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DOI 10.

1007/s11055-018-0668-3
Neuroscience and Behavioral Physiology, Vol. 48, No. 9, November, 2018

Use of Robotic Devices in Post-Stroke Rehabilitation

A. A. Frolov,1,2 I. B. Kozlovskaya,3
E. V. Biryukova,1,2 and P. D. Bobrov1,2 UDC 612.821

Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 67, No. 4, pp. 394–413,
July–August, 2017. Original article submitted March 3, 2017. Accepted May 3, 2017.

This review addresses the use of robotic devices in the rehabilitation of poststroke and posttrauma patients
as a rehabilitation technology which has developed rapidly over the last decade. The types of devices used
are described – manipulators and exoskeletons – along with the clinical protocols for their use and the ef-
fectiveness of rehabilitation procedures. Particular attention is paid to the neurophysiological basis of the
rehabilitation potential of this technology, including analysis of measures of plastic rearrangements of the
brain. Results obtained from state-of-the-art rehabilitation technology using hand exoskeletons controlled
by brain–computer interfaces based on kinesthetic motor imagery are considered.
Keywords: neurorehabilitation, stroke, robotic devices, brain–computer interface.

Introduction. Robotic devices driving human limb on the neuroplasticity of the brain [Nudo et al., 1996; Taub
movements in response to biological signals are increas- et al., 2002; Bach-Y-Rita, 2001]. The studies reported by
ingly being introduced into clinical practice. Two types of Nudo et al. [1996] using monkeys with experimental stroke
application for these devices can be discriminated – social demonstrated the efficacy of restoring MF depending on
rehabilitation and neurorehabilitation. Social rehabilitation the intensity and repetition of the goal-directed movements.
aims to involve the person in everyday life, including self- Taub et al. [2002] presented results obtained by restriction
care at home, and in interactions with people and various therapy – stimulation of the targeted repeated movements of
appliances. Social rehabilitation makes use of prostheses the afflicted limb by restricting the movements of the intact
and manipulators supporting the main daily needs. The aims limb. Bach-Y-Rita [2001] summarized the physiological
of these devices are to substitute for rather than to restore grounds for motivated, functionally significant active train-
losts motor functions. ing allowing progression from compensation of MF to its
In contrast to social rehabilitation, neurorehabilitation restoration. Long before the principles neurorehabilitation
aims to restore motor functions lost after stroke or brain in- based on brain plasticity were formulated, functionally sig-
jury [Chernikova, 2016]. Tools and approaches to motor re- nificant movements were used for motor rehabilitation on
habilitation include therapeutic physical exercise, massage, another theoretical basis – switching of the nervous system
and physiotherapy – which have long remained limited and levels at which movements are constructed using changes
insufficiently effective. The situation changed dramatical- in the sense of the motor task [Leont’ev and Zaporozhets,
ly at the turn of the century as a result of the formulation 1945; Bernshtein, 1947]. The main hypothesis underlying
of the principles of neurorehabilitation, which are based both approaches is that functional plasticity comes from the
structural plasticity of the brain.
The following neurorehabilitation principles were for-
1 Institute of Higher Nervous Activity and Neurophysiology, mulated on the basis of these theoretical grounds:
Russian Academy of Sciences, Moscow, Russia;
– active involvement of the patient in rehabilitation
e-mail: ebiryukova@mail.ru.
2 Pirogov Russian National Research Medical University, procedures;
Moscow, Russia. – goal-directed training to movements which are func-
3 Institute of Medical-Biological Problems, Russian Academy tionally significant for the patient;
of Sciences, Moscow, Russia. – intensity and regulatory of sessions.

1053
0097-0549/18/4809-1053 ©2018 Springer Science+Business Media, LLC
1054 Frolov, Kozlovskaya, Biryukova, and Bobrov

Fig. 1. Exoskeletons produced in Russia: A) Z-hand driven by pneumatic muscles. Made by Neurobotics, Zelenograd. B) Pianist hand exoskeleton driven by
electric motors. Made by NPO Android Technics, Magnitogorsk. C) Arm exoskeleton with seven degrees of freedom (flexion-extension and abduction-ad-
duction of wrist, flexion-extension and pronation-supination of forearm, flexion-extension, abduction-adduction, and rotation relative to long axis at the
shoulder joint) driven by electric motors. Made by NPO Android Technics, Magnitogorsk.

Rehabilitation programs using robotic devices pro- these methods in both healthy subjects and patients under-
vides ideal realization of these principles. Firstly, these going training to control a BCI are presented;
devices produce many repetitions of movements at a con- 3. Clinical data demonstrating the effectiveness of pro-
trolled speed, “without producing fatigue,” in contrast to cedures using hand exoskeletons controlled by BCI for res-
work with medical staff. Secondly, the repertoire of move- toration of MF in poststroke patients are presented.
ments most appropriate to the individual characteristics of Robotic Devices Used in Neurorehabilitation
the patient can be selected [Wolbrecht et al., 2006]. Robot 1. Types of robotic devices. Robotic devices currently
devices are fitted with sensors detecting the kinetic and used in neurorehabilitation can be divided into two groups
force parameters of movements, providing feedback and – manipulators and exoskeletons. Manipulators are attached
objective evaluation of movement parameters [Reiner et only to the distal part of the arm – the hand or fingers. As a
al., 2005]. Feedback based on detection of movement pa- rule, the patient holds the handle of the manipulator, which
rameters allows a virtual environment to be generated on a carries out some movement or other. Thus, a manipulator
computer which is either near-real or includes gaming com- controls the operating point of the hand but not its individual
ponents, which increases motivation to take part in rehabil- joints. In cases of severe movement disorders, movements at
itation [Jack et al., 2001]. the arm joints follow the hand passively, decreasing rehabil-
As a rule, the use of robotic systems requires some itation effectiveness [Marchal-Crespo and Reinkensmeyer,
preserved movements. If a movement is completely absent 2009]. In cases of moderate motor disorders, when there is
(plegia) or is too minimal, the only means of activating the persistence, perhaps to a limited extent, of a) the ability of
plastic mechanisms of the brain for rehabilitation consists the hand to hold the handle and b) movement at the elbow
of kinesthetic motor imagery. Motor imagery is known to and shoulder joints, manipulators can operate in assistance
activate essentially the same areas of the brain as execution mode using the residual muscle activity.
of movements [Jeannerod and Frak, 1999]. Signals relating Exoskeletons directly controlling movements at the
to the activity of these areas during motor imagery can be joints of the arm constitute a more physiologically appro-
transformed into commands controlling robotic systems via priate means of rehabilitation than manipulators, at least for
a BCI. Systematic controlled studies of the effectiveness of severe motor disorders. However, active exoskeletons are
rehabilitation procedures using robotic systems controlled much more complex technical devices than manipulators:
by BCI started to be undertaken about ten years ago, but are the exoskeleton structure must adapt to the anatomical pe-
still few in number [Buch et al., 2008; Ang et al., 2014, 2015; culiarities of the patient’s arm – the lengths of the segments
Ramos-Murguialday et al., 2013; Ono et al., 2014; Kotov et and the positions of the axes of rotation of the joints; control
al., 2014; Mokienko et al., 2016; Frolov et al., 2016a]. of torque must be concordant with the viscoelastic proper-
In the present article: ties of the neuromuscular apparatus.
1. Robotic systems used in neurorehabilitation are Manipulators for neurorehabilitation started to be de-
reviewed; veloped at the end of the 1990s, some 10 years earlier than
2. Methods for analysis of plastic rearrangements of exoskeletons. There are now commercial versions active-
the brain are described and some results obtained using ly used in poststroke rehabilitation – InMotion ARM and
Use of Robotic Devices in Post-Stroke Rehabilitation 1055

TABLE 1. Manipulators for Motor Recovery of Arm Movements Tested in Controlled Clinical Trials (F-E – flexion-extension, Ab-Ad – abduction-adduction,
P-S – pronation-supination, Rot – rotation about the longitudinal axis)

Description, clinical
Developer Country Manipulator actions Arm joints
application
Interactive Motions [Ang et al., 2011,
MIT-Manus Damps deviations from speci- Shoulder, elbow (move-
Technologies USA, USA 2015; Krebs et al.,
(InMotion ARM) fied trajectory ment in specified plane)
Watertown, MA 1998]
T-WREX (Therapy National Institute of
Assistance mode in computer Shoulder (F-E, Ab-Ad,
Wilmington Robotic Disability and USA [Sanchez et al., 2004]
games Rot), elbow (F-E)
Exoskeleton) Rehabilitation Research
MIME (Mirror Shoulder, elbow (rectilin-
The Catholic University Reproduces trajectory of
Image Movement USA [Lum et al., 2006] ear movements of forearm
of America healthy arm for paretic arm
Enabler) in different directions)
Reha-Stim Medtec GmbH Active and passive bimanual Elbow (P-S), radiocarpal
Bi-Manu-Track Germany [Hesse et al., 2003]
& Co. KG modes (F-E)
NeReBot
Recording and reproduction of
(NEuro- Shoulder (Ab-Ad), elbow
Padua University Italy [Rosati et al., 2007] arm trajectory recommended
REhabilitation- (F-E, P-S)
by rehabilitation physician
RoBOT)
Execution of a large repertoire
of slow movements at constant Shoulder (Ab-Ad, F-E,
REHAROB European project – REHAROB [Fazekas et al., 2006] speed to increase movement Rot), elbow (Ab-Ad, F-E),
amplitude and decrease joint radiocarpal (Ab-Ad, F-E)
spasticity
Shoulder (Ab-Ad, F-E),
[Amirabdollahian Operates in three modes: pas-
Haptic Master European project – Gentle/G elbow (F-E, P-S), radiocar-
et al., 2007] sive, assistance, and active
pal (F-E)
MEMOS
Assistance mode in the process
(MEchatronic system Scuola Superiore Shoulder (Ab-Ad, F-E),
Italy [Micera et al., 2005] of moving the patient’s arm to
for MOtor recovery Saint’Anna in Pisa elbow (F-E)
a specified target
after Stroke)
Assistance mode in the process
Rehabilitation Institute of [Reikensmeyer et al., Shoulder (F-E), elbow
ARM Guide USA of moving the patient’s arm to
Chicago 2000] (F-E)
a specified target

ArmeoSpring, based, respectively, on the original devel- slender tendons running into the hand [Sinel’nikov, 1967].
opments MIT-Manus and T-WREX (Table 1). Along with Thus, an artificial pair of antagonistic muscles located out-
MIT-Manus and T-WREX, Table 1 shows other manipula- side the fingers can provide anatomically appropriate control
tors which have been used in controlled clinical trials. of flexion-extension of the fingers using a mobile exoskele-
The development of exoskeletons over the last 10 years ton attached to the distal phalanges (Fig. 1).
has run at such a high rate that the number is currently com- Most exoskeletons are at the prototype stage and have
parable with the number of manipulators developed. For ex- been approved only in healthy subjects [Bos et al., 2016; Heo
ample, a detailed review [Maciejasz et al., 2014] listed 44 et al., 2012]. However, exoskeleton constructions for post-
manipulators and 35 exoskeletons intended for poststroke stroke patients have much more stringent requirements than
rehabilitation. Most exoskeletons have been developed for those for healthy subjects. These restrictions are mainly as-
the hand. There are at least two reasons for this. First, the sociated with arm and hand spasticity, which hinders attach-
hand and fingers have the greatest level of impairment after ment to the exoskeleton. Exoskeletons tested on poststroke
stroke and recovery of their movements is prolonged and dif- patients are shown in Table 2 (hand) and Table 3 (arm).
ficult [Shelton and Reding, 23001]. Second, the arrangement A total of three hand exoskeletons – HWARD, Reha-
of the muscular apparatus of the fingers can be reproduced Digit, and Hand Mentor (Table 2) – and two arm exoskele-
quite simply for exoskeletons: the fingers extend by means of tons – T-WREX and ARMOR (Table 3) – have been used in
the common extensor whose individual tendons are attached controlled clinical trials in which the effectiveness of proce-
to the distal phalanges, and they flex by means of common dures using exoskeletons were compared with the effective-
flexors. The muscles controlling flexion and extension of the ness of standard poststroke treatment.
thumb also attach to the distal phalanges. The contractile Among hand exoskeletons approved in clinical tri-
parts of all these muscles are located in the forearm, only the als, those in Table 2 include two Russian-made models:
1056 Frolov, Kozlovskaya, Biryukova, and Bobrov

TABLE 2. Hand and Finger Exoskeletons

Developer Country Description Action of exoskeleton Arm joints


HWARD (Hand Flexion-extension of hand
Radiocarpal, 1st carpo-
Wrist Assistive at radiocarpal joint, thumb
University of California USA [Takahashi et al., 2008] metacarpal, 2nd–5th
Rehabilitation and fingers 2–5
metacarpophalangeal
Device) simultaneously
[Kotov et al., 2014;
Hand exoskeleton Simultaneous extension of
Neurobotics, Zelenograd Russia Mokienko et al., 2016; All joints of fingers 1–5
Z-hand fingers
Frolov et al., 2016]
Hand exoskeleton NPO Android Technics, Simultaneous extension of Radiocarpal, all joints of
Russia [Kondur et al., 2016]
Pianist Magnitogorsk fingers fingers 2–5
Hand of Hope
Rehab-Robotics Comp. Hong Kong, Independent flexion-exten-
(commercial [Ho et al., 2011] All joints of fingers 2–5
Ltd. China sion of fingers 2–5
system)
Active linear
National University of
HandCARE Singapore [Dovat et al., 2008] displacement of fingers All joints of fingers 2–5
Singapore
2–5
Center for Applied
HEXORR (Hand
Biomechanics and Simultaneous flexion-ex-
EXOskeleton [Schabowsky et al.,
Rehabilitation Research, USA tension of fingers 2–5, All joints of fingers 1–5
Rehabilitation 2010]
National Rehabilitation flexion-extension of thumb
Robot)
Hospital, Washington
InMotion Hand
Interactive Motion Tech.,
(commercial USA [Masia et al., 2007] Ball grip All joints of fingers 1–5
Inc.
system)
Electronic and Information Simultaneous flexion-ex-
Hand exoskeleton Department, Politecnico Italy [Mulas et al., 2005] tension of fingers 2–5, All joints of fingers 1–5
di Milano flexion-extension of thumb
Simultaneous flexion-ex-
Reha-Digit,
tension of fingers 2–5,
Reha-Stim Reha-Stim Medtec, GmbH
Germany [Hesse et al., 2008] vibrational stimulation of All joints of fingers 2–5
(commercial & Co, Berlin
the palmar surface of the
system)
fingers used in plegias
Department of Health
Technology and Metacarpophalangeal and
Independent flexion-exten-
Hand exoskeleton Informatics, The Hong China [Tong et al., 2010] distal interphalangeal
sion of fingers 2–5
Kong Polytechnic joints of fingers 2–5
University
AMES (Assisted Simultaneous flexion-ex-
AMES Technology, Inc.,
Movement with tension of hand and fingers Radiocarpal and metacar-
a spin-off company from
Enhanced USA [Cordo et al., 2009] 2–5, at the metacarpopha- pophalangeal joints of
Oregon Health & Science
Sensation) (com- langeal joints, vibrational fingers 2–5
University
mercial system) stimulation of muscles
Hand Mentor™
Kinetic Muscles, Inc., Extension of hand and Radiocarpal and joints of
(commercial USA [Koeneman et al., 2004]
Tempe, Arizona fingers 2–5 fingers 2–5
system)
AMADEO robotic [Kwakkel, Meskers, Flexion-extension of each
Tyromotion GmbH Graz Austria All joints of fingers 1–5
system 2014] finger separately

the Z-hand exoskeleton, operated by pneumatic muscles trolling these devices, which should ideally follow the prin-
(Neurobotics, Fig. 1, A), and the Pianist exoskeleton, oper- ciples of controlling the human hand by the CNS. Otherwise,
ated by electric motors (NPO Android Technics; Fig. 1, B). the patient perceives a movement made by an external de-
These exoskeletons have been used in a controlled, multi- vice as imposed and unfriendly, which leads to a decrease in
center, randomized trial [Frolov et al., 2016a]. the effectiveness of rehabilitation. Improvements in means
2. Biologically appropriate means of controlling ro- of controlling robotic devices are needed because of insuffi-
botic devices. A fundamental challenge for the use of ma- cient understanding of the principles of movement control
nipulators and exoskeletons in rehabilitation is that of con- by the CNS [Ferris, 2009]. However, the achievement of
Use of Robotic Devices in Post-Stroke Rehabilitation 1057

TABLE 3. Exoskeletons Supporting Movements at Different Joints of the Arm (F-E – flexion-extension; Ab-Ad – abduction-adduction, P-S – pronation-su-
pination, Rot – rotation relative to the longitudinal axis of the arm)

Developer Country Description Action of exoskeleton Arm joints


MUNDUS
Shoulder (Ab-Ad, F-E),
(MUltimodal Italy, Austria,
European project [Pedrocchi et al., Assistance mode in every- elbow (F-E, P-S), radiocar-
Neuroprosthesis for Germany,
MUNDUS 2013] day actions pal (F-E), finger joints
Daily Uppe limb Switzerland
(ball grip)
Support)
Shoulder (Ab-Ad, F-E),
Assistance mode stimulat-
Sensory Motor System elbow (F-E, P-S), radiocar-
ARMin Switzerland [Nef et al., 2009] ing involvement of the
Lab, Universität Zürich pal (F-E), finger joints
patient
(ball grip)
RUPERT (Robotic
Shoulder (F-E, Rot), elbow
UPper Extremity [Balasubramanian Assistance mode in every-
Arizona State University USA (F-E, P-S), radiocarpal
Repetitive Therapy et al., 2008] day actions
(F-E)
device)
T-WREX (Training Department of Mechanical Shoulder (Ab-Ad, F-E,
Wilmingyon Robotic & Aerospace Engineering, USA [Sanchez ey al., 2004] Passive mode Rot), elbow (F-E), finger
EXoskeleton) California University joints (ball grip)
Shoulder (Ab-Ad, F-E,
PneuWREX Minimum required assis-
[Wolbrecht et al., horizontal movement),
(Wilmington Robotic USA tance mode in everyday
2006] elbow (F-E), finger joints
EXoskeleton) actions
(ball grip)
Provides feedback from
PERCRO Laboratory,
L-exos (Light pressure on the palmar Shoulder (Ab-Ad, F-E,
Scuola Superiore Italy [Frisoli et al., 2007]
exoskeleton) surface of the hand during Rot), elbow (F-E)
Sant’Anna, Pisa
training movements
Design and Materials
ARAMIS Two symmetrical exoskel-
Technology Centre,
(Automatic etons, one of which com-
Brindisi; S. Anna Institute Shoulder (Ab-Ad, F-E,
Recovery Arm Italy [Pignolo et al., 2012] pensates for lack of
and Research on Advanced Rot), elbow (F-E, P-S)
Motility Integrated strength and accuracy in
Neurorehabilitation,
System) the paretic arm
Crotone
Department of
Passive mode, restricting
Biomechanical Shoulder (Ab-Ad, F-E,
Dampace Netherlands [Stienen et al., 2009] movement in specific de-
Engineering, University Rot), elbow (F-E)
grees of freedom
of Twente, Enschede
Shoulder (Ab-Ad, F-E,
Abteilung für
Rot), elbow (F-E, P-S),
ARMOR Neurologische Austria [Mayr et al., 2008] Active training mode
thumb (F-E), fingers 2-5
Akutbehandlung
(simultaneous F-E)
Shoulder (Ab-Ad, F-E,
Rehabilitation Institute Active mode: assistance or Rot), elbow (F-E), radio-
IntelliArm USA [Ren et al., 2009]
of Chicago preventative carpal (F-E), finger joints
(ball grip)

physiological movements nonetheless provides a theoreti- cally appropriate manner. However, studies have shown that
cal basis for developing biologically appropriate means of damage to brain structures generally produces less impair-
control. ment to planning of movements in terms of the trajectory
Theoretical and experimental studies have shown that of the working point than to the mechanisms of interactions
planning of goal-directed arm movements occurs in terms between joints [Levin, 1996]. This raises the challenge of
of the trajectory of the working point in external space, for the physiologically appropriate formation of joint rotations.
example, the trajectory of the hand for grasping an object The task of transforming the trajectory of the working point
or the trajectory of the tip of the finger for placing it at a to joint rotations does not have any single solution because
specific point [Hogan and Flash, 1987]. Thus, manipulators of the overprovision by the skeletal and neuromuscular ap-
forming the trajectory of the working point of the arm carry paratus of the human arm. This transformation is learned
out the plan of a goal-directed movement in a physiologi- during the process of motor training, leading to the forma-
1058 Frolov, Kozlovskaya, Biryukova, and Bobrov

tion of synergies of central commands, which are apparent Al-Jumailyb [2002] provides a detailed description of the
as coordinated changes in joint angles (kinematic syner- feedback control of the REHAROB manipulator and the
gies) and muscular torque at the joints (dynamic synergies) IntelliArm, ARMin, L-Exos, Rupert, and Pneu-WREX arm
[Bernshtein, 1935]. exoskeletons.
There are currently no generally accepted methods for However, the problem of low stiffnesses in exoskel-
determining motor synergies suitable for use in active exo- eton articulations remains unsolved. Experimental physi-
skeletons. Hand exoskeletons (Table 2) do not need joint ological studies have demonstrated that control of a joint
rotations for the trajectory of the working point. The con- with low stiffness comes up against the problem of control
struction of these exoskeletons is close to the anatomical stability. In living systems, the total torque at a joint can be
construction of the flexor-extensor apparatus of the fingers modeled by a viscoelastic spring with controllable parame-
and provide good reproduction of the main grasping move- ters: equilibrium length, stiffness, and viscosity [Fel’dman,
ments of the fingers. Arm exoskeletons (Table 3) are also 1979; Gomi and Kawato, 1996]. The equilibrium length of a
not faced with the task of realizing any particular kinematic spring corresponds to the desired joint angle and is specified
or dynamic synergies. As a rule, an assistance mode is used, at the supraspinal level of the CNS. Stiffness and viscosity
where residual movements in the arm joints are amplified are determined by the interaction of three different physio-
by feedback signals, or in the passive mode, where move- logical mechanisms: the viscoelastic properties of muscle
ments are restricted into one or another set of degrees of fibers and tendons, the spinal stretch reflex circuit, and the
freedom, in accordance with the rehabilitation protocol. Just feedback circuit passing through the brain [Peterka, 2002].
one arm exoskeleton approved in clinical trials – ARMOR In contrast to the first mechanism, operation of the second
[Mayr et al., 2008] – reproduces, in the active mode, the and third have significant delays. The delay for the stretch
joint movements of the functionally intact arm in the joints reflex circuit is ~50 msec, compared with up to 150 msec for
of the paralyzed arm. the second circuit [Peterka et al., 2002; Frolov et al., 2000,
Some authors have suggested that in transforming the 2006]. The effective delay used in feedback control is de-
trajectory of the working point into changes in joint angles, termined by the relative contributions of these three mech-
the nervous system solves several optimization tasks. This anisms. The existence of a time delay imposes restrictions
approach, actively developed in the 1970s–1980s [Bizzi et on the feedback parameters supporting stable control. These
al., 1982], also has more contemporary supporters [Kaneko restrictions are apparent in that stiffness and viscosity must
et al., 2005]. This suggestion, which is entirely logical in be limited both from above and from below [Alexandrov et
prototyping robotic system, is rather artificial for living sys- al., 2005].
tems. A more biologically appropriate approach consists of The appropriateness of the model of control of the total
using a controlling neural network which learns on the basis muscular torque at the joint based on a viscoelastic spring
of trial and error [Frolov et al., 1994]. Both approaches, al- with controllable parameters has been demonstrated for
though supporting selection of a trajectory in the space of control of the elbow joint in conditions of unexpected con-
the joint angles close to the experimentally observed, are trolled unloading of the forearm [Biryukova et al., 1999], by
not universal because of the arbitrariness of selecting the the joints of the human arm in goal-directed movements
target function to be optimized and because of the neural [Frolov et al., 2006], by the hip, knee, and ankle joints when
network training algorithm. people are tilted in the sagittal plane [Alexandrov et al.,
Another complexity in controlling exoskeletons comes 2005; Alexandrov and Frolov, 2011].
from the viscoelastic nature of the joint torque in combina- An effective means of computing biologically appro-
tion with low physiological joint stiffness levels. In living priate control parameters using feedback based on the prin-
systems, this difficulty is overcome by control using feed- ciple of independent control of movements along dynamic
back and multiple repetition of movements during motor control eigenvectors has been proposed in [Kaneko et al.,
learning [Bernshtein, 1947/1991]. Given that joint stiffness 2005; Alexandrov and Frolov, 2011; Frolov et al., 2013].
in the arm is not great (according to different literature sourc- This has been realized for control of an arm exoskeleton
es: from 2 to 100 Nm at the elbow and from 10 to 70 Nm at with seven degrees of freedom made by NPO Android
the shoulder) [Frolov et al., 2000, 2006], rigid control of the Technics (Magnitogorsk) and has been tested in healthy
joint in executing a specified kinematic is perceived by the subjects (Fig. 3).
patient as uncomfortable. Biologically appropriate control 3. Neurorehabilitation technologies. Technical solu-
of the joint torque requires feedback from the joint angle and tions realizing active actions by the exoskeleton on the pa-
for the exoskeleton to provide the low joint stiffnesses that tient’s arm during neurorehabilitation can be divided into
the patient is familiar with. Feedback from the joint angle assistance, restrictive, and technologies using BCI.
and control in terms of impedance, equivalent to control us- 3.1. Assistance technologies. Impedance-assistance.
ing a PD (proportional derivative) – the controller in techni- As long as the arm follows the specified trajectory, the ex-
cal systems – is successfully used in manipulators (Table 1) ternal device does not interfere; however, if it deviates in
and exoskeletons (Tables 2, 3). The review of Anam and terms of some critical parameter, the external device devel-
Use of Robotic Devices in Post-Stroke Rehabilitation 1059

ops a force returning the arm towards the desired trajec- trigger the plastic mechanisms of the brain to rearrange the
tory. In general, the returning force acts as a viscoelastic sensorimotor system [Di Pino et al., 2014]. For this, exo-
spring [Anam and Al-Jumailyb, 2002]. To provide natural skeleton movement must be carried out only at the moment
variability in movements, some family of trajectories re- at which the brain is most sensitive to receiving peripheral
garded as available is considered, i.e., those which when signals produced by exoskeleton movement, i.e., those mo-
followed do not involve the exoskeleton acting on the arm ments at which the patient intends to complete the move-
[Reinkensmeyer et al., 2000]. ment. In many studies, the patient’s intent to carry out a
Sometimes the external device interferes in the pa- movement is recognized by detecting the EMG with super-
tient’s voluntary movement only when the patient cannot ficial electrodes [Mulas et al., 2005; Tong et al., 2010]. In
complete the desired movement. In this case, the exter- this case, increases in the EMG serve as a trigger signal for
nal device helps this to happen. The MIT-Manus. MIME, the exoskeleton. However, this signal cannot be used in
Haptic Master, and ARM Guide manipulators, the hand completely paralyzed patients or patients with impairment
exoskeleton HWARD, and the hand exoskeleton Rupert are to normal muscle coactivation [Wright et al., 2014].
able to operate in this mode. The advantage of this control is BCI based on kinesthetic motor imagery were used in
that the patient initiates the movement independently, which [Buch et al., 2008; Ang et al., 2011, 2014, 2015; Ramos-
is fundamental for successful motor learning [Lotze et al., Murguialday et al., 2013; Ono et al., 2014; Kotovet et al.,
2003]. The drawback of this control is the risk of triggering 2014; Mokienko et al., 2016; Frolov et al., 2016] to recog-
an uncontrolled movement. nize the patient’s intent. The patient’s intent to carry out a
Equalizing assistance. This frequently used technolo- movement was successfully linked with real movements
gy is based on equalizing the force of gravity when the arm performed by the exoskeleton. Patients’ ability to lean mo-
rests on a support or is elevated. Some methods consider tor imagery was comparable with that of healthy people
partial unloading of the arm and use devices controlling the [Frolov et al., 2017]. It is also important that over a quite
degree of unloading during training [Marchal-Crespo and wide range of patients, no correlations were found between
Reinkensmeyer, 2009]. task performance success and the level of cognitive deficit
Assistance using EMG signals. Within the framework [Kotov et al., 2014; Frolov et al., 2016; Ang et al., 2011].
of this technology, the exoskeleton assists in completing All the studies cited above apart from that of Ono et al.
movements, developing a force proportional to the EMG [2014] used hand exoskeletons. The expectation that the use
amplitude [Ho et al., 2011; Mulas et al., 2005; Tong et al., of these exoskeletons will be effective is associated with the
2010; Koeneman et al., 2004]. This method has significant large representation of the hand in the cerebral cortex, such
limitations because of the sensitivity of the EMG to electrode that large areas of the brain are activated. On the other hand,
positioning and the overall state of the patient. In addition, movements performed by these exoskeletons – flexion/ex-
there is the risk of unpredictable exoskeleton movements tension of the fingers – are far from the multiple-joint move-
when the patient inappropriately activates muscles, which ments performed by people in their daily lives. However, it
often occurs as a result of stroke [Dipietro et al., 2005]. is well known [Bernshtein et al., 1947] that patients with
3.2. Restrictive technologies. Poststroke patients often motor disorders perform highly important functional auto-
use the healthy arm or joints with retained motor functions mated movements far better than purposeless movements.
in executing motor tasks. The most widespread example is In fact, the whole practice of poststroke rehabilitation is
movement of the body instead of extending the arm if re- based on the intensification and repetition of target multi-
quired to reach the target. These cases use a restriction strat- ple-joint movements. It can be suggested that the simplicity
egy where the healthy arm or preserved joints are fixed with and absence of an aim for movements had the result that the
the aim of stimulating movement in the joints with impaired effects obtained using the BCI + exoskeleton procedure
movement function [Taub et al., 2002; Shaw et al., 2005]. In were less than expected when they were first introduced
mild forms of hemiparesis, recovery mechanisms are stimu- [Buch et al., 2008; Ang et al., 2011; Kotov et al., 2014]. It
lated by addition of forces preventing movement and re- therefore seems encouraging to rehabilitate using the exo-
quiring the patient to make an effort to overcome them skeleton procedure providing goal-directed movements ori-
[Hesse et al., 2003; Rosati et al., 2007]. ented to functionally significant tasks under BCI control.
In some rehabilitation procedures, movement execu- The single report of studies of the potential for rehabil-
tion errors are increased artificially by movement perturba- itation procedures using BCI controlling a multicomponent
tions [Patton et al., 2006] or distortion of visual feedback arm exoskeleton providing the whole range of human arm
[Brewer et al., 2008]. Increases in kinematic errors (over- movements is that of Brauchle et al. [2013]. This study used
shooting the target or deviation from the specified trajecto- an Armeo Power, Hocoma (Volketswil, Switzerland), con-
ry) are additional neural signals triggering adaptation mech- trolling all seven degrees of freedom of the human arm. The
anisms to correct errors. exoskeleton supports the arm in the gravitational field and
3.3 Technologies using BCI. The effectiveness of re- allows a large repertoire of goal-directed arm movements to
habilitation procedures depends on the extent to which they be made. This study demonstrated that the exoskeleton
1060 Frolov, Kozlovskaya, Biryukova, and Bobrov

could be linked with a BCI to carry out three sequential signals generated by a large set of sources, which, as demon-
movements towards fixed targets in nine healthy subjects strated by fMRI, are distributed through the whole volume
and two poststroke patients. The effectiveness of this sys- of the brain. This fact is responsible for the poor spatial res-
tem for motor rehabilitation was not assessed. olution of the EEG. Recent years have seen the development
Physiological Requirements for the Use of Robotic of an approach increasing the resolving ability of the EEG to
Devices in Poststroke Rehabilitation at least the level obtained with fMRI, retaining its high time
1. fMRI and transcranial magnetic stimulation resolution [Makeig et al., 1996; Onton et al., 2006; Delorme
data. fMRI study data from brain areas showing increases et al., 2012]. This approach is based on use of the indepen-
in hemodynamic activity over the resting level on kinesthet- dent components analysis method [Kachenoura et al., 2008]
ic motor imagery and on performance of movements almost and solution of the inverse EEG problem.
coincided [Jeannerod and Frak, 1999]. The exclusion is the This method identified tens of independent EEG sourc-
motor cortex, which is activated on execution of move- es active during motor imagery, though systematic study of
ments but whose activity in motor imagery is seen in only these has only just started [Frolov et al., 2012, 2013; Bobrov
15% of studies [Hétu et al., 2013; Grèzes and Decety, 2001]. et al., 2011; Bobrov et al., 2016].
Changes in brain activity due to training to motor im- Movement, preparation for movement, observation of
agery in controlling a BCI were specifically studied by movement, or imagination of the movement of some execu-
Mokienko et al. [2013] and Frolov et al. [2016b] in healthy tive organ is usually accompanied by decreases in the μ and
subjects serving as the control group for comparison with β rhythms in the cortical representation of this organ. This
poststroke patients. These studies showed that at least 14 decrease is termed event-related desynchronization (ERD)
brain areas showed increases in levels of hemodynamic ac- [Pfurtscheller and Berghold, 1989; Pfurtscheller, 1999;
tivity due to training to motor imagery in the BCI control Pfurtscheller and Lopes da Silva, 1999]. Increases in the μ
procedure. However, significant increases were seen only in rhythm, i.e., event-related synchronization (ERS) are seen
the following five areas: Brodmann fields 44 and 45, the in brain areas representing organs not involved in execu-
insula, the middle frontal gyrus, and the anterior cingulate tion of the movement of interest [Pfurtscheller, 1999]. One
gyrus. It is interesting that all these areas are in the anterior hypothesis is that the ERD and ERS reactions correspond
part of the brain, though imagination and execution of to cortical control of the “thalamic gating mechanism”
movements show a strong interaction between the anterior [Klimesch et al., 2007; Klimesch, 2012]. Cortical areas
and parietal areas of the brain [Hétu et al., 2013; Grèzes and demonstrating ERS are tuned to perceive strong but unde-
Decety, 2001]. The absence of any significant differences in fined signals without detailed encoding, while those demon-
activity in the parietal areas of the brain appears to be asso- strating ERD are tuned to the detailed analysis of specific
ciated with the fact that the sensory flow of information in signals uniformly encoded over the whole region in which
motor imagery is limited and training to control a BCI does they change. On execution of motor imagery too, afferent
not require any increase in activity in the areas processing it. signals (for example, proprioceptive) must constantly be
In contrast, activity in the anterior areas forming motor compared with efferent copies and any deviation arising as
commands increases. a result of this comparison must be corrected immediately
Apart from changes in brain hemodynamic activity [Jeannerod, 1994]. It can be suggested that the site at which
on motor imagery, Mokienko et al. [2013] studied plastic this comparison takes place is the primary somatosensory
changes in the brain as a result of training to control a BCI cortex [Sun et al., 2015]. It can also be suggested that the
using transcranial magnetic stimulation. Motor imagery is efferent copy generated by the premotor cortex arrives in
known to decrease the magnetic field intensity triggering the primary somatosensory cortex and switches it to the
threshold for the activity of the relevant muscles on stimula- ERD regime, tuning to detailed comparison with peripheral
tion of the primary motor cortex [Stinear, 2010]. Important signals associated with the movement. This interpretation
evidence for plastic rearrangements of the brain due to train- of the functional significance of the ERD and ERS reac-
ing to control a BCI was provided by the observation that tions is consistent with the localization of the EEG source
the increase in primary motor cortex arousability was sig- demonstrating these reactions most strongly as reported in
nificantly more marked in trained than untrained subjects. [Frolov et al., 2012], in the depth of the central sulcus and
2. EEG activity data. Most reports of brain activity Brodmann area 3a, where the proprioceptive sensation of
during the execution, imagination, and observation of move- the palms and fingers is represented.
ments have been obtained using fMRI studies. However, the Thus, the main, albeit not the only, neurophysiological
functional role of each of the areas whose activity increased grounds for high operating quality of BCI based on motor
on execution of the tasks remained unclear. This is largely imagery are ERD and ERS reactions, i.e., suppression of the
due to the poor time resolution of fMRI – of the order of sec- resting μ rhythm in the representation area of the proprio-
onds. EEG recording provides an alternative to fMRI and has ceptive sense of the arm whose movement is imagined, with
resolution on the order of tens of milliseconds. However, the increases in this rhythm in the representation area of the
signal recorded by each electrode is a superimposition of the opposite arm.
Use of Robotic Devices in Post-Stroke Rehabilitation 1061

TABLE 4. Use of BCI + Exoskeleton Technology in Clinical Practice for Motor Recovery After Stroke

Extent of Age of Duration Assessment


Exo- Motor Number of
Description impairment to patients of stroke Protocol of Results
skeleton imagery patients
MF (years) (months) effectiveness
1. BCI +
Improvement in
Haptic Knob.
Flexion- MF in group 1
[Ang et al., Haptic F-M 10–50 2. Haptic
extension 7+8+7 30–79 6–22 F-M significantly great-
2014] Knob (max 66) Knob
of fingers er than in groups 2
3. Standard
and 3
treatment
Improvement in
1. BCI + MF in both groups
[Ang et al., MIT- Movement of F-M 4–40
11 + 15 35–62 2–18 MIT-Manus F-M with no significant
2015] Manus arm to target (max 66)
2. Mit-Manus difference between
them
Significant im-
36 (20, 13,
provement in MF
and 3 from
1. BCI + F-M, ARAT, seen in a larger
[Frolov et Extension different F-M 61–104
Z-hand 47–73 1–13.5 Z-hand MAS, proportion of pa-
al., 2016] of fingers clinics) + 11 (max 126)
2. Z-hand MRC-SS tients of the study
(control
group than the
group)
control group
1. BCI with
Improvement in
visual feed-
[Ono et al., Hand Extension SIAS0–1 SIAS, MF of fingers only
6+6 41–84 4–155 back
2014] orthosis of fingers (max 5) EMG in BCI + orthosis
2. BCI +
group
orthosis
Stretching Improvement in
[Ramos-
of arm and 1. BCI + MF in study group
Murgui- Arm F-M 4–21
grasping 16 + 16 37–62 21–111 orthosis F-M significantly great-
alday et al., orthosis (max 54)
imaginary 2. Orthosis er than in control
2013]
apple group
Flexion- 5 + 3 (two Hand plegia
[Buch et al., Wrist BCI + No improvement
extension different (MRC 0/5, 14–68 12–41 MRC
2008] orthosis orthosis in MF
of fingers clinics) MAS < 3)

Use of BCI + Exoskeleton Technology in Clinical lar interest in a case of plegia and profound pareses, where
Studies motor imagery was the only active paradigm modulating
1. Results of controlled studies. There are as yet few neuroplasticity processes in the motor zones of the brain
applications of exoskeleton-controlling BCI based on rec- [Mokienko et al., 2013; Shih et al., 2012; Soedakar et al.,
ognition of the EEG in kinesthetic motor imagery. Table 4 2015; Grosse-Wentrup et al., 2011]. Buch et al. [2008] stud-
shows those which included a control group of patients not ied eight patients with hand plegia (muscle strength on the
performing a mental motor imagery task. The studies in- Medical Research Council (MRC) scale was 0/5 and muscle
cluded patients with a wide range of ages (from 14 to 84 spasticity on the Modified Ashworth Scale (MAS) was <3)
years), durations of stroke (from one month to 13 years), who underwent courses of rehabilitation with BCI-controlled
and extents of MF impairment (from 4 to 50 points out of hand orthoses. Despite the fact that all patients successfully
the maximum 66 points on the Fugl-Meyer scale). Studies controlled the orthosis and that the number of procedures
differed in terms of the numbers of procedures and their du- was significant (16–22), no improvements in MF were seen
rations, and procedures used different types of exoskele- after the procedures. It may be that this negative result was
tons. Despite these differences, all studies (Table 4) showed associated with the low sensitivity of the MRC and MAS
that improvements in MF after procedures were more scales used to evaluate MF. Assessment of biomechanical
marked in the study groups than the control groups. This parameters of the movements of patients with hand plegia,
leads to the conclusion that the use of BCI controlling limb extensive cortical injuries, and long durations of brain trau-
exoskeletons on the basis of EEG signals corresponding to ma demonstrated improvements in MF after 15 BCI + hand
kinesthetic motor imagery has positive clinical effects. exoskeleton procedures [Biryukova et al., 2016].
It should be noted that the extent of neurological defi- 2. Assessment of the effectiveness of BCI + exoskele-
cit in these studies was mostly moderate. There is particu- ton technology. The question of the appropriate evaluation
1062 Frolov, Kozlovskaya, Biryukova, and Bobrov

of MF after stroke is extremely relevant, particularly in re- eton. Even cases of extensive cortical injury showed the
lation to assessment of new rehabilitation methods. Most ability to exert voluntary control of the μ rhythm both in the
studies assessing the effectiveness of exoskeleton-con- hemisphere ipsilateral to the injury and in the contralateral
trolling BCI have used the Fugl-Meyer scale [Fugl-Meyer et hemisphere [Buch et al., 2008]. fMRI data showed stronger
al., 1975], which includes a large number of motor tests and activation in the contralateral hemisphere, as well as activa-
is recommended as a validated and reliable scale [Gladstone tion in its primary motor cortex, in a patient with hand ple-
et al., 2002]. However. This scale, like other clinical scales, gia who underwent a prolonged course of training to motor
is not free from subjective components and, using discrete imagery [Biryukova et al., 2016].
scores for assessment, is insufficiently sensitive to detect Analysis of fMRI data in a controlled study [Ramos-
small changes in MF which even so can serve as an import- Murguialday et al., 2013] showed that training to active
ant predictor of the effectiveness of the treatment method. motor imagery led to a shift in activity in the motor and pre-
As the question of the effectiveness of BCI + exoskeleton motor areas of the cortex from the contralateral (preserved)
rehabilitation methods can be regarded as open [Teo and hemisphere to the ipsilateral, i.e., to the side showing ac-
Chew, 2014], its assessment needs methods excluding the tivity in health. The index of lateralization of this activity
subjective component and giving numerical, physiological- [Stinear et al., 2010] correlated with assessment of MF on
ly interpretable data on the state of MF to be used. the Fugl-Mayer scale.
Recording of limb movements with subsequent biome- The study reported by Ono et al. [2014], conversely,
chanical analysis of the parameters of these movements showed no correlation between improvements in MF and
provides such a method. This method is widely used to as- the extent of desynchronization of the μ rhythm: activity in-
sess the state of MF in poststroke and posttrauma patients creased in both the study group and the control group, while
[Alt Murphy and Häger, 2015]. However, only two studies improvements in MF were seen only in the study group.
have used this method for assessment of the state of MF As regards the link between success in recognizing EEG
during rehabilitation using BCI + exoskeleton technology. activity associated with motor imagery and improvement in
The first [Biryukova et al., 2016] analyzed the trajectory of MF, these studies are contradictory: Ang et al. [2011] found
the working point of the paretic arm in movements to a sta- no correlation between them, while Ang et al. [2015] report-
tionary target, along with the contributions of the various ed a negative correlation and Frolov et al. [2016] found a
arm joints to these movements. Approximation of the speed significant positive correlation. Differences in these results
profile of the working point to a bell-shaped curve and inhi- may be associated with the different types of classifiers and
bition of joint movements not taking the working point to methods of evaluating MF used in these studies.
the target were interpreted as improvements in overall con- Ono et al. [2014] made the following suggestion be-
trol quality. In the second study [Kondur et al., 2016], angu- cause improvements in MF were seen only in the group us-
lar accelerations at the arm joints were taken as assessments ing the exoskeleton. Desynchronization of the μ rhythm
of the total muscle torque and the number of local peaks in could reflect arousal of the primary motor cortex during ex-
angular speed as assessments of muscle spasticity driving ecution of a significant motor task [Takemi et al., 2013].
joint movement. After 10 BCI + exoskeleton procedures, a Thus, the sensory input from the exoskeleton involving the
patient with a duration of stroke of 4 months and severe finger in motion may aid neuronal reorganization processes
impairment to MF showed increases in muscle strength and in this region. Furthermore, because of the nonlinear nature
decreases in spasticity. Assessment of strength on the MRC of neuron activity, additional arousal of the motor cortex by
scale and spasticity on the MAS scale did not identify any somatosensory feedback may promote additional arousal of
changes, while the overall assessment of MF on the Fugl- the primary motor cortex, in turn helping to restore MF.
Meyer scale increased. Each of these studies presented a Conclusions. Despite use of intense rehabilitation
single clinical case of severe impairment to MF and report- measures, restoration of the motor functions of the arms
ed detailed biomechanical analysis of movements in all the for everyday self-care remains unachievable for most post-
degrees of freedom of the arm. The results showed that this stroke patients. Further improvements in and standardiza-
analysis captures subclinical changes in movement parame- tion of rehabilitation procedures over recent years have led
ters. These changes can be regarded as predictors of suc- to a multiplicity of procedures using robotic systems aiding
cessful restoration of MF at the early stage of treatment and motor training in patients. However, these have not been as
can provide appropriate assessments of the potential of re- encouraging as expected [Lo et al., 2010].
habilitation using this method. Rehabilitation effectiveness appears to depend not so
3. Plastic rearrangements after BCI + exoskeleton much on assistance to the arm – unweighting of the arm, the
procedures. Changes in MF seen during rehabilitation us- type and number of movements performed by them – as the
ing BCI + exoskeleton technology are due to plastic rear- extent of involvement of the patient in the treatment pro-
rangements occurring in the cerebral cortex as a result of cess: concentration of attention and muscular and/or mental
training to kinesthetic motor imagery and its reinforcement efforts [Patton et al., 2008]. Passive robot therapy can even
by proprioceptive feedback from movement of the exoskel- improve recovery of MF and aid general relaxation of the
Use of Robotic Devices in Post-Stroke Rehabilitation 1063

patient [Marchal-Crespo and Reinkensmeyer et al., 2009]. Alexandrov, A. V., Frolov, A. A., Horak, F. B., Carlson-Kuhta, P., and
BCI controlling exoskeletons support the active involve- Park, S., “Feedback equilibrium control during human standing,”
Biol. Cybern., 93, 309–322 (2005).
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motor resource is significantly restricted. Clinical studies of tremity alter stroke – how far have we reached and what have we
BCI + exoskeleton procedures including a wide spectrum of grasped?” Phys. Ther. Rev., 20, 137–155 (2015).
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Amirabdollahian, F., Loureiro, R., Gradwell, E., Collin, C., Harwin, W.,
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that of the development of a standard rehabilitation protocol: Ang, K. K., Guan, C., Chua, K. S., and Ang, B. T., Kuah, C. W., Wang, C.,
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(2011).
little study, though this depends on the type and severity Ang, K. K., Guan, C., Phua, K. S., Wang, C., Zhou, L., Tang, K. Y.,
of damage. In these conditions, the task of identifying tar- Ephraim Joseph, G. J., Kuah, C. W., “Brain–computer interface-
get groups of patients with rehabilitation potential in whom based robotic end effector system for wrist and hand rehabilitation:
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critical [Kotov and Stakhovskaya, 2014]. As noted above, stroke,” Front. Neuroeng., 7, 30 (2014).
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Russian Foundation for Basic Research (Grant Nos. 16-29- 107–117 (1999).
08247 ofi_m, 16-29-08206 ofi_m, 16-04-01506, and 16-04- Bizzi, E., Acconero, N., Chapple, W., and Hogan, N., “Arm trajectory for-
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Abbreviations: nin, Ya. V., Popod’ko, A. I., and Frolov, A. A., “Sources of electro-
MF – motor function; physiological and foci of hemodynamic activity in the brain signifi-
BCI – brain–computer interface; cant for the control of a hybrid brain–computer interface based on
fMRI – functional magnetic resonance imaging; the recognition of EEG patterns and near infrared spectrograms on
motor imagery,” Fiziol. Cheloveka, 42, No. 3, 12–24 (2016).
CNS – central nervous system; Bobrov, P., Frolov, A. A., and Húsek, D., “Brain computer interface en-
EMG – electromyogram; hancement by independent component analysis,” in: Proceedings of
EEG – electroencephalogram. the Third International Conference on Intelligent Human Computer
Interaction (IHCI 2011), Prague, Czech Republic, August, 2011,
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