy in the theta
and beta band. Based on findings that patients with CNP have a reduced dominant
frequency in the alpha band [8.9], we trained patients to increase (up-regulate)
energy in the ‘higher’ alpha band (9-12 Hz). We set the training ‘threshold’ to
110% of the average power in the alpha band and to 90% of the average power in
the theta and beta band. We provided training from electrode location C4/C3/Cz in
six to seven 5 min long sub-sessions. These electrodes were chosen because they
are located over the primary motor cortex.
During NF training the patient sat in front of a computer screen showing three
bars, the size of which corresponded to relative EEG power in the three chosen
frequency bands, described above. Bars were green when power of the
representative frequency band was in the right range (under the threshold for the
theta and beta band and above the threshold for the alpha band) and red when it
was out of range. Patients were instructed to relax and to ‘do whatever necessary to
make the bars green’.
826 A. Vuckovic et al.

Table 1 Information about patients

Patient/ Injury level Years after Pain


Nr of injury before/after
Sessions NF (NRS)
1/40 T5 complete 5 6/5
2/40 T6 complete 5 7/5
3/40 T6 incomplete 9 6/2
4/40 T6 incomplete 25 9/6
5/20 T6 incomplete 9 9/6

Fig. 1 Power spectral density before neurofeedback (NF) training session, during NF and
after 30 min of NF training in Patient 5. Arrows indicate increase in alpha and decrease in
beta power.

On-line data analysis was developed in Simulink under Matlab and the
Graphical User Interface was designed in LabView. Ethical approval was obtained
from the Ethical committee for the Greater Glasgow and Clyde Health Authority.

3 Results

Five out of seven patients completed the study. One patient dropped out after
failure to experience reduction of pain after 3 NF sessions and one patient dropped
out after 3 NF sessions due to problems with transport. Four patients received 40
sessions and the fifth patient, who stayed at the hospital for the purpose of the
study, received 20 sessions. Patients who travelled from their homes received 1-3
sessions per week while a patient who stayed at the hospital received daily NF
therapy.
A Pilot Study on Clinical and Neurological Effects of Neurofeedback Training 827

3.1 The Effect of NF Training on the Intensity of Pain


All five patients achieved a statistically significant reduction of pain and in four
patients this reduction was clinically significant (>30%) reduction. Table 1 shows
pain intensity at the beginning and at the end of the NF therapy. During each
session of NF training patients reported an immediate reduction of pain. However
to achieve a longer-term effect that lasted from one session to another, repeated
sessions were needed. The reduction of pain in all patients was gradual and lasted
for several weeks after termination of the therapy.
Initially we tested several locations over the primary motor cortex: C3, Cz and
C4. In patients with incomplete paraplegia (preserved sensation) we occasionally
observed the uncontrolled movements of legs or the whole body (spasm) which
was higher when practicing from C3 than from C4, so we chose C4 as a preferred
training site to reduce discomfort. Anecdotally patients reported being spasm-free
for several hours following NF training. Interestingly, NF training from Cz, which
is located over the cortical area that corresponds somatotopically with the legs,
produced the smallest reduction of pain.

3.2 EEG Modulation during NF Training


Figure 1 shows logarithmic Power Spectral Density (PSD) in one patient before,
during and after NF. The patient modulated their EEG power in the desired
direction, increasing the alpha and decreasing the beta power; PSD remained in the
desired range even several minutes after finishing the daily NF treatment (post-NF,
Fig 1). Figure 2 shows scalp maps of PSD over three frequency bands before and
during training at electrode location C4. Neurofeedback training affected PSD
recorded over wider areas of the skull in all three frequency bands. This was very
prominent in the beta range where PSD was also reduced contralateral to the
training site. All other patients showed similar wide spread modulation of EEG
power during NF training. The widespread neuromodulation might be partially
attributed to the fact that EEG recorded over C4 reflects activity of mixed neural
sources, in particular in the alpha range, that is a wide spread rhythm. To check for
this, the analysis of coherence between different areas of the brain was performed
for 16 channel recording. Large changes (both increase and decrease) were noticed
in the beta range in all five patients. Figure 3 shows change in the coherence which
correspond to PSD shown in Fig 2. The occipital areas showed a reduced coherence
with the other parts of the cortex in all three frequency bands; the coherence
increased between the central and the frontal areas in the alpha and beta (20-30 Hz)
band.
We tested a placebo effect by providing an occasional feedback from the
electrode location Oz without informing patients. This location was chosen because
the occipital area is normally not involved in the pain matrix and patients did not
report reduction of pain during audio NF training from that site. Patients typically
did not report reduction of pain during these placebo trials. Four patients however
828 A. Vuckovic et al.

Fig. 2 Cortical maps of power spectral density in the theta (4-8 Hz), alpha (9-12 Hz) and
beta (20-30 Hz) frequency bands before and during NF practice in patient 5. Black dots
indicate training site C4.

Fig. 3 Changes in coherence (During NF-before NF) in three frequency ranges.The same
EEG data were used as in Fig 3. Solid lines present increase and dashed line presents
decrease in coherence.

learned to practice the neurofeedback mental strategy without a visual feedback


(confirmed by EEG recording); after that stage it was very difficult to assess the
placebo effect.

3.3 The Long-Term Effect of NF Training


Multichannel EEG in relaxed state was analyzed in four frequency ranges: theta (4-
8 Hz), alpha (8-12 Hz), lower beta1 (12-15 Hz) and higher beta2 (20-30 Hz). The
lower beta band was included in the analysis as a rhythm used in some previous
neurofeedback studies of chronic pain [6]. Figure 4 shows the difference in
LORETA estimate of current density after the last day of training and before the
first day of training. A wide spread reduction of the activity could be noticed, in
particular in higher frequency bands. Figure 5 shows reduction of activity at ACC
(BA 24) in beta band (12-15 Hz) averaged over all five patients.

4 Discusion
The paper presents the effect of NF training on reduction of CNP and on related
neurological measures. Using a graphical user interface, patients learned how to
modulate their brain activity in a desired direction which resulted in reduction of
pain. Although the effect of training on intensity of pain lasted for several weeks
A Pilot Study on Clinical and Neurological Effects of Neurofeedback Training 829

Fig. 4 LORETA images of the lateral views of the cortex showing differences in activity
(after last day -before first day of NF) averaged over 5 patients. Blue presents negative
values.

Fig. 5 LORETA images of differences in activity(after-before NF) in 12-15 Hz range


averaged over 5 patients, in ACC (BA 24). Blue presents negative values.

after the therapy, a regular NF would be needed to achieve a long lasting effect and
to help patients to practice NF mental strategy from memory for a longer period of
time.
While patients practiced NF provided from one electrode site only, the effect on
EEG power was widespread. This can be partially attributed to the nature of the
EEG signal which reflects the activity of multiple sources. However a wide spread
modulation of power can also be attributed to changes in connectivity, as confirmed
by the analysis of coherence. We provided training from the electrodes located over
830 A. Vuckovic et al.

the primary motor cortex, as this was a preferred stimulation site in rTMS and
tDCS studies [3,4]. Yet, because the primary motor and sensory cortices are close
to each other, we cannot exclude the possibility that the activity of the sensory
cortex was also modulated. Although NF was practiced from the right side central
cortex, somatotopically corresponding to the left arm, patients reported reduction of
pain in their legs. This is in accordance with observation from rTMS studies that
the exact somatotopical location of stimuli is not relevant [11].
Previous studies on CNP found the strongest correlation between the intensity of
theta and low beta (12-16 Hz) power and the intensity of pain [12]. Although we
noticed reduced activity in all frequency bands, the reduction of power was
strongest for the beta1 (12-15 Hz) band including the pain related areas of brain
such as ACC and IC.
We tested NF on patients who had a long-standing CNP. The effect of NF might
be better on patients who suffered from CNP for a shorter period of time, as
prolonged pain might cause long lasting changes in brain connectivity [13].
To our knowledge this is the first study to show a positive effect of
neurofeedback on CNP. Further studies on larger number of patients would be
needed to confirm the effectiveness of neurofeedback in clinical practice.

Acknowledgment. This work has been partially supported by the MRC grant G0902257/1,
the Glasgow Research Partnership in Engineering and by NED University of Pakistan PhD
scholarship. We thank Dr Purcell and Dr Mclean for choosing participants of the study and
to all participants.

References
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1075–1083. Elsevier, Philadelphia (2006)
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stimulation of primary motor cortex for neuropathic pain: a randomized, multicenter,
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438–445 (2010)
Parametrization of an Exoskeleton for
Robotic Stroke Rehabilitation

Patrick Weiss1 , Georg Männel2 , Thomas Münte3 ,


Achim Schweikard4 , and Erik Maehle5
1
Institute of Computer Engineering and the Graduate School for Computing in
Medicine and Life Sciences, University of Lübeck, Germany
2
Institute of Computer Engineering, University of Lübeck, Germany
3
Department of Neurology, University Medical Center Schleswig-Holstein,
Lübeck, Germany
4
Institute for Robotics and Cognitive Systems, University of Lübeck, Germany
5
Institute of Computer Engineering, University of Lübeck, Germany

Abstract. This paper describes a novel exoskeleton focusing on its


parametrization and the redesign of the mechanical metacarpophalangeal
joint with an integrated sensor. The joint is based on an arc structure with
its rotation axis being aligned with the anatomical center of rotation. A Hall
effect based linear encoder is integrated into the base-connected arc read-
ing out a multi-pole magnetic strip in the moving arc. The accuracy was
evaluated based on the tendon displacement measured by the motor encoder
and converted into the respective angle with two different calculation meth-
ods. The parametrization adapts the exoskeleton to the patient’s hand size to
avoid misalignment without the use of adaption mechanisms. The exoskeleton
is parameterized to a stroke patient. The measurement process is described
and evaluated, quantitatively, by comparing two data sets and, qualitatively,
by examining the visual overlay of the model onto an image of the hand.

1 Introduction
Stroke is the leading cause of acquired disabilities [1]. In around 60 % of
the cases, the hand is impaired for longer periods and estimated 5 - 20 %
do not recover completely [2]. Hand impairments constitute significantly to
the patient’s independence and lead to problems in coping with daily life
activities.
Post stroke therapy mostly includes repetitive, task-specific training [3]
which makes it a suitable field to take advantage of robotics. Although there
is no general consensus about the effectiveness of robotic rehabilitation [4],
a recent study showed that it can improve motor function after stroke [5].
Besides increasing the outcome in comparison to traditional therapy, robotic
rehabilitation can also be an important tool by extending the rehabilitation

This work was supported by the Graduate School for Computing in Medicine
and Life Sciences funded by Germanys Excellence Initiative (DFG GSC 235/1).

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 833
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_114,  c Springer International Publishing Switzerland 2014
834 P. Weiss et al.

to the home environment. This requires inexpensive portable hardware which


is usable without the help of therapists.
Several robotic rehabilitation systems have been developed to support and
extend traditional therapy [6]. Due to the high complexity of the hand, exo-
skeletons tend to be complex, expensive, and bulky e.g. [7, 8]. Devices that
use adjustment mechanisms to fit different hands [7, 9] can increase weight
and set up time impeding the use outside a clinical setting. Some systems use
orthodic material to increase compliance and compensates rigid mechanical
motion [10], which could, however, lead to soreness and incorrectly trained
motions [11]. These problems impede the use of exoskeletons in the home
environment.
We address these shortfalls by applying rapid prototyping technology for
manufacturing that enables us to parameterize the computer-aided-design
(CAD) model of the exoskeletons. The parameters control the link dimen-
sions which are based on measurements of the user’s hand dimensions. Thus,
misalignment is reduced without the use of adjustment mechanisms, and, due
to dropping prices, 3D-printing is expected to become economical even for
single customized versions.
The first prototype iteration demonstrated the functioning of the concept
[12]. This paper presents the new design considering experiences from the
former version. It focuses on the revised metacarpophalangeal joint (MCP)
with an integrated angle sensor. Moreover, the extended parametrization is
described and evaluated.

2 Design and Implementation


2.1 Mechanical Design
The development of hand exoskeletons requires to accept trade-offs due to the
complexity and the high degree of freedom (DOF) of the anatomy. Especially
focusing on cost-effective systems, we restrict the number of actuators to one
per finger which pulls at the exoskeleton’s tip over a tendon-based transmis-
sion. A 3D-printed winder is mounted within a casing on the shaft to attach
the tendon. The drawback of this simplified design is that the trajectory is
not defined. Still, different kinds of training are made possible by changing
the configurations. The cable can also be attached to the MCP to control one
DOF with one motor. Another possibility is to block the MCP to focus on
training of distal interphalangeal joint (DIP) and proximal interphalangeal
joint (PIP). The therapy may be supported with the use of botulinum toxin
[13].
A Faulhaber 2657 CR motor exerts a nominal torque of 44 mNm which
results in a force of 14.7 N with a winder radius of 3 mm. A gear was omitted
reducing friction and avoiding other undesired effects like backlash. Thus,
actuation and sensing is improved and high backdrivability can be achieved
Parametrization of an Exoskeleton for Robotic Stroke Rehabilitation 835

which is an important property for haptic systems. Moreover, the weight is


lower than a motor-gear combination with about the same nominal torque.
Increased tone is a common stroke symptom which makes the donning
of gloves problematic. Therefore, the exoskeleton is left open on the palmar
side. The fingers are detachable from the palm, which is necessary for the
integration of the sensor. Moreover, a set of generic palm and finger sizes
can be created so that customization to every single user is not necessarily
required. They are secured with retaining rings that go into a groove on
the pin of the guiding arc. The material strength at the side is thinner in
comparison to the former version, which increases the range of abduction.
The metacarpophalangeal (MCP) joint’s abduction / adduction rotation is
designed as a pin joint. The joint for extension / flexion is redesigned to match
the mechanical and anatomical joint’s center of rotation. It consists of two
arcs gliding into each other and bearing beads to avoid contact between the
arcs and reduce friction. The guiding arc is connected to the palm whereas the
other arc is attached to the proximal phalanges with their midpoints forming
the center of rotation. Two beads follow the guiding arc and are kept from
falling out by the use of an indentation. The other two beads run freely within
a groove (Fig. 1). Inserting two beads more leads to more stability, but also
to higher friction and lower range of motion (ROM). The new design requires
to replace the formerly used Hall effect based angle sensors which determined
the rotation by measuring the field of magnets in revolute the joints [12]. In
comparison to other arc structured joints [9, 11], the angle sensor is integrated
into the design which is described in section 2.3.

Guiding arc connected to palm Bearing beads fixed


to guiding arc

Space for
Arc attached to finger
magnetic strip

Center of rotation
Floating bearing beads
PIP Revolute Joint contraint by finger arc

Fig. 1. Schematic drawing of the MCP joint

Since the metacarpus is not a plane area, we introduce parameters to adapt


the exoskeleton’s base to the anatomy. We divide the base into three angled
planes that roughly follow the transversal arc. Slits and taperings increase
flexibility and compensate for parametrization errors.
836 P. Weiss et al.

2.2 Parametrization
The parametrization enables customizing the exoskeleton’s dimension to sin-
gle users reducing joint misalignment and, thus, unwanted reaction forces. In
comparison to the previous prototype, the total number of measurements is
increased from 34 to 44. Fig. 2 depicts the parameters inserted into a scan of
the hand. The measurements for width and height are shown in orange and
the joint positions and link lengths in yellow. Further parameters define the
material strength and thickness of an additional neoprene layer.
The parameters are based on measurements by hand using a caliper. The
soft tissue complicates exact measurements. As a rule, slight force was intro-
duced and the measurement was taken after the relaxation of the soft tissue.
Two sets of measurements were taken by different persons to reduce errors
in the measurement process.

DIP-Tip
DIP-Tip Width DIP DIP-Tip

Width DIP Width DIP


PIP-DIP
DIP-Tip
PIP-DIP PIP-DIP Measured
Width PIP
Height DIP at each
Width PIP DIP-TIP finger
Width PIP PIP-DIP
Width DIP Height PIP
MCP-PIP MCP-PIP
PIP-DIP
Outer side of the
MCP-PIP MCP-PIP
Os metacarpale II head MCP: Width PIP
MCP:
IF-MF
MF-RF MCP-PIP
MCP: Height MC
RF-IF Width of the hand along
Distance between W-IF the knucklebones
W-MF
the center of the wrist W-RF (Width Hand)
and the outer side of the
W-LF Outer side of the
hand at the index finger
(W-IF lateral) Os metacarpale V head

Center of the wrist


Distance between
approximately on
the center of the wrist
the tendon sheath
and the outer side of the
Width Wrist hand at the little finger Height Wrist
(W-LF lateral)

Edges between carpal


and forearm bone

Fig. 2. Measured parameters

2.3 Joint Angle Sensing


The redesign of the joint does not permit to use Hall effect sensors in combi-
nation with rotating magnets for angle sensing. Nevertheless, capturing the
MCP movement remains important to assess the rehabilitation progress and
Parametrization of an Exoskeleton for Robotic Stroke Rehabilitation 837

to give real-time feedback on the performance enabling motivating games and


study of motor learning.
We use a chip with integrated Hall elements to measure rotary motion in
combination with a multi-pole magnetic strip. The advantages are that the
chip and the strip can be integrated into the joint and that the measurements
are contactless so that friction is not increased. The integrated circuit (IC)
AS5306 by AMS sits in a recess of the outer arc and reads the magnetized
strip on the inner arc and provides a quadrature incremental output with a
resolution of 15 μm.
The resulting angle resolution depends on the parameters of the customized
joint. For a radius of 20.44 mm of the bent magnet strip belonging to the
exoskeleton of a female subject, the angle resolution is 0.04◦ . Besides the
quadrature channels, the IC provides an analog signal of the magnetic field
strength and a channel showing pole transitions and loss of signal.

3 Evaluation
First, the parametrization of the glove is evaluated, both, qualitatively and
quantitatively, followed by the accuracy assessment of the MCP joint sensor.

3.1 Parametrization
The exoskeleton was parametrized to a female patient who suffered stroke in
2004. Her hand functionality is strongly impeded and tone is increased. Fig.
4 shows an image of the printed exoskeleton.
The parametrization was evaluated in three different ways. First, compar-
ing differences between the subjects in the measurement data itself which
gives conclusions about its accuracy. Then, the parameterized model was
compared to a scan of the healthy hand. It was not possible to scan the im-
paired hand due to the increased tone. Finally, the print was qualitatively
evaluated.

3.1.1 Measurements
Two subjects obtained two sets of parameters each from the healthy and
the impaired hand of the patient. The average of both measurements of the
impaired hand is used for the parametrization.
The standard deviation (SD) between both subjects over all measurements
gives conclusions about the accuracy of the measurement. The squared de-
viation from the mean for each pair of measurements was summed up and
divided by the samples for both subjects resulting in a SD of the impaired
hand of 1.44 mm, and 1.3 mm of the healthy hand.
838 P. Weiss et al.

Table 1. Measured values of the left hand in millimeters. Left of the vertical di-
viding line: Parameters taken from the back of the hand. Right of the dividing
line: Only parameters of the index finger are exemplary stated (highest deviations
compared to other fingers). S1/S2 = measurements by subject 1/2, SD= stan-
dard deviation, W = wrist, IF = index finger, MF = middle finger, RF = ring fin-
ger, LF = little finger. The measurements with their abbreviations are visualized in
Fig. 2.

MCP: MF-RF

MCP: RF-LF
MCP: IF-MF

Height Wrist
Width Wrist

Height MCP
Width Hand

W-LF radial

Height DIP
W-IF ulnar

Height PIP

Width DIP
Width PIP
MCP-PIP

PIP-DIP

DIP-Tip
W-MF

W-RF

W-LF
W-IF

S1 78.2 75.0 64.8 65.5 25.1 21.6 20.5 53.0 35.7 72.9 78.5 67.0 39.0 23.0 20.8 14.4 13.2 11.7 10.1 23.0
S2 71.1 69.2 66.4 63.6 23.2 18.9 16.3 50.4 35.6 70.3 75.1 68.6 39.0 23.0 20.8 14.4 13.2 11.7 10.1 23.0
SD 3.55 2.9 0.8 0.95 0.95 1.35 2.1 1.3 0.05 1.3 1.7 0.8 4.8 1.1 0.85 1.25 0.35 0.6 0.15 0.85

Table 1 contains the measured values related to the palm and, exemplary,
the measurements from the index finger of the impaired hand only. The other
fingers showed comparable but even better results with lower SDs.

3.1.2 Visual Comparison


A visual comparison between the modeled exoskeleton and an image of the
hand was used to further evaluate the functioning of the parametrization
before printing.
The camera was manually pointed onto the hand from a top-down per-
spective. A caliper was set to 10 mm and placed next to the hand acting as
a reference to resize the image to the same scale as the model. The scaling
was carried out in the CAD program by drawing a 10 mm line and fitting
the caliper on the image to the same length.
The qualitative observation reassured the functioning of the parametriza-
tion. Strongest deviations are found at the little finger, which was, however,
not completely extended due to increased tone. The figure also shows that
the middle and the ring finger overlap. This means that the exoskeleton will
cause slight abduction of the fingers.

3.2 MCP Joint Sensor Accuracy


For the evaluation of the accuracy, the measurements of the new sensor are
compared to an angle estimation based on the tendon displacement. One fin-
ger is fixed in a bench vise and the tendon is connected to a motor fixed at a
second vise. At the beginning of the experiment, the MCP is fully flexed and
the DIP and PIP remain fully extended so that only the MCP joint changes.
Then, the motor pulls at the finger until the MCP is completely extended
and the motor encoder and AS5306 samples are stored simultaneously. The
Parametrization of an Exoskeleton for Robotic Stroke Rehabilitation 839

10 mm

10mm

Fig. 3. Comparison of the parametrized model to an image of the impaired hand


(l.) and a scan of the right hand (r.) with their parameters based on the respective
measurements.

Alternative Tendon
d Attachment

Revolute PIP joint

Tendon
Attachment Bead
Guiding points
(d for MCP Angle Evaluation)

Fig. 4. Parametrized exoskeleton put on patient

sensors start counting at the beginning of the experiment so that the compar-
ison represents the relative angular accuracy. The experiment was repeated
four times.
840 P. Weiss et al.

The motor encoder values represent the relative displacement of the tendon
which is a function of the angle, given that only one joint is moved. The angle
is calculated from the motor encoder values by two methods. First, the cosine
formula solves the relation between the tendon displacement, the radii of the
guiding points (Fig. 4), and the joint angle. The parameters are taken from
the CAD drawing.
The second calculation is based on the maximum positions of the joint
and their respective tendon displacement in the form of motor encoder value.
In between, the angle is linearly interpolated according to the current motor
encoder sample.
The results are plotted with the angle of the sensor against the converted
angle from the motor encoder (Fig. 5).

80
AS5306 sensor Ideal
70
Converted angle motor encoder [°]

70 Motor encoder (lin.) AS5306 to conv. motor enc. (lin.)


Motor encoder (trig.) AS5306 to conv. motor enc. (trig.)
60 60

50 50
Angle [°]

40 40
30
30
20
20
10
10
0
0
−10
0 1 2 3 4 0 10 20 30 40 50 60 70
Time [s] Angle AS5306 sensor [°]

Fig. 5. Exemplary plot of one of four runs of the angular accuracy experiment with
the angle over time (l.) and over converted angle (r.).

The root-mean-square error (RMSE) and maximum error were computed


for the linear and the trigonometric approach of the plotted run and averaged
over all four runs (Table 2).

Table 2. Root-mean square error (RMSE) and maximum error of the angular
accuracy experiment

Plotted run (Fig. 5) Avg. over four runs


RMSE Max. Error RMSE Max. Error
Linear 1.89 3.11 1.8 3.24
Trigonometric 1.36 2.81 1.38 2.98
Parametrization of an Exoskeleton for Robotic Stroke Rehabilitation 841

3.3 Discussion
The standard deviations of the parameter measurements are acceptable which
was confirmed in the visual comparison. However, especially the little finger
showed some degree of misalignment which was observed as well when the
patient was wearing the printed exoskeleton. We expect this to be caused by
the impeded measurements due to the strongest muscle spasms of this finger.
The evaluation of the sensor using the motor encoder allows for automating
the sampling process, which is not possible using e.g. a goniometer. Repeating
the experiment resulted in comparable plots speaking for the validity of the
method.
The winder radius has an influence on the estimated angle so that the
change of diameter due to the winded cable can cause errors. Therefore, a
second estimation with linear approach is included, which depends on the
mechanical range of motion. Although the second approach is not without
errors either, it is independent from the first method and gives additional
information on the validity of the evaluation. It cannot clearly be determined
which way is the most accurate but the overlapping of all three results speak
for functioning of the method and low errors in either case.
The higher total RMSE of both calculation methods of 1.8◦ lies slightly
over the angular accuracy requirement for hand rehabilitation applications
of 1.5◦ [14]. This is, however, a good result regarding the inexpensive hardware
and the low manufacturing accuracy and strength of the 3D-printing material.

4 Conclusion
This work presents an exoskeleton based on a parameterized CAD model that
can be fitted to the hand of the patient omitting adjustment mechanisms and,
thus, reducing set up time and weight.
The new MCP joint’s axis of rotation is parameterized so that it aligns
with the anatomical axis. This is advantageous in comparison to the former
prototype where a combination of a revolute and a prismatic joint was used.
The integrated sensor provides joint angle measurement also when no motors
with encoders are equipped.
In the former version, the exoskeleton was printed in one piece. A clear-
ance in the joint kept the moving parts from melting together during the
3D-printing process but also induced errors in the angle sensing. Nominal
dimensioning of the joint parts in the present version avoids additional er-
rors from lateral shifts. The new joint requires to print the exoskeleton’s
parts separately. The consequent assembly effort is reduced by using a clip-in
mechanism to connect them.
The patient was capable of donning the glove herself within four minutes
without practicing. This self-dependence is particularly important for home
rehabilitation.
842 P. Weiss et al.

The next steps are to implement an actuation module with Bowden trans-
mission, extend configurations to support flexion movement, development of
a thumb extension and automation of the parameter acquisition process.

References
1. Johnston, S.C., Mendis, S., Mathers, C.D.: Global variation in stroke burden
and mortality: estimates from monitoring, surveillance, and modelling. The
Lancet Neurology 8(4), 345–354 (2009)
2. Kwakkel, G., Kollen, B.J., van der Grond, J., Prevo, A.J.H.: Probability of
regaining dexterity in the flaccid upper limb impact of severity of paresis and
time since onset in acute stroke. Stroke 34, 2181–2186 (2003)
3. Woldag, H., Hummelsheim, H.: Evidence-based physiotherapeutic concepts
for improving arm and hand function in stroke patients. Journal of Neurol-
ogy 249(5), 518–528 (2002)
4. Kwakkel, G., Kollen, B.J., Krebs, H.I.: Effects of robot-assisted therapy on
upper limb recovery after stroke: a systematic review. Neurorehabilitation and
Neural Repair 22(2), 111–121 (2008)
5. Milot, M.-H., Spencer, S.J., Chan, V., Allington, J.P., Klein, J., Chou, C.,
Bobrow, J.E., Cramer, S.C., Reinkensmeyer, D.J.: A crossover pilot study eval-
uating the functional outcomes of two different types of robotic movement
training in chronic stroke survivors using the arm exoskeleton bones. Journal
of Neuroengineering and Rehabilitation 10(1), 112 (2013)
6. Maciejasz, P., Eschweiler, J., Gerlach-Hahn, K., Jansen-Toy, A., Leonhardt, S.,
et al.: A survey on robotic devices for upper limb rehabilitation. Journal of
NeuroEngineering and Rehabilitation 11(1), 3 (2014)
7. Li, J., Wang, S., Wang, J., Zheng, R., Zhang, Y., Chen, Z.: Development of
a hand exoskeleton system for index finger rehabilitation. Chinese Journal of
Mechanical Engineering 25(2), 223–233 (2012)
8. Jones, C.L., Wang, F., Osswald, C., Kang, X., Sarkar, N., Kamper, D.G.: Con-
trol and kinematic performance analysis of an actuated finger exoskeleton for
hand rehabilitation following stroke. In: 2010 3rd IEEE RAS and EMBS Inter-
national Conference on Biomedical Robotics and Biomechatronics (BioRob),
pp. 282–287. IEEE (2010)
9. Tong, K., Ho, S., Pang, P., Hu, X., Tam, W., Fung, K., Wei, X., Chen, P.,
Chen, M.: An intention driven hand functions task training robotic system. In:
2010 Annual International Conference of the IEEE Engineering in Medicine
and Biology Society (EMBC), pp. 3406–3409. IEEE (2010)
10. Takahashi, C.D., Der-Yeghiaian, L., Le, V., Motiwala, R.R., Cramer, S.C.:
Robot-based hand motor therapy after stroke. Brain 131(2), 425–437 (2008)
11. Burton, T.M.W., Vaidyanathan, R., Burgess, S.C., Turton, A.J., Melhuish, C.:
Sensitivity analysis of a parametric hand exoskeleton designed to match natural
human grasping motion. In: Herrmann, G., Studley, M., Pearson, M., Conn, A.,
Melhuish, C., Witkowski, M., Kim, J.-H., Vadakkepat, P. (eds.) TAROS-FIRA
2012. LNCS (LNAI), vol. 7429, pp. 390–401. Springer, Heidelberg (2012)
12. Weiss, P., Heyer, L., Münte, T.F., Heldmann, M., Schweikard, A., Maehle,
E.: Towards a parameterizable exoskeleton for training of hand function af-
ter stroke. In: 2013 IEEE International Conference on Rehabilitation Robotics
(ICORR). IEEE (2013)
Parametrization of an Exoskeleton for Robotic Stroke Rehabilitation 843

13. Pooyania, S., Semenko, B.: Botulinum toxin type-a (bonta) and dynamic wrist-
hand orthoses versus orthoses alone for the treatment of spastic-paretic upper
extremity in chronic stroke patients. Open Journal of Therapy and Rehabilita-
tion 2, 12 (2014)
14. Shuang, W., Jiting, L., Yuru, Z., Ju, W.: Active and passive control of an ex-
oskeleton with cable transmission for hand rehabilitation. In: 2nd International
Conference on Biomedical Engineering and Informatics, BMEI 2009, pp. 1–5.
IEEE (2009)
Pelvic Support Mechanism for Training
Dynamic Balancing and Turning during
Treadmill-Based Walking: A Pilot Study

Matjaž Zadravec, Andrej Olenšek, and Zlatko Matjačić

University Rehabilitation Institute, Republic of Slovenia, Linhartova 51,


SI-1000 Ljubljana, Slovenia
{matjaz.zadravec,andrej.olensek,
zlatko.matjacic}@mail.ir-rs.si

Abstract. Walking is an important human activity of daily living. Turning during


walking represents up to a half of the time of all walking activities, where humans
use different skills and muscle coordination as compared to the straight walking.
This contribution presents a system for training dynamic balancing and turning
during treadmill-based walking, which includes pelvic support mechanism with
passive 6 DoFs parallel mechanism that embraces pelvis and supports the subject.
For this system, three training modes with different difficulty levels were
developed in order to establish suitable training conditions. In addition, the virtual
scene was programmed that visualizes the walking path during training. To test all
three training modes and compare biomechanical signals of pelvic
rotations/translations during walking on the treadmill that can rotate around its
vertical axis, one subject participated in this initial experiment. The results show
that the pelvic movements are highly correlated with the treadmill rotations
around the vertical axis. The proposed system for training dynamic balancing and
turning during treadmill-based walking with the pelvic support mechanism,
supported by the different training modes and different virtual scenes may be a
promising device to recover the function of walking and balance after neurological
injury.

Keywords: rotating treadmill, pelvic support mechanism, gait rehabilitation,


pelvis angle, robot control.

1 Introduction

Since walking is an elementary function of human movement, gait rehabilitation


in neurologically impaired people is the most important way to improve impaired
gait, which in general is due to spasticity, muscle weakness and diminished
dynamic stability. Pathological walking is cost-ineffective and increases also risk
of falling [1]. Therefore, it is imperative to commence gait rehabilitation as soon

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 845
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_115, © Springer International Publishing Switzerland 2014
846 M. Zadravec, A. Olenšek, and Z. Matjačić

as possible by focusing on task-oriented practice with many repetitions of


particular movement in order to maximize rehabilitation success. In the early stage
of gait rehabilitation physiotherapists focus on regaining muscle strength and
restoration of a cyclic leg movement and eventually on increasingly more
challenging gait maneuvers that improves gait function (e.g. gait initiation and
stopping, straight walking and turning). According to some studies turning during
walking can represent from 8 % to 50 % of all walking activities depending on
environment [2]. Furthermore, in turning people use different muscle coordination
as is the case in straight walking. Nowadays rehabilitation promotes robot-
supported rehabilitation devices including treadmill augmented gait rehabilitation
(e.g. Lokomat, Gait Trainer, AutoAmbulator), which are also able to provide
assist-as-needed support of the lower limbs [3-5]. These devices allow only
straight-walking gait practice, while turning maneuvers during walking on a
treadmill cannot be trained. We proposed a device that enables turning during
walking, where the regular treadmill is placed on a platform, which can rotate
around its vertical axis (i.e. rotating treadmill). Our recent research has shown that
walking on such rotating treadmill is to some extent similar to over ground turning
[6]. Keeping balance during walking and turning is also challenging, especially in
neurologically impaired population. Therefore, the rotating treadmill was further
extended with an innovative passive 6 DoFs parallel mechanism that embraces
subject’s pelvis. It helps keeping balance and prevents falling owing to mechanical
support of spring elements. In order to make the whole system more challenging
for the training sessions, we upgraded it with the virtual scenes showing walking
path with several sections requiring turning movement. Furthermore, the system is
also upgraded with three different training modes each of which controls the
treadmill rotation differently. The objective of this preliminary study was to test
these three training modes supported with the virtual scene. A single
neurologically intact subject was walking on rotating treadmill while different
pelvic biomechanical signals were measured and used in a subsequent qualitative
comparison of performance.

2 Methods

2.1 Rotating Treadmill with Pelvic Support Mechanism


Rotating treadmill is composed of the three main components: base plate, rotating
platform and conventional treadmill. Base plate creates ground surface on which
the rotating platform is moving. To confine the rotation of the rotating platform
around the vertical axis a mechanical vertical axis is mounted in the center of the
base plate. On the edge of rotating platform four castor wheels and two larger
wheels are positioned in a way that the center of rotation of the rotating platform is
aligned with the passive vertical axis. One larger wheel is equipped with a DC
servo motor and motor controller that impose the rotation on the rotating platform
and the other wheels support the weight of the whole apparatus. Rotating platform
Pelvic Support Mechanism for Training Dynamic Balancing and Turning 847

carries a conventional treadmill which enables a person to walk straight locally in


the coordinate system of rotating platform, and also changing directions of walking
by rotating the rotating platform globally in the coordinate system of base plate.

Fig. 1 Schematic representation of rotating treadmill with pelvic support mechanism on the
left, and all three pelvic rotations: pelvic list (upper right), pelvic vertical (middle right)
rotation and pelvic tilt (bottom right)

The innovative and important component for gait balance and coordination of
walking is pelvic support mechanism, which consists of four parts: supporting
springs, supporting bars, translational spherical joints and pelvic link. Pelvic link is
attached through the two spherical joints to the support bars. The support bars, each
on one side of the treadmill, are mounted through the support springs to the rotating
platform. Pelvic link has 6 DoFs (3 translations and 3 rotations), which allow the
user to freely move the pelvis. Due to the supporting springs attached at the bottom
of the supporting bars, pelvis can move forward/backward and left/right, while the
translation of the spherical joint along the supporting bars on the top enables pelvis
up/down movement. Three rotations allowed by pelvic mechanism are pelvic list,
pelvic vertical rotation and pelvic tilt. The rotating treadmill and 6 DoFs pelvic
support mechanism with translation and rotations markings are schematically
represented in Fig. 1.

2.2 Training Modes


Three different training modes, supported with the virtual environment, were
developed for walking on the rotating treadmill: robot control mode, human
848 M. Zadravec, A. Olenšek, and Z. Matjačić

control mode and robot-human control mode. A detailed description is given


below.
• Robot control mode is a closed-loop mode meaning that the system
controller drives the rotation of rotating platform on the basis of predefined
reference path shown in the virtual scene. Here, the subject does not
contribute anything to the system control; the subject only follow the speed
of the treadmill while keeping balance during turning movement of the
rotating platform.
• Human control mode is an open-loop mode, where the turning (i.e. rotation
of the rotating platform) is initiated only with the voluntary movement of the
subject’s pelvis while walking on the treadmill. To initiate the turn, the
subject has to translate the pelvis in the lateral direction up to the predefined
threshold value (i.e. pelvic left/right displacement angle). In the virtual scene
the desired walking path is shown to which the subject should follow. Here,
the system controller does not contribute anything to the turning initiation.
• Robot-human control mode is a combination of both previous modes.
Around reference walking path a tolerance area is defined, where human
control mode is enabled. As soon as the shortest distance between the
subject’s current position C and the reference path dC is greater than
maximum tolerated distance dmax, the controller switches to robot control
mode, which guides the subject back to the reference walking path at the
desired point F and then switches back to human control mode. The
schematic representation of this mode is shown in Fig. 2.

Fig. 2 Schematic representation of the robot-human control mode

2.3 Experimental Setup


One male subject (age: 30, weight: 75 kg, height: 181 cm) with no known
neurological or orthopedic disorders participated in our preliminary experiment.
Pelvic Support Mechanism for Training Dynamic Balancing and Turning 849

The subject was placed on a treadmill and the pelvic link was raised to the pelvis
height. Pelvic link was then tightened around subject’s pelvis in a way that
allowed comfortable feeling during walking. Walking speed was set to 3 km/h and
the maximum angular velocity of the rotating platform did not exceed 30 deg/s. To
visualize the path of walking, we programmed a virtual scene showing current
walking trajectory as shown in the example in Fig. 3. Virtual scene was displayed
in a computer screen, which was fixed to the rotating platform and raised to the
head height in front of the subject. The subject tested all three training modes,
where each lasted approximately two minutes.

Fig. 3 Example of a virtual scene showing walking path

2.4 Data Acquisition


To obtain data about subject’s pelvis position and orientation the inclinometers
were placed on each supporting bar as shown in Fig. 1. The signals from the
inclinometers, which measure the inclination of the supporting bars, were first
filtered with a suitable low-pass filter in order to remove noise and irrelevant part
of the signal, followed by a calculation of the pelvic rotation angle and pelvic
left/right displacement angle. In order to relate these signals with the rotation of
the rotating platform, angular velocity of the rotating platform was also recorded
in MATLAB/Simulink environment.
850 M. Zadravec, A. Olenšek, and Z. Matjačić

3 Results

The results of the experiment are shown in Fig. 4. There are three graphs of three
training modes showing the measured data: angular velocity of the rotating
platform (grey-colored area), pelvic rotation angle (solid line) and pelvic
displacement angle in the lateral (left/right) direction (dotted line) as a function of
training time. Red-colored area in the robot-human control mode graph represents
the angular velocity, when the controller switched to the robot control mode.
Positive angular velocities define the rotation to the right and vice versa.
Similarly, positive pelvic rotation angles (pelvic L/R displacement angles) define
pelvic rotation (pelvic lateral translation) to the right and vice versa. The results
show some features displayed by a human when walking on a rotating treadmill.
In a robot control mode it can be seen that the correlation between angular
velocity and pelvic rotation angle is quite high. For example, when the treadmill is
turning counter clockwise, at first the pelvis is left behind, which can be seen,
when pelvic rotation angle is making an opposite turn (i.e. to the left). This short-
timed feature is a transitional in his nature and occurs at the beginning of the
treadmill rotation and lasts until human starts to making a turn. The amplitude of
this initial turn is around 3 deg. Afterwards the human starts to rotate his pelvis as
a response to the rotation of the rotating platform. When rotating, the pelvic
rotation angle goes ahead of the treadmill turning angle to around 5 degrees and it
drops to zero with the termination of platform rotation. In lateral plane of
movement, the pelvic L/R displacement angle also shows some correlation with
treadmill rotation, but particularly with this person in robot control mode the
pelvic displacement angle is more expressed to the right direction (i.e. positive
angle), while there is no correlation when observing left rotations. Similar
behavior can also be seen in the human control mode, only with the difference that
the pelvic rotation angle and pelvic L/R displacement angle outpass the angular
velocity, which is the consequence of this mode – the turning is initiated with the
pelvic L/R displacement. The angular velocity is here more step-shaped than in
the robot control mode, because with the human turning movement as the
initiation of platform rotation the robot controller is rotating the rotating platform
only with the constant angular speed (approximately 30 deg/s), while in the robot
control mode the angular velocity depends on the planned walking path. The
bottom graph shows all measured signals in the robot-human control mode, where
the angular velocities when switching to the robot control mode (red-colored area)
are lower than those in the human control mode, because the robot is controlling
the rotation only with needed angular velocity – e.g. to come from the current
point C to the desired point F. Here, both angles are not as correlated with the
angular velocity as in the previous modes, but nevertheless, on some occasions,
especially when turning is initiated with the subjects’ pelvis, the previously
described features can be observed.
Pelvic Support Mechanism for Training Dynamic Balancing and Turning 851

Fig. 4 The results of robot control mode (upper graph), human control mode (middle graph)
and robot-human control mode (bottom graph) show angular velocity of the rotating
platform, pelvic rotation angle and pelvic left/right displacement angle. Red-colored area in
the bottom graph represents angular velocity when switched to the robot control mode.

4 Discussion

In this preliminary study we focused on three control modes for the rotating
treadmill, which are important in the training sessions for impaired people with
reduced ability of walking. Although, this preliminary study was done on a single
healthy subject, some very preliminary observations can be summarized as
follows. All three control modes have different difficulty level. Physical and
cognitive challenge depends in particular whether the initiation of turning is in the
domain of the subject or of the controller. Referred to this, the least demanding
training mode is the robot control mode in which the patient is not required to
initiate the turning. Turning is preprogrammed according to the walking path in
the virtual scene. In this case, the subject can concentrate only on walking and
keeping the balance. Slightly more challenging task is the robot-human control
mode. Here, the subject takes control of turning partially with the supervision of
the robot controller. This mode may actually be a very appropriate mode from the
perspective of implementing some adaptive features in the controller in the sense
of following the well-established “assist-as-needed” approach, which is common
in controlling the rehabilitation robots. In our case, a simple on/off controller was
used, which was switching between the human control mode and the robot control
mode depending on whether the subject was located within the tolerance area or
not. Besides just walking and keeping the balance, in robot-human control mode
the subject needed to focus also on the virtual scene, which shows the reference
path, and tried to initiate the turn with the particular movement of the pelvis.
852 M. Zadravec, A. Olenšek, and Z. Matjačić

Rather demanding mode is the human control mode, which is open-loop mode
without any guidance. To follow the reference walking path, in this case the
subject needs to be concentrated to the virtual scene, be more familiar with the
device, which is conditioned by a large number of training sessions, and also
capable of keeping balance at any turning point of the walking path. Another
important finding of this preliminary experiment is the correlation of the measured
biomechanical signals. At this point, it should be mentioned, that the pelvic link
support is working well, especially it gives the subject sensory information about
turning of the rotating platform. According to the results, it is evident that the
pelvis is continuously rotating while walking, but nevertheless, the mean value of
pelvic rotation is higher while turning, while during the straight walking pelvic
rotates around equilibrium point (i.e. around zero angle). Similarly, the lateral
pelvic translation is also highly correlated with the angular velocity.
The proposed system for walking and turning with pelvic support mechanism,
supported by the different training modes and different virtual scenes may be a
promising device to recover the function of walking and balance after neurological
injury, which needs to be properly investigated in the future well-controlled
clinical trials.

Acknowledgment. This preliminary study is a part of the research, which is partially


supported by the Slovenian Research Agency – the research program number P2-0228 and
the research project number L2-5471.

References
[1] Latham, N.K., Jette, D.U., Slavin, M.: Physical therapy during stroke rehabilitation for
people with different walking abilities. Arch. Phys. Med. Rehabil. 86, 41–50 (2005)
[2] Glaister, B.C., Bernantz, G.C., Klute, G.K., Orendurff, M.S.: Video task analysis of
turning during activities of daily living. Gait Posture 25, 289–294 (2007)
[3] Hornby, G., Campbell, D., Zemon, D.H., Kahn, J.H.: Clinical and quantitative
evaluation of robotic-assisted treadmill walking to retain ambulation after spinal cord
injury. Top. Spinal Cord Inj. Rehabil. 11, 1–17 (2005)
[4] Westlake, K.P., Patten, C.: Pilot study of Lokomat versus manual-assisted treadmill
training for locomotor recovery post-stroke. J. Neuroeng. Rehabil. 6, 1–11 (2009)
[5] Hussain, S., Xie, S.Q., Liu, G.: Robot assisted treadmill training: Mechanisms and
training strategies. Med. Eng. Phys. 33, 527–533 (2011)
[6] Olenšek, A., Pavčič, J., Matjačić, Z.: Comparing over ground turning and walking on
rotating treadmill. In: Proc. IFMBE 2014, vol. 41, pp. 1535–1538 (2014)
Feature Extraction APP for Pain Profiles

Shellie A. Boudreau1, Richard Spence1,2, Georgi Vasov1,2, and Line L. Egsgaard1


1
Aalborg University, Center for Sensory Motor Interaction (SMI), Department of Health
Science and Technology, Aalborg University, 9220 Denmark
{sboudreau,egsgaard}@hst.aau.dk
2
University of College of Nordjylland, Aalborg, 9000 Denmark
{rspencedk,gvasov}@gmail.com

1 Technical Field
Pain, e-Health, mobile technology, big data.

2 Business Opportunity

Project team is seeking capital investments, expertise within data mining, market
research, and clinical partners.

2.1 Current State of Technology


The feature extraction APP has been designed and developed by pain specialists
for healthcare professionals and medical institutions. The feature extraction APP
uses touch-screen technology and unique data entry tools to record pain
symptoms. Local functions are available for data capture, analytics, and
visualization.
The feature extraction APP is a gateway application for an umbrella project
known as Navigate Pain. The project is seeking commercial collaboration and
funds to continue research, development and validation of advanced feature
extraction algorithms. Investment capital is underway.
The feature extraction APP is currently restricted to select research and clinical
partners for user testing, validation and data collection.

3 Applications

• Basic and clinical research tool


• Patient management and tracking
• Patient screening, assisted referral and diagnosis

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 853
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_116, © Springer International Publishing Switzerland 2014
854 S.A. Boudreau et al.

4 Commercial Value
Pain is the primary reason for seeking medical attention and it is estimated that one
out every three households, at any given time, has a pain complaint. Pain can result
from many reasons and determining cause is often extremely difficult but
nonetheless, a firm expectation and demand placed on health care providers.
Enhanced communication will save time and money: Direct consultation time with
primary care givers and specialists is limited, and communication of pain-related
symptoms consumes a large proportion of this time. Market: Healthcare
professionals and institutions.
Tracking and Monitoring: Tracking pain-related symptoms between referrals can
accelerate diagnosis or document efficacy of the prescribed treatment (e.g.
medicine) or intervention (e.g. surgery). Market: Healthcare professionals and
institutions, University and Research-based institutions, Pharmaceutical Industry.
Addresses patient’s needs and quality of life: There is a positive psychological
impact to be gained for creating a conduit for patients to express and accurately
communicate their pain. Further, proper communication can alleviate avoidable
anxiety and stress which can worsen current pain symptoms. Market: Patient
Unknown unknowns – In development: Advanced feature extraction is used to
design patentable algorithms that identify known and new sub-types of patients
within a patient population. These distinctions will reveal novel biomarkers and
options for targeted-therapeutics. Market: Research-based institutions,
Pharmaceutical Industries
Guiding Referrals – In development: Validated feature extraction algorithms will
be applied to patient data entry and results communicated to form a basis for an
assisted referral platform for professional users (e.g. referral to a specific treatment
center, medical intervention, or specialist). Market: Healthcare professionals and
institutions, insurance corporations.

5 The Technology
The feature extraction APP is a research and clinical tool to record, extract, and
visually communicate pain symptoms. The feature extraction APP has been
inspired by gold-standard paper-based records and functions as a novel portal to
assess patient symptoms. The technology can reduce time, effort and enhance
communication between health care providers and their patients. The feature
extraction APP is currently developed on Android and functions across android
devices.

6 Intellectual Property Rights


All rights are owned by Aalborg University, Denmark.
Marsi Bionics’ Wearable Exoskeletons for the
Daily Rehabilitation of Children

Elena Garcia1,2 and Nacho Barraque2


1
Centre for Automation and Robotics,
Spanish National Research Council-Technical University of Madrid,
Madrid, Spain
2
Marsi Bionics, 28500 Arganda del Rey, Spain
{elena.garcia,nacho.barraque}@marsibionics.com

Abstract. Marsi Bionics is a startup developing wearable exoskeletons for daily


gait rehabilitation of children.

1 Technical Field

Robotics for Healthcare and Rehabilitation.

2 Business Opportunity
Marsi Bionics is looking for Investors and Research collaborations.

3 Current State of Technology


A first prototype has been tested in quadriplejia and Muscular Distrophy patients
with successful results. We are preparing for clinical trials. Our business plan is
scheduled into four phases along 5 years:
Phase 1: develop a commercial device. 200.000€ needed.
Phase 2: Enter clinical trials. Funding from public bodies is sought.
Phase 3: Marketing and commercialization: We are looking for 700.000€ of
investment to start our marketing plan.
Phase 4: Internationalization: 5 Million € investment required.

4 Applications

Rehabilitation of Neuromuscular Diseases, Cerebral Palsy, Spinal Cord Injury.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 855
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_117, © Springer International Publishing Switzerland 2014
856 E. Garcia and N. Barraque

5 Commercial Value

There are 15 million children in the world that have lost their walking ability due
to a variety of disorders: Neuromuscular diseases, cerebral palsy, spinal cord
injury, etc. Once the ambulatory ability is lost, a number of physiological
complications arise: joint spasticity, contractures, osteporosis, scoliosis, blood
circulatory problems, hip dislocation, pressure ulcers, etc. Physical rehabilitation
plays an essential role in the prevention and treatment of complications. It has
been noticed that complications show up later in children that receive treatment to
prolong ambulation (like those affected by SMA Type III). This treatment is based
on long orthoses that assist in gait training until the walking ability is finally lost.

Fig. 1 Wearable exoskeleton ATLAS 2020 (prototype)

Unfortunately at present there is no available procedure to facilitate walking to


all other children that have already lost their walking ability. Therefore it is a
current need to have a device that allows these children walk effortlessly and
so to delay related complications.
Marsi Bionics has developed a wearable exoskeleton for the physical treatment
of these children. The device is attached to their trunk and lower limbs and
provides ambulation ability.
Marsi Bionics’ Wearable Exoskeletons for the Daily Rehabilitation of Children 857

6 The Technology

Marsi Bionics develops lower-limb exoskeletons to provide mobility and


rehabilitation. Model ATLAS 2020 has the following features (see Fig. 1):
• Wearable active orthotic devices that attach to the legs and trunk of the patient
• Designed for daily use (private home and/or hospital)
• Designed to
• Reproduce a natural physiological gait with optimum number of
degrees of freedom
• Rehabilitate neuromuscular function
• Compatible with spasticity and other dynamic perturbations thanks to
a controllable-rigidity joint with embedded sensors.
• Specially designed for children

7 Intellectual Property Rights

Two devices are protected by patent:


1. Supporting Frame with mechanism for sitting down and standing up:
P201231567. PCT/ES2013/070689.
2. Controllable rigidity joint with embedded force sensor: P201330882, PCT
pending.
A Poly-fascicular, In Vitro Nerve Model for
Development and Optimization of Peripheral
Nerve Interfaces

Kristian Rauhe Harreby

Aalborg University,
Department of Health Science and Technology (HTS)
krauhe@hst.aaul.dk

Abstract. Neuroprosthetic devices are underutilized due to a lack of selective and


safe peripheral nerve interfaces. Currently used methods for evaluating new PNI
are resource demanding and do not model well the large human nerves. A new in
vitro pig nerve model is therefore developed to constitute a cheap and flexible
testing platform for testing new PNI or optimizing existing ones.

1 Technical Field

The area of neuprosthetic devices is hampered by a lack of safe and selective


peripheral nerve interfaces (PNI). An important tool for the development of new
and better PNIs is the ability to assess and quantify the effect of improvements.
Current available nerve models, however, have several drawbacks:
• Typical animal models such as cats and rats have too small nerves to
model well the large and polyfasicular human nerves
• In typical animal models the recruitment of the nerve is not assessed
directly, but indirectly via the evoked muscle responses or torque.
• Human experiments are resources demanding and typical the outcome
measures are subjective or related to one particular application.
I am therefore developing a new in vitro nerve model for the development and
optimization of PNIs in general which:
• Make it cheap to assess PNIs
• Model well the size and complexity of human nerves
• Is not application specific (any nerve can be used)
• Provide direct measures (nerve recordings) of the nerve recruitment
• Provide much more detailed information (from each nerve fascicle) about
the spatial recruitment selectivity than any of the current used in vivo
models.
• Minimizes the number of animal experiments need

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 859
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_118, © Springer International Publishing Switzerland 2014
860 K.R. Harreby

2 Collaboration Opportunity

I am currently looking for collaborators within the area of PNI development, who
could benefit from using the new model for the assessment and optimization of
PNIs.

3 Current State of Technology

The model is based on poly-fascicular nerves from farm pigs. Nerves are
explanted from euthanized pigs e.g. after non-related surgical training at our
animal facility. As nerves are extracted after pigs are euthanized, experiments are
not regarded as animal experiments.
The nerve is kept functional in an oxygenated and temperature controlled organ
bath. In one end of the nerve, the PNI which is to be tested is mounted on the
nerve / implanted in the nerve, in the other end the individual fascicles (~30 for
the median nerve) are freed and pined with custom made electrodes for recording
the evoked electrofasciculogram (EFG).
Stimulation is now performed with the PNI while the EFG is being recorded.
During offline analysis the spatial selectivity can be assessed, e.g. by calculating a
selectivity index (1)
Via previous work and local funding an experimental setup have been
established which includes: Stimulators, organ bath, amplifiers, data acquisition
equipment and custom made Matlab scripts for controlling stimulation and
recording.
During previous work with the model (2, 3), a lot of knowledge has been
gained. The maturity of the model is, however, still low and more experience is
needed to e.g.improve signal to noise quality, to map the plexiform fascicle
arrangement of the nerves and to combine structural data (histology) with the EFG
measurements.

4 Applications

The in vitro model constitute a flexible, realistic, and cheap PNI testing platform
which can provide academia and industry with detailed feedback on their PNI
innovations. Given the higher detail level which it provides, fewer experiments
will be needed compared to conventional animal models, which complies well
with the “Reduction, Refinement and Replacement” principle.

References
[1] Jensen, W., Harreby, K.R.: Selectivity of peripheral neural interfaces. In: Periferal
Nerve Interfaces, IEEE edn., IEEE (2012)
A Poly-fascicular, In Vitro Nerve Model for Development and Optimization 861

[2] Harreby, K.R., Sevcencu, C., Jensen, W.: In vitro large polyfascicular nerve model for
assessment of fascicular recruitment characteristics of peripheral nerve interfaces. In:
International Conference on Neurorehabilitation 2012, November 14-16 (2012)
[3] Ranieri, A., Andersen, R.E., Lauridsen, M.V., Harreby, K.R.: A combined
interfascicular-cuff electrode (ICE) for selective recruitment of polyfascicular
peripheral nerves using transversal stimulation. Accepted for ICNR 2014 (2014)
Control of Robotic and Prosthetic Arms
Using an Inductive Tongue Control System

Daniel Johansen1,*, Dejan B. Popovic1,2, and Lotte N.S. Andreasen Struijk1


1
Center for Sensory-Motor Interaction (SMI),
Department of Health Science and Technology,
Aalborg University, DK-9220 Aalborg, Denmark
{djoh,dbp,naja}@hst.aau.dk
2
Faculty of Electrical Engineering, University of Belgrade, Belgrade, Serbia
dbp@etf.rs

Abstract. A novel control scheme implementing an Inductive Tongue Control


System and allowing for partial or full control of robotic and prosthetic arms and
hands has been developed.
The applications of the developed control scheme include but are not limited to:
Upper limb prosthetics; Control of robotics involved in reaching and grasping and
Added control.
Proof of concept and comparative studies have been carried out using both a
computer model of a robotic hand, and a commercially available robotic/prosthetic
hand.
The possible commercial value of the technology and system is strongly linked
to the possible applications and if the use of the control scheme and the ITCS is
broadened in relation to robotics and added control, the potential commercial
value of the control scheme would increase significantly.
A patent on the described technology with application number
WO2011DK50171 was filed on the 24th of May 2011, and is currently pending in
regions under EPO.

Keywords: Prosthetics, Robotics, Control.

1 Technical Field

For the last decades the advances in robotics technology translated into the
prosthetic hand field has resulted in new commercial devices, like dexterous hands,
motorized wrists and elbows, that could potentially restore enhanced manipulation
abilities. However this new hardware requires suitable control systems and
interfaces in order to maximize its effectiveness.
A novel prosthesis control scheme implementing the Inductive Tongue Control
System (ITCS) introduced by Struijk in [1], has been developed. This control

*
Corresponding author.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 863
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_119, © Springer International Publishing Switzerland 2014
864 D. Johansen, D.B. Popovic, and L.N.S.A. Struijk

scheme allows for partial or full control of robotic and prosthetic arms and hands.
The control scheme can be implemented in combination with other control
modalities or solely through use of the ITCS.

2 Business Opportunity

Business opportunities regarding the developed control scheme using the ITCS
includes research collaboration focused on the further development and maturing of
the control scheme used in relation to control of hand and arm prosthetics, or
research collaborations focused on using the ITCS and the control scheme in the
field of robotics.
Possible collaborators would be companies in the field of advanced prosthetics
and prosthetic control schemes and/or reaching and grasping robotics.
Collaboration with companies could be started by applying for an industrial
Post.Doc. project at the Danish National Advanced Technology Foundation.

3 Current State of Technology

The ITCS control scheme has been developed and implemented on a prototype of
the ITCS. Proof of concept studies have been carried out using both a computer
model of a robotic hand, and using a commercially available robotic/prosthetic
hand. Also comparative studies using the ITCS control scheme and a standard
prosthesis control scheme for activating specific grasps/functions of a prosthesis
hand have been carried out.
Ethical approvals have been granted for experiments using amputees. But due to
lack of funding, further planning of these experiments have been put on hold.
All studies have been completed as part of an industrial Ph.D. project funded by
Bevica Innovation A/S and the Danish Agency for Science, Technology and
Innovation

4 Applications
The applications of the ITCS control scheme includes, but are not limited to:
• Upper limb prosthetic and/or environmental control
• Control of robotics involved in reaching and grasping
• Added control in tasks where hands and feet of an operator of robotics or
machinery are already in use or not available for providing control input
Control of Robotic and Prosthetic Arms Using an Inductive Tongue Control System 865

5 Commercial Value
The possible commercial value of the technology and system is strongly linked to
the possible applications of the developed control scheme and the ITCS.
The incidence of major upper limb amputations has been reported to be 0.6 per
100.000 [2]. This corresponds well to the 30-40 people that have major upper limb
amputations in Denmark every year, and in Europe this will sum up to
approximately 4500 people a year.
If the prosthesis control scheme could be implemented as a control modality in
one of the new advanced upper limb prosthesis from a major prosthesis
manufacturing company, this could possibly allow for 1800-2000 sales a year.
Furthermore if the use of the control scheme and the ITCS is broadened in
relation to robotics and added control, the potential commercial value of the control
scheme would increase significantly.

6 The Technology

The Inductive Tongue Control System introduced by Struijk in [1], is a wireless


controller that resembles a dental retainer. It comprises inductive sensors that are
hosted in the upper palatal area that can be activated using a special activation unit
pierced or glued to the tip of the tongue. The ITCS can provide the functionality of
a wireless joystick or keyboard.
The ITCS includes a mouthpiece unit (MU) and a central unit (CU). Each MU is
customized to the user and is built using a dental imprint of the upper palatal area
taken by a dentist. The MU transmit sensor information to the CU, which handles
the main part of the signal processing as well as managing the communication with
the connected devices e.g. robotic arm.

7 Intellectual Property Rights


A patent on the described technology with application number WO2011DK50171
was filed on the 24th of May 2011, and published the 1st of December 2011. The
spinoff company TKS A/S has ownership of the patent, and the patent is currently
pending in regions under EPO.

References
[1] Struijk, L.N.: An inductive tongue computer interface for control of computers and
assistive devices. IEEE Trans. Biomed. Eng. 53, 2594–2597 (2006)
[2] Davidson, J.H., Jones, L.E., Cornet, J., Cittarelli, T.: Management of the multiple limb
amputee. Disability and Rehabilitation 24(13), 688–699 (2002)
A New Device for Measuring Body Part
Movements and Stretches

Michael Skovdal Rathleff1, Line Rode1, and Ole Simonsen2


1
Department of Occupational Therapy and Physiotherapy,
Aalborg Hospital, Aalborg, Denmark
{misr,l.rode}@rn.dk
2
Orthopaedic Surgery Research Unit,
Aalborg University Hospital, Aalborg, Denmark
ohs@rn.dk

1 Technical Field
A medical device to measure hyperpronation and prevent future overuse injuries.

2 Business Opportunity

• The project is looking for investors.

3 Current State of Technology

Our group has developed a new device enabling the measurement of


hyperpronation for diagnostic, prophylactic, and therapeutic use. The device is
called the stretch-sensor.
Currently, our group is testing the technology by using a robust prototype
connected to a portable data logger that can store data from the device during a
longer period of time for later visualization. We are in the final process of testing
reliability and validity of the device for this application. Our current research
suggests that the sensor is highly valid and reliable, even among inexperienced
testers. The next step consists of clinical trials conducted in collaboration with
LaTrobe University, Melbourne, Australia and the Australian military.

4 Commercial Value

Musculoskeletal disorders cost society approximately 36 billion annually and are a


major cause of early retirement. One of them is called hyperpronation
(biomechanical problem during walking and running). Hyperpronation is
associated with an increased risk of developing pain in the knee, hip or back. The
treatment often consist of an orthotics that may reduce hyperpronation and thereby

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 867
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_120, © Springer International Publishing Switzerland 2014
868 M.S. Rathleff, L. Rode, and O. Simonsen

treat the pain. However, in a clinical setting it is difficault to measure


hyperpronation in a valid and reliable way. The stretch-sensor will help solve this
problem.
The new device will be used in daily clinical practice among physiotherapists
and medical doctors, examining hyperpronation and injury risks during work
situations and sports. In addition the new device may be used to support the
fabrication of custom made shoes and insoles to correct hyperpronation and to
follow up on the effect of these solutions.
Already existing methods are visual observation, video analysis, and pressure
measurements. Today there are no simple and cost effective solutions for the
health professional to diagnose and treat patients with hyperpronation. Therefore,
we suggest that the stretch-sensor becomes an easy-to-use tool for the health
professionals to ease the diagnosis and treatment of patients with hyperpronation.
Today, the treatment of mal-alignments such as hyperpronation consists of
training and customized insoles. The value of the treatment is measured over a
longer period of time by changes in pain level and quality of life. The treatment
will result in a healthier gait and can be measured, followed, and documented with
the help of the stretch-sensor.

5 The Technology

The stretch-sensor consists of a capacitative sensor that charges its resistance as a


function of elongation of the sensor. This enables the calculation of how much it is
being stretched. By positioning the sensor on the medial side of the foot, it enables
us to measure hyperpronation during walking, running, or other dynamic
activities. The sensor is designed to be about 1mm thin and can therefore fit in a
shoe. The signals are sent from the stretch-sensor with 200Hz to an input box that
records the data on a storage unit or transmits it directly to a computer through a
USB cable.

6 Intellectual Property Rights

A patent application has been filed in September 2011. The application has been
published in March 2013 under number WO 2013/041101. It is pending in several
countries.
Smattress: A Smart Mattress Providing an
Active Unobstructive Bedding System
Based on Musculoskeletal Modeling

Afshin Samani

Center for Sensory Motor Interaction,


Aalborg University, Aalborg East, 9220 Denmark
afsamani@hst.aau.dk

Abstract. This short note presents an established concept for design a smart
mattress using advanced musculoskeletal modeling. The mattress design aims at
decreasing the intervertebral compressive and shear force thereby decreasing
the incidence of back pain. The concept can be generalized to prevent pressure
ulcer.

1 Technical Field

A combination of biomechanics and ergonomics can be utilized to improve the


human well-being. Within this concept, the presented concept promises an
innovation in designing a smart bedding system aiming at decreasing the risk of
back pain or pressure ulcer.

2 Business Opportunity

I am looking for research collaboration with both scientific and industrial partners.

3 Current State of Technology

The general concept of the project is established and needs to be implemented. The
steps of implementation have been identified and proper approaches have been
planned.

4 Applications

The end product can be offered as a shelf product for healthy individuals and/ or it
can target hospitals and health care units. The concept can be generalized to
alleviate or prevent back pain or pressure ulcer.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 869
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_121, © Springer International Publishing Switzerland 2014
870 A. Samani

5 Commercial Value

Back pain is a common problem society, with a monthly prevalence up to 40% in


the working population. Pressure ulcer is a major problem in acute-care patients
with an incidence rate of up to 5%. There is some solid scientific evidence
suggesting that the mattress firmness play a role in triggering back pain.
Additionally, a poor adjustment of mattress firmness may result in sleep
deprivation. Thus, the end product may also be presented as a shelf product
targeting the healthy individuals.

6 The Technology

Decreasing the load of spinal vertebrae is important and may reduce the incidence
of unspecified back pain occurring at the lumbar segment of the spine. In the
current project, we aim at utilizing a musculoskeletal model to control the firmness
of a modular air mattress to minimize the intervertebral loading. First, a full body
scanning is performed and thereby a surface model of body is composed. A
musculoskeletal model of the human body is scaled and fit into the surface model.
Pressure distribution over the mattress surface is recorded. The lying posture is
identified using the pressure distribution. This information will be fed to the
musculoskeletal modeling to obtain an estimation of intervertebral forces. The air
pressure in the mattress is adjusted to minimize the estimated forces.

7 Intellectual Property Rights

There are possibilities to apply for grants from Danish and European funds if a
company is willing to engage partly in the project.
Kinect-Based Tele-rehabilitation System
for Hand Function

Daniel Simonsen*, John Hansen, Erika Geraldina Spaich,


and Ole Kæseler Andersen

Center for Sensory-Motor Interaction, Aalborg University, Denmark


dsim@hst.aau.dk

1 Technical Field
The system presented in this paper is within the field of stroke tele-rehabilitation.

2 Business Opportunity

We are looking for research collaborations and potential industrial collaborations.

3 Current State of Technology

In an ongoing study (part of a 3-year PhD project) conducted in collaboration with


a Danish rehabilitation unit, a tele-rehabilitation system is being tested on
stroke patients with hand function deficits, in order to validate the accuracy of the
system and assess its functional value. Further development and testing of the
tele-rehabilitation system will be accomplished.

4 Applications
The tele-rehabilitation system has multiple potential applications. The intended
users of the system are individuals who suffered a stroke and train in their own
home, but other users suffering from motor deficits might as well benefit from
using the system.
The tele-rehabilitation system could also be introduced in rehabilitation centres.
This could make it possible for therapists to treat multiple patients simultaneously,
as the system only requires an initial minor introduction and proper positioning of
stimulation electrodes.

*
Corresponding author.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 871
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_122, © Springer International Publishing Switzerland 2014
872 D. Simonsen et al.

5 Commercial Value
Rehabilitation of motor skills after stroke is a time demanding and expensive
healthcare effort. Patients discharged from rehabilitation centres must continue
their training at home to regain movement skills lost due to their stroke. At home,
the patient is not supervised and/or supported by a therapist, which might have a
significant impact on the potential outcome of the rehabilitation program.
Furthermore, several studies have shown that the effect of rehabilitation is largest
within the first year after stroke, which emphasizes the need for technology that can
assist and supervise patients during training in their own home.
We have designed and realised a tele-rehabilitation system for home use. The
system is based on functional electrical stimulation and is controlled by a Microsoft
Kinect sensor. Thus, the system is capable of automatically assisting the patient
during training at home while monitoring kinematics. The kinematic data could
eventually be sent online to a remote therapist for inspection. Additionally, the
settings of the system could be adjusted online by a remote therapist. Further
development of the system could include design of games that facilitate specific
movement tasks.
Introducing this system in the home of stroke patients could potentially improve
the outcome of their rehabilitation, while reducing the general healthcare costs and
saving time for both the patient and the healthcare system at the same time. This
will accommodate the expected demographic changes with an elderly society in
Europe while still improve the existing rehabilitation schemes.

6 The Technology

The tele-rehabilitation system is based on electrical stimulation and is controlled in


a closed loop by a Microsoft Kinect sensor. By applying electrical stimulation via
skin surface electrodes to the forearm muscles of the user it is possible to assist
training of hand functions. In contrast to existing FES-based rehabilitation systems,
this system does not require direct user input (e.g. pushing a button) to trigger the
FES. In the current system the images captured by the Kinect sensor are used for
controlling proper triggering of FES in a closed loop to assist the user in both
hand opening and grasping. Besides being used for FES control, the images
captured by the Kinect camera can be used for kinematic analysis of the hand
movements.
A New Method to Diagnose Neuromuscular
Disorders in the Neck-Shoulder Region

Steffen Vangsgaard, Ernst Albin Hansen, and Pascal Madeleine

Center for Sensory-Motor Interaction (SMI),


Department of Health Science and Technology,
Aalborg University, Fredrik Bajers Vej 7, DK-9220 Aalborg, Denmark
{sv,eah,pm}@hst.aau.dk

1 Technical Field

The H-reflex is often used in the clinic as a tool to test for cervical radiculopathy or
other neurologic disorders. Additionally, it is often used experimentally to
investigate neural changes at a segmental level following an intervention
(e.g. strength training) (1). Methods for recording H-reflexes in the soleus and
tibialis anterior muscles have been thoroughly tested. However, only few studies
have assessed H-reflexes of the upper extremity (2).
The trapezius muscle is considered one of the most important muscles of the
neck-shoulder region, and is often involved in musculoskeletal disorders. Its motor
and sensory innervation is supplied by the accessory nerve and the C3/4 cervical
nerves, respectively. Thus, it is possible to evoke H-reflexes in the trapezius muscle
with minimal influence of M-waves (3,4).

2 Business Opportunity
Clinical research collaboration is warranted to investigate the trapezius muscle H-
reflex on a patient population (e.g. with shoulder impingement syndrome or
cervical radiculopathy).

3 Current State of Technology


Studies have been performed on healthy subjects in order to investigate the changes
in the trapezius muscle H reflex following strength training and in the presence of
muscle soreness and pain (3,4). Furthermore, the reliability of the method has been
investigated and found to be good (unpublished). The next step will be to perform
studies involving patients with neck-shoulder disorders.

4 Applications
The ability to evoke an H-reflex in the trapezius muscle allows researchers and
clinicians to assess neurologic changes at the C4 level of the spinal cord.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 873
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_123, © Springer International Publishing Switzerland 2014
874 S. Vangsgaard, E.A. Hansen, and P. Madeleine

Furthermore, measures of the trapezius muscle H-reflex could potentially be used


to monitor the efficiency of a rehabilitation program targeting the neck-shoulder
region.

5 Commercial Value

Shoulder and neck pain are reported in about 23% of the workers in European
countries and the costs have been estimated to be between 0.5% and 2% of Gross
National Product (GNP) (5). Thus, better diagnostic methods and therapeutic
strategies are needed.

6 The Technology

H-reflexes are evoked in the trapezius muscle by electrical stimulation of the C3/4
cervical nerves; M-waves are evoked by electrical stimulation of the accessory
nerve (see Figure 1).

Fig. 1 The area searched to find the location for the cathode used to stimulate the accessory
nerve is indicated by the dark area, and that for the cervical nerves of C3/4 is indicated by
the light area. Examples of cathode placements are marked with black dots inside the search
areas. The figure is adapted from (4).

References
1. Misiaszek, J.E.: The H-reflex as a tool in neurophysiology: Its limitations and uses in
understanding nervous system function. Muscle Nerve 28(2), 144–160 (2003)
2. Palmieri, R.M., Ingersoll, C.D., Hoffman, M.A.: The Hoffmann reflex: methodologic
considerations and applications for use in sports medicine and athletic training research.
Journal of Athletic Training 39(3), 268 (2004)
3. Vangsgaard, S., Nørgaard, L.T., Flaskager, B.K., Søgaard, K., Taylor, J.L., Madeleine,
P.: Eccentric exercise inhibits the H reflex in the middle part of the trapezius muscle.
Eur. J. Appl. Physiol. 113(1), 77–87 (2013)
A New Method to Diagnose Neuromuscular Disorders in the Neck-Shoulder Region 875

4. Vangsgaard, S., Nørgaard, L., Madeleine, P., Taylor, J.L.: Crossed Responses Found in
Human Trapezius Muscles are not H-Reflexes. Muscle Nerve 49, 362–369 (2014)
5. Schneider, E., Irastorza, X., Copsey, S., Verjans, M., Eeckelaert, L., Broeck, V.: OSH in
figures: Work-related musculoskeletal disorders in the EU—Facts and figures. In:
Luxembourg: European Agency for Safety and Health at Work 2010 (2010)
How to Turn an Idea into a Commercial Success

Peter Mørch Eriksen

BioPorto A/S, Hellerup, Denmark


and
Chairman MTIC and Advisory Board Member at Lund University

There are a number of obstacles for most ideas and startups why only a few of
them turn into success stories. One of the major obstacles is how to get the
necessary funding for the development of the first proto type. Having achieved
this, however, the road to commercial success for a product is still long and full of
pitfalls.
The presentation draws upon experience from the last 20 years in funding,
bringing products to markets and creating commercial success and will touch upon
success stories as well as failures. The presentation will also include other aspects
such as how the big industry is looking at potential acquisitions and development
to illustrate different entry and exit points.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 877
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_124, © Springer International Publishing Switzerland 2014
Industrial Perspectives on Innovation within
Neurorehabilitation between Private and Public
Partners

Bernhard Graimann

Translational Research and Knowledge Management,


Otto Bock HealthCare GmbH, Duderstadt, Germany

Academic research institutions produce a large amount of interesting research


results. Results that could lead to innovative products, services or processes.
However, very often the industry cannot just take such a result and develop an
innovation out of it. The gap between academic achievement and the point a
company can take over with a reasonable risk is usually large. This gap can be
reduced or even eliminated by setting up a research collaboration between
academia and industry which fosters knowledge transfer. Knowledge transfer from
academia to industry and from industry to academia. In this talk, I will present
examples of such collaborations together with best practices and lessons learned.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 879
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_125, © Springer International Publishing Switzerland 2014
Reflex-Based Electrical Therapy:
A Novel Method for Gait Rehabilitation

Kristian Hennings

Nordic NeuroSTIM ApS, Vejle, Denmark

Reaching the point of being able to walk is an important first goal for a majority of
stroke patients, and is a focus area for the Integrative Neuroscience Group headed
by Ole. K. Andersen at Center for Sensory-Motor Interaction. Over the past 10
years, they have been developing a novel method termed Reflex-based electrical
therapy that utilizes the nociceptive withdrawal reflex to assist the patients in
regaining the ability to walk after a stroke. In this talk, I will give an introduction
to this method and how it was brought out of academia and into a spinout
company.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 881
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_126, © Springer International Publishing Switzerland 2014
The MedTech Industry at a Glance:
Solving Tomorrow’s Healthcare Challenges

Louise Feilberg

European Affairs, Coloplast A/S, Humlebæk, Denmark


Board Member Eucomed and Medicoindustrien (Danish MedTech Association)

The MedTech Industry is playing an increasingly important role in solving


tomorrow’s healthcare challenges. Today, more than 500,000 medical
technologies are available to healthcare professionals, the MedTech industry
employs 500.000 people in Europe, and it grows more than 5% per year.
The industry continues to grow and thus continues to contribute to solving the
healthcare challenges. However, there are challenges ahead. Regulatory burdens
are increasing. Ageing societies with more people needing care means healthcare
budgets are under pressure – how does that impact the industry? how can the
MedTech industry continue to develop products to fit the needs of patient and
professionals whilst keeping up innovating new products at a fast pace?

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 883
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_127, © Springer International Publishing Switzerland 2014
Transferring Rehabilitation Technology
to Markets: Lessons Learned in the
Past Ten Years

Zlatko Matjačić

Biomechanics, Head of R&D, University Rehabilitation Institute, Ljubljana, Slovenia


NeuroReTrain ApS, Aalborg, Denmark

Ageing societies demand efficient rehabilitation technologies that would increase


the productivity of rehabilitation of movement disorders while at the same time
decreasing the number of clinical staff. This would appear as a perfect opportunity
for related industry, however, one needs to note that the market for rehabilitation
devices is fragmented, segmented and often fall under regulatory constraints of
each individual country. Therefore, ideas for new devices often also require
creation of a new market for a particular device. This means that time-to-market is
rather long representing a substantial financial burden, which also makes a process
of transferring new ideas into products through either establishing a spin-off
company or setting-up a licensing agreement rather unique in each particular case.
In this talk our experience on developing rehabilitation devices for balancing
during standing and walking as well as for training sit-to-stand maneuvers and
movement of upper extremities and transferring them to markets will be presented.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 885
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_128, © Springer International Publishing Switzerland 2014
Translational Research on Tongue Control
Interface

Gert Spender1 and Lotte N.S. Andreasen Struijk2


1
TKS A/S, Aalborg, Denmark
2
Center for Sensory-Motor Interaction,
Department of Health Science and Technology, Aalborg University
Aalborg, Denmark

Advanced computer input devices are important for severely disabled people
suffering from e.g. tetraplegia. An example of such a computer interface is the
inductive tongue computer interface which has been developed from research at
Center for Sensory-Motor Interaction Aalborg University. The interface consist of
an intraoral keyboard and a mouse pad, which is operated by the tongue, and is
used to control computers, wheelchairs, tablets, etc. In this talk we will give an
introduction to the method and describe the challenges and experiences from the
process of translating an idea into a product - starting from the research performed
at the university, the establishment of the related spin off company TKS A/S, the
CE-marking process, and the marketing aspects of the end product: iTongue which
was CE-certified in 2013.

W. Jensen et al. (eds.), Replace, Repair, Restore, Relieve – Bridging Clinical 887
and Engineering Solutions in Neurorehabilitation, Biosystems & Biorobotics 7,
DOI: 10.1007/978-3-319-08072-7_129, © Springer International Publishing Switzerland 2014
Author Index

Al-Angari, Haitham M. 227 Bergamasco, Massimo 637


Aleixandre, Manuel 295 Bermejo-Pareja, Félix 373
Alguacil, Isabela 437 Bieńkiewicz, Marta M.N. 289, 393, 629
Aliakbaryhosseinabadi, Susan 237 Birgit Larsen, P.T. 49, 725
Allan, David B. 823 Bischof, Birgit 775
Alnajjar, Fady S. 245 Biurrun Manresa, José Alberto 271
Amirabdollahian, Farshid 665 Blicher, Jakob Udby 23
Andersen, Ole Kæseler 165, 255, 271, Bøg, Mette F. 751
421, 741, 751, 871 Borghese, Nunzio Alberto 129
Andersen, Rasmus Elbæk 685 Boudreau, Shellie A. 853
Andersen, Tina K. 465 Brånemark, Rickard 25
Andreu, David 513 Bravo-Esteban, Elisabeth 295
Anson, J. Greg 789 Buurke, Jaap H. 665
Aoki, Kanta 149
Aoki, Yoshitaka 83 Casali, Carlo 709
Aoustin, Yannick 303 Cesario, Alfredo 665
Archambault, Philippe S. 263 Chou, Li-Wei 493
Arendt-Nielsen, Lars 103 Chung-Lan, Kao 621
Arguissain, Federico Gabriel 271 Cincotti, Febo 563
Arredondo, Maria Teresa 629 Cipriani, Christian 227
Aszmann, Oskar C. 51, 169, 775 Cogollor, Jose Maria 629
Azorín, José María 321, 647, 655, 795 Colombo, Roberto 313
Conte, Carmela 709
Baad-Hansen, L. 47 Conway, Bernie 823
Barraque, Nacho 855 Coscia, Martina 637
Barroso, Filipe 601 Costa, Álvaro 321, 647, 655
Barss, Trevor S. 219, 279, 479 Crocher, Vincent 329
Beattie, Simone 479 Cullen, Kathryn 405
Becerra-Fajardo, Laura 447 Cusmano, Ivana 313
Behrens, S.M. 187
Benito-León, Julián 373 Dambreville, Charline 29
Bentsen, Bo 521 D’Antonio, Erika 569
Bera, Rossana 369 Da Rocha-Souto, Bibiana 695
Berenz, Vincent 245 de Brito Silva, Priscila 103
890 Author Index

del-Ama, Antonio J. 341, 601 Grey, Kurt 725


del Castillo, M. Dolores 437 Guger, Christoph 507
Delconte, Carmen 313 Guiraud, David 513
de los Reyes-Guzmán, Ana 601 Gulde, Philipp 289, 393
Dideriksen, Jakob Lund 351, 373
Dobsak, Petr 487 Haase, Jens Peter 403
Dong, Nhung P.T. 465 Haavik, Heidi 35, 113, 121
Dosen, Strahinja 351, 383 Hadidi, Niloufar Niakosari 405
Draicchio, Francesco 709 Hahn, Marie 51
Dremstrup, Kim 121, 237, 465, 701 Hansen, Ernst Albin 873
Duehr, Jens 35 Hansen, John 741, 871
Duehra, Jens 121 Hansen, Mia H. 411
Hansen, Nicolas B. 473, 759
Egsgaard, Line L. 853 Harreby, Kristian Rauhe 457, 529, 685,
Erber, Stefan 361 859
Eriksen, Peter Mørch 877 Hasan, Muhammad A. 823
Erkocevic, Ema 751 Haugland, Morten 403
Hayashibe, Mitsuhiro 513
Farina, Dario 237, 303, 351, 373, 383,
Hennings, Kristian 421, 881
465, 575, 701, 813
Herceg, Malvina 169, 775
Feilberg, Louise 883
Hermsdörfer, Joachim 289, 393, 629
Ferrazzoli, Davide 369
Higashi, Toshio 93
Ferre, Manuel 393
Ho, Yi-Ching Lynn 23
Fialka-Moser, Veronika 169, 775
Holobar, Ales 373
Fjorback, Morten 543
Honeycutt, Claire F. 431
Flor, Herta 1
Hortal, Enrique 321, 655, 795
Fong, Justin 329
Hughes, Charmayne 393
Frahm, Ken Steffen 585
Hundza, Sandra R. 255
Fraser, Matthew 823
Frazzitta, Giuseppe 369 Hurteau, Marie-France 29
Frigon, Alain 29
Frisoli, Antonio 637 Iáñez, Eduardo 321, 647, 655
Fujiie, Kaoru 149 Ibáñez, Jaime 437
Iosa, Marco 563, 569, 781
Gaihede, Michael 521 Irani, Ramin 741
Gallego, Juan Álvaro 373 Ishikawa, Ryo 93
Ganeswarathas, Sahana 529 Ishimatsu, Takakazu 93
Garcia, Elena 855 Iso, Naoki 93
Gargantini, Roberto 369 Ivorra, Antoni 447
Gee, Nan 169 Izquierdo, Mikel 537, 553
Geertsen, Svend S. 765
Genna, Clara 383 Jappe, Leah 405
Gervasio, Sabata 421, 575 Jean-Baptiste, Emilie 629
Gil-Agudo, Ángel 341, 601 Jensen, J. 47
Glackin, Cornelius 139 Jensen, Winnie 457, 591
Göbel, Peter 169 Jiang, Ning 237, 465, 701
Goebel, Peter Michael 361 Jiao, Jianhang 457
Gómez, Marisol 537, 553 Jochumsen, Mads 121, 411, 465
Gómez-Soriano, Julio 295 Johansen, Daniel 863
Graimann, Bernhard 383, 879 Johansen-Berg, Heidi 23
Author Index 891

Jørgensen, Martin G. 473, 759 Li-Wei, Chou 621


Juhl, Anne 725 Loadman, Pamela M. 255
Jung, Ranu 529 Lontis, Eugen Romulus 521
Lontis, Romulus 237, 701
Kairy, Dahlia 263 Luft, Andreas 63
Kamavuako, Ernest N. 411 Lykholt, Line E. 529
Kanitz, Gunter 227
Kao, Chung-Lan 493 Madeleine, Pascal 873
Kassebaum, Eric 411 Maehle, Erik 833
Katamoto, Ryuji 149 Maestri, Roberto 369
Kaupp, Chelsea 219, 479 Mainetti, Renato 129
Ken-ichi, Ozaki 245 Makihara, Yukiko 103
Kern, Nora 695 Mandl, Thomas 361
Kersten, Stefanie M. 675 Männel, Georg 833
Kersting, Uwe G. 103 Marchal-Crespo, Laura 65
Kihara, Yoshimitsu 149 Marcheschi, Simone 637
Kinget, Mat 35 Mari, Silvia 709
Kingett, Mat 121 Marinozzi, Franco 569
Kirk, Eileen M. 195 Martínez-Ramírez, Alicia 537, 553
Kjaersgaard, A. 47 Martinikorena, Ion 537
Klaic, Marlena 329 Masiero, Stefano 569
Klamroth-Marganska, Verena 39 Matjačić, Zlatko 75, 845, 885
Klarner, Taryn 219, 279, 479 Mazzone, Alessandra 313
Klimstra, Marc 255 Meei-I, Lai 621
Kolarova, Jana 487 Meier, Kaare 81
Komiyama, Tomoyoshi 219 Meijs, Suzan 543
Kondo, Izumi 245 Mei-Wun, Tsai 621
Koopman, Bram 187 Meuleman, Jos 187
Kothari, M. 47 Mezzarane, Rinaldo A. 219
Kotova, Marketa 487 Miangolarra-Page, J. 437
Koutsou, Aikaterini D. 795 Micera, Silvestro 637
Kuczynski, Victoria 29 Millor, Nora 537, 553
Kudo, Seiya 93 Mørch, Carsten Dahl 117, 271, 585
Kuo, Min-Fang 3 Moeslund, Thomas B. 501, 741
Molina, Francisco 437
Lai, Meei-I 493 Molinari, Marco 563, 569, 781
Lanzi, Pier Luca 129 Mondino, C. 159
Larsen, Jeppe V. 501 Monge, Esther 437
Lauridsen, Mette Vandborg 685 Monsifrot, Jonathan 303
Lawn, Murray J. 93 Moreno, Juan C. 341, 563
Le Carpentier, Eric 303 Morita, Yoshifumi 83
Lechner, Alexander 507 Moromugi, Shunji 93
Lecumberri, Pablo 537, 553 Morone, Giovanni 563, 569
Lee, Yong-Kwun 149 Mountain, Gail 665
Levin, Mindy F. 263 Mrachacz-Kersting, Natalie 103, 237,
Lewis, Sören 51 465, 575, 701, 765
Li, Zhan 513 Muceli, Silvia 351
Li-Ling, Pan 621 Müller-Putz, Gernot R. 611
Lindeløv, Jonas 61 Münte, Thomas 833
892 Author Index

Murakami, Koji 149 Poli, Patrizia 569


Murphy, Bernadette 113 Pons, José Luis 295, 341, 373, 437, 563,
Muzzioli, Luca 563 601, 795
Popovic, Dejan B. 863
Næss-Schmidt, Erhard 23 Popović, Mirjana 701
Nagao, Toru 83 Prange, Gerdienke B. 665, 675
Nakajima, Tsuyoshi 219 Purva Sharma, F.A. 735
Nasr, Nasrin 665
Nasrollahi, Kamal 741 Raai, Mark van 65
Near, Jamie 23 Ranavolo, Alberto 709
Niazi, Imran Khan 35, 121, 465 Ranieri, Alessandro 685
Nielsen, Gebbie A.R. 465 Rathleff, Michael Skovdal 867
Nielsen, Jens B. 765 Rauter, Georg 39, 65
Nielsen, Jørgen Feldbæk 23, 47, 751 Rechendorff, Kristian 543
Nielsen, Rasmus Kragh 591 Reenalda, Jasper 191
Nielsen, Thomas Nørgaard 717 Reggiani, Monica 813
Nijenhuis, Sharon M. 665, 675 Resquín, Francisco 795
Nitsche, Michael A. 3 Riberholt, Christian Gunge 137
Norouzi, Nahid Gheidari 263 Riener, Robert 39, 65
Rietman, J.S. 675
Østergaard, Leif 23
Rigosa, Jacopo 227
Oetomo, Denny 329
Rijkhoff, Nico J.M. 543
Ofner, Patrick 611
Ristić-Durrant, Danijela 139
Ohno, Kensuke 245
Rivas, Francisco 437
Olenšek, Andrej 75, 845
Roas, Gianluca 637
Ooso, Shirou 93
Oppel, L. 725 Roche, Aidan 169
Ortner, Rupert 507 Rocon, Eduardo 373
Overholt, Dan 501 Rode, Line 867
Rodríguez-López, Carlos 695
Pan, Li-Ling 493 Rojo, Javier 629
Paolucci, Stefano 563, 569 Romero, Juan Pablo 373
Paredes, Liliana 383 Rotshtein, Pia 629
Parekh, Manish 393 Rovsing, Cecilie 465
Pastorino, Matteo 629 Rovsing, Helene 465
Paulus, Walter 3 Russel, Martin 393
Perez, Alberto L.R. 473, 759 Russold, Michael 51
Pérez-Nombela, Soraya 601
Perini, Gloria 369 Sakaki, Taisuke 149
Perreault, Eric J. 431 Sale, Patrizio 665
Petersen, Tue Hvass 127 Salsedo, Fabio 637
Pezzoli, Gianni 369 Samani, Afshin 869
Pflügler, Johannes 629 Sandrini, Giorgio 159, 709
Pierelli, Francesco 709 Sartori, Massimo 813
Pirondini, Elvira 637 Sato, Noritaka 83
Pirovano, Michele 129 Savić, Andrej 701
Pisano, Fabrizio 313 Savik, Kay 405
Pisotta, Iolanda 563 Schachinger, Markus 361
Planelles, Daniel 647, 655, 795 Schlegel, Andrea 289, 629
Plocharska, Marlena A. 411 Schweikard, Achim 833
Author Index 893

Scivoletto, Giorgio 781 Taylor, Denise 789


Sebik, Oğuz 35 Taylor, Julian 295
Serrano, J. Ignacio 437 Telonio, Alessandro 29
Serrao, Mariano 161, 709 Thakor, Nitish V. 15
Sevcencu, Cristian 457, 717 Thibaudier, Yann 29
Severinsen, Kaare 725 Thomas, Evan 255
Shimoda, Shingo 245 Thompson, Aiko K. 179
Shirotani, Takeaki 93 Thota, Anil K. 529
Shun-Hwa, Wei 621 Torricelli, Diego 295, 601
Simon-Martínez, Cristina 295 Tresch, Ursina A. 431
Simonsen, Daniel 741, 871 Tsai, Mei-Wun 493
Simonsen, Ole 867 Tsuruta, Kazuhiro 149
Sinkjær, Thomas 103, 403, 575, 765 Türker, Kemal S. 35
Slavnić, Siniša 139 Turolla, Andrea 383
Smidstrup, Anne 751
Sørensen, Marina E. 465 Úbeda, Andrés 321, 647, 795
Soerensen, Preben 725 Ugincius, Paulius 35
Sørensen, Søren 543 Ukai, Hiroyuki 83
Solomon, John M. 263 Ushimi, Nobuhiro 149
Soriano, Julio Gómez 601
Spaich, Erika Geraldina 165, 421, 473, van Asseldonk, Edwin H.F. 187, 805
741, 751, 759, 871 van der Kooij, Herman 187
Vangsgaard, Steffen 873
Spence, Richard 853
van Meulen, Fokke B. 191
Spender, Gert 887
van Oort, Gijs 187
Spina, Letizia 369
van Voort, H. Carsten 187
Stagg, Charlotte J. 23
Vasov, Georgi 853
Sterpi, Irma 313
Vasudevan, Erin V. 195
Stevenson, Andrew J.T. 765
Veltink, Peter H. 191
Stieglitz, Thomas 9
Veneman, Jan F. 203
Stienen, Arno H.A. 675
Vera-Portocarrero, Louis 135, 585
Struijk, Johannes J. 717
Vivian, Michele 813
Struijk, Lotte N.S. Andreasen 521, 863,
Vuckovic, Aleksandra 237, 823
887
Sturma, Agnes 169, 775 Wei, Shun-Hwa 493
Sugyo, Atsushi 149 Weiss, Patrick 833
Sun, Yao 219, 479 Wing, Alan 393
Svensson, P. 47 Wolf, Peter 65
Wolpaw, Jonathan R. 209
Tagliapietra, Luca 813
Takagi, Yoshiaki 83 Yamada, Hitoshi 245
Tamburella, Federica 563, 781 Yash Jobanputra, S.B. 735
Tan, Ying 329 Yılmaz, Gizem 35
Tanabe, Hirofumi 83
Tanemura, Rumi 83 Zadravec, Matjaž 75, 845
Tarantino, Sergio 227 Zalud, Ludek 487
Tateishi, Kenji 149 Zehr, E. Paul 219, 255, 279, 479

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