NEW INSIGHTS INTO FUNCTIONAL

MAPPING IN CEREBRAL TUMOR

SURGERY

No part of this digital document may be reproduced, stored in a retrieval system or transmitted in any form or
by any means. The publisher has taken reasonable care in the preparation of this digital document, but makes no
expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No
liability is assumed for incidental or consequential damages in connection with or arising out of information
contained herein. This digital document is sold with the clear understanding that the publisher is not engaged in
rendering legal, medical or any other professional services.
NEW INSIGHTS INTO FUNCTIONAL
MAPPING IN CEREBRAL TUMOR
SURGERY

HUGUES DUFFAU

Nova Science Publishers, Inc.

New York
Copyright © 2009 by Nova Science Publishers, Inc.

All rights reserved. No part of this book may be reproduced, stored in a retrieval system or
transmitted in any form or by any means: electronic, electrostatic, magnetic, tape, mechanical
photocopying, recording or otherwise without the written permission of the Publisher.

For permission to use material from this book please contact us:
Telephone 631-231-7269; Fax 631-231-8175
Web Site: http://www.novapublishers.com

NOTICE TO THE READER

The Publisher has taken reasonable care in the preparation of this book, but makes no expressed
or implied warranty of any kind and assumes no responsibility for any errors or omissions. No
liability is assumed for incidental or consequential damages in connection with or arising out of
information contained in this book. The Publisher shall not be liable for any special,
consequential, or exemplary damages resulting, in whole or in part, from the readers’ use of, or
reliance upon, this material.

Independent verification should be sought for any data, advice or recommendations contained
in this book. In addition, no responsibility is assumed by the publisher for any injury and/or
damage to persons or property arising from any methods, products, instructions, ideas or
otherwise contained in this publication.

This publication is designed to provide accurate and authoritative information with regard to the
subject matter covered herein. It is sold with the clear understanding that the Publisher is not
engaged in rendering legal or any other professional services. If legal or any other expert
assistance is required, the services of a competent person should be sought. FROM A
DECLARATION OF PARTICIPANTS JOINTLY ADOPTED BY A COMMITTEE OF THE
AMERICAN BAR ASSOCIATION AND A COMMITTEE OF PUBLISHERS.

LIBRARY OF CONGRESS CATALOGING-IN-PUBLICATION DATA

Duffau, Hugues
New insights into functional mapping in cerebral tumor surgery / Hugues Duffau.
p. ; cm.
Includes index.
ISBN 978-1-60741-397-4 (E-Book)
1. Brain--Tumors--Surgery. 2. Brain mapping. I. Title.
[DNLM: 1. Brain Mapping. 2. Brain Neoplasms--surgery. 3. Brain Neoplasms--
physiopathology. 4. Postoperative Complications--prevention & control. WL 358 D855n
2009] RD663.D84 2009
616.99'481059--dc22 2008042534

Published by Nova Science Publishers, Inc. + New York

 CONTENTS

Preface vii
Chapter I Introduction 1
Chapter II Study of the Dynamic Biological Behavior of the
Tumor 3
Chapter III Study of the Dynamic Organization of the Brain 9
Chapter IV Study of the Dynamic Interactions between the
Tumor and the Brain 23
Chapter V Surgical Results 31
Chapter VI Conclusions and Perspectives 33
References 37
Index 85
 PREFACE

The rationale of brain tumor surgery depends on two antagonist goals: on one
hand, to optimize the quality of resection, on the other hand, to minimize the risk
of permanent postoperative deficit. However, due to the physiological
interindividual anatomo-functional variability, increased in cases of cerebral
tumors because of the plastic potential of the brain, a study of the interactions
between the lesion and the host seems mandatory – in order to understand the
individual dynamic organization of the brain, then with the goal to avoid
postsurgical sequelae.
In this way, new methods of functional brain mapping can be useful for the
neurosurgeon.
First, before surgery, non-invasive functional neuroimaging techniques
(fMRI, PET, MEG) and invasive extraoperative electrical mapping (subdural
grids) may allow to study the cortical organization for each patient. Furthermore,
Diffusion Tensor Imaging can help to understand the brain connectivity. Thus, the
relationships between the tumor and the eloquent areas can be estimated, and
these data applied to the surgical planning.
Second, during surgery, direct intraoperative electrical stimulation permits to
detect with accuracy and reliability, both the cortical sites and the white pathways
essential for a given function, at each moment and each place of the tumor
removal. Moreover, repeated stimulations all along the surgical act also allow to
study the mechanisms of short-term plasticity, induced by the resection itself. This
on-line mapping is used to tailor the resection according to cortico-subcortical
functional boundaries.
Third, postoperative neurofunctional imaging, combined to the precise
evaluation of the clinical course and the objective assessment of the location and
extent of resection, gives the opportunity to study the mechanisms underlying the
viii Hugues Duffau

functional compensation, i.e. the long-term plasticity. This potential may be used
to perform a second surgery with a better quality of resection than the first one,
thanks to possible brain remapping.
Such a pre-, intra- and post-surgical longitudinal study of dynamic
interactions between brain and lesion, allows to better apprehend the distinct
patterns of functional redistribution for each patient, thus to apply this knowledge
in order:

to better select the surgical indication in brain tumors;

to better inform the patient of the actual risk of transient postoperative deficit;
to better plan the resection (surgical approach, cortico-subcortical
boundaries);
to optimize the quality of tumor removal while preserving the functional areas
and tracts;
and to plan a specific rehabilitation.

Finally, on a fondamental point of view, the association of methods of

functional mapping in neurosurgical patients allows to better understand the
pathophysiology of brain areas, their connectivity, and the mechanisms of plastic
potential of the glio-neurono-synaptic networks.

Keywords: functional neuroimaging, brain mapping, electrical stimulations,

connectivity, plasticity, tumor surgery.
Chapter I

INTRODUCTION

Since long time, the classical conception of cerebral tumor surgery was to try
to remove a lesion located within a “static” host, i.e. a brain with a functional
organization definitely fixed for each patient and quite similar between patients,
while preserving the structures commonly considered as crucial – namely, the
rolandic, Broca’s and Wernicke’s areas.
In the last decade, technical developments in the field of functional brain
mapping demonstrated the existence of not only a physiological inter-individual
anatomo-functional variability [1,2], but also a plastic potential of the central
nervous system allowing a short- and long-term redistribution of the functional
maps within the same subject, in particular in learning or memory [3,4]: this is the
so-called “natural plasticity”. Moreover, this capacity to reorganize itself was
shown to participate to the functional recovery of patients who presented an acute
cerebral lesion, such as traumatic injury or stroke [5,6]: this is the “post-lesional
plasticity”.
Interestingly, more progressive lesions such as slow-growing tumors are also
able to induce brain functional reshaping [7]. This explains the frequent lack of
neurological deficit despite the growth of infiltrative neoplasms such as low-grade
gliomas within the so-called “eloquent” areas. Consequently, a new conception of
brain tumor surgery could consist on the study of the dynamic interactions
between the natural history of the lesion and the induced cerebral adaptation, in
order to apply this knowledge to each patient and each tumor. Such an attitude
may allow to better select the surgical indications and to maximize the quality of
tumor removal while minimizing the risk of postoperative definitive deficit.
The goal of this article is to review the recent research in brain mapping,
which permits the study of (1) the biological behavior of each tumor, which can
2 Hugues Duffau

change with time (2) the plastic functional brain organization of each patient (3)
and their dynamic interactions – in order to optimize the ratio : benefit / risk of the
cerebral tumor surgery.
Chapter II

STUDY OF THE DYNAMIC BIOLOGICAL

BEHAVIOR OF THE TUMOR

A – NATURAL HISTORY
The knowledge of the natural history of a tumor is essential in the optimal
selection of the therapeutical strategy, especially for surgical indications. Among
the spontaneous prognostic factors of brain tumors, in particular concerning
gliomas (i.e. the most frequent tumors of the central nervous system [8,9]), the
biological behavior of the lesion remains one of the more important (or even the
most important) parameter. This includes not only the histological grade of the
tumor and its potential of invasion, but also its ability to change its aggressivity.
One of the best examples is represented by the low-grade gliomas (LGG),
namely the glioma WHO grade II [10]. Indeed, a better understanding of their
natural history shows that LGG can follow three ways of evolution, i.e. (1) local
growth (2) invasion (3) anaplastic transformation. First, recent works have shown
that before any anaplastic transformation, LGG show a continuous, constant
growth of it mean tumor diameter over time, with an average slope around 4 mm
per year [11]. Second, invasion of LGG along the main white matter pathways
within the lesional hemisphere or even controlaterally via the corpus callosum
was also extensively described [12]. Third, it is currently well-known that LGG
systematically changes its biological nature and evolves to a high grade glioma,
with a median of anaplastic transformation estimated around 7 to 8 years,
invariably fatal (median survival around 10 years) [13-36].
This vision of a tumor with a “dynamic” behavior needs to be integrated in
the therapeutical strategy, in order to adapt the treatment both to the actual
4 Hugues Duffau

biology of the glioma at time of diagnosis (“tumor mapping”) and to the

functional compensation of the brain already induced by the slow-growing glioma
before any symptom (“cerebral mapping”) – thus to their interactions. Since the
determination of spontaneous risk factors remains very difficult for each patient
using classical clinical and radiological parameters, as demonstrated by many
retrospective studies and prospective trials in the literature [37-42], the adjunct of
complementary individual data using recent advances in the field of metabolic
neuroimaging allowing a “tumor mapping” is very useful, in addition to parallel
progresses in molecular biology [42-48] and biomathematical modelisation
[49,50] (not discussed in this review).

B - METABOLIC NEUROIMAGING
Indeed, the use of various brain radioactive tracers has shed invaluable light
on the pathophysiology of cerebral neoplasms: nature and degree of heterogeneity
of the tumor, patterns of growth and extension, risk and delay of anaplastic
transformation.
First, Single Photon Emission Computed Tomography (SPECT) studies
showed a relationship between tracers uptake and tumor grade, using both
Thallium-201 [51,52] or 99mTc-MIBI [53-55]. Thus, determination of regions with
the highest metabolic activity within the tumor was used to guide surgical biopsy
in a stereotactic frame [56]. Moreover, SPECT was used in the differential
diagnosis of various brain tumors [58-59], and allowed to differentiate a high-
grade tumor recurrence from radiation necrosis [60]. Some authors also suggested
that 99mTc-MIBI SPECT might help in predicting the response to chemotherapy in
patients with gliomas [61], and in establishing the prognosis of survival after
radiation therapy [62]. However, despite the development of new tracers such as
99m
Tc- Tetrofosmin [63] or 123I-Alpha-Methyl Tyrosine (IMT), potentially useful
for identifying postoperative tumor residue [64] and recurrence [65], SPECT still
lacks reliability, and cannot be used as the sole noninvasive diagnostic or
prognostic tool in brain tumors patients [66].
Second, less widely available and more expensive, Positron Emission
Tomography seems to represent a more reliable and accurate method of metabolic
imaging in brain tumors [67]. Beyond recent studies with positron emitters
presenting definite research interest in molecular imaging [68], e.g. [I-
124]Iododeoxyuridine [69] or [F-18]Fluorothymidine proposed to measure tumor
proliferation rate [70], or FIAU as an indicator of gene expression in glioma
useful for gene therapy [71], most clinical works have focused their efforts on
 Study of the Dynamic Biological Behavior of the Tumor 5

metabolic substrates such as 11C-choline [72,73], and above all 18Fluoro-2-deoxy-

2-glucose (FDG) and 11C-methyl-methionine (MET). Indeed, FDG PET can
predict tumor grade [74,75], while low-grade oligodendrogliomas and pilocytic
astrocytomas can be quite FDG avid – so FDG uptake in such lesion does not
necessarily imply a poorly differentiated histology [76]. Also, the metabolic
activity of brain tumors as shown by the PET-FDG method seems to have a good
prognostic significance [77,78], independent from histology [79,80]. Furthermore,
because brain tumors are histologically heterogeneous, PET-FDG was used to
guide stereotactic biopsies [81,82]. Indeed, while low-grade gliomas are noted to
have low levels of FDG uptake, areas of malignant degeneration show increased
metabolic activity [83], associated with an unfavorable prognosis [84]. Finally,
FDG-PET has been used to document the extent of tumor resection [85], and
differentiate brain tumors from necrosis after radiation and/or chemotherapy [86].
In a pilot study, Brock et al. (2000) even reported that FDG-PET could
differentiate responders from non responders after one cycle of temozolomide in
recurrent high-grade gliomas [87].
However, since FDG-PET has limited value in defining the extent of tumor
involvement and recurrence of low-grade gliomas, MET-PET may be preferable
for this group of lesions [76,88]. Indeed, MET-PET appears to be related to tumor
aggressivity [89], with a high uptake statistically associated with a poor survival
time [90-93] and allows to delineate the invasion of tumors (in particular low-
grade gliomas) much better than FDG-PET – thus representing a better choice for
PET guidance in neurosurgical procedures [94] an for assessing response to
therapy [95]. Furthermore, the value of the combination of FDG-PET and MET-
PET has been suggested [94], in particular in low-grade gliomas with a low
methionine uptake [80], for instance in astrocytomas – which have low levels of
MET uptake in comparison to oligodendrogliomas [96].
Finally, recent development of 18F-labeled amino acid tracers such as 18F-
alpha-methyl-tyrosine, with promising preliminary results in the evaluation of
gliomas [97], opens the field for wider use of PET scanning in the management of
brain tumors [90,98].
Third, Proton MR spectroscopy (MRS) represents a new, noninvasive tool
recently used in clinical practice to investigate the spatial distribution of metabolic
changes in brain lesions, in particular tumors [99]. Indeed, several authors have
reported increased levels of choline-containing compounds (Cho) [100] and a
reduction in the signal intensities of N-Acetyl Aspartate (NAA) and Creatine (Cr)
in brain tumors [101,102]. Indeed, Cho is thought to be a marker of increased
membrane turnover or higher cellular density [103], NAA is regarded as a
neuronal marker mainly contained within neurons [104], and Cr is a marker of
6 Hugues Duffau

energy metabolism [105]. The ranges of Cho increase and NAA decrease seem
compatible with the range of tumor infiltration [106,107]. The calculation of
metabolic maps by integrating the peak area of a metabolite of interest or some
ratios such as the Cho-NAA index for each voxel is currently a common method
to visualize these changes [108-109].
Metabolite profiles have been used to differentiate non-neoplastic lesions
such as inflammation, stroke, multiple sclerosis, gliosis and necrosis [110] from
various types of tumor, which themselves can be distinguished from one another
[111], in particular low-grade gliomas [112] / gliomatosis [113], high grade
gliomas / metastasis [114], meningiomas / hemangiopericytomas [115], and
schwannomas [116]. Metabolite maps have also helped to determine brain tumor
grade [117] and to predict the length of survival [118], notably using : the
phosphocholine / glycerophosphocholine ratio which increases with the grade of
glioma [119]; Cho levels which correlate with proliferative potential as
determined by immunohistochemical analysis of tumors biopsies using the KI-67
labelling index for gliomas [120]; Cho/Cr ratio which increases with grade [111]
while myo-Inositol [121] and Glycine [122] decrease with grade; and the lipids
which correlate with necrosis [123] then are increased in high-grade tumors
[101,124]
Also, this non-invasive method can monitor response to therapy, since the
typical change that occurs when a tumor responds to treatment is a reduction of
Cho with possibly an increase in lactate and/or lipids [125], indicating the
transformation of viable tumor cells towards necrosis. Following radiotherapy,
glioma progression could be predicted on the basis of MRS abnormalities (in
particular an increase of Cho/Cr ratio) that were outside the MRI-defined
treatment region, and can occur prior to subsequent increase in contrast
enhancement [125]. However, the sensitivity of MRS to detect tumor progression
drops when there is a mixture of necrosis and recurrent tumor [126]. The
improved spatial resolution and a more detailed spectral information using higher
field MR systems could optimize the discrimination between radiation damage
and glioma recurrence [127]. Progression to higher grade could be equally
documented using MRS [128].
Moreover, integration of SRM biochemical images of a tumor into a
stereotactic system was proposed both for optimal selection of biopsy target
[107,126,129,130,131] and during tumor resection in order to provide a better
identification of lesion border zones based on metabolic changes due to tumor
infiltration [132-134] (see paragraph dedicated to the image-guided surgery).
SRM was also used to delineate tumor extent for radiation therapy treatment
planning [135-136].
 Study of the Dynamic Biological Behavior of the Tumor 7

Finally, a combined used of PET and SRM in the evaluation of tumor

metabolism was recently proposed [137].
To be noted that the biological behavior of brain tumors can also be indirectly
studied using complementary sequences of MRI [138], i.e. diffusion weighted
imaging (DWI) [139] and perfusion weighted imaging [140]. DWI is an imaging
technique in which microscopic water motion is responsible for the contrast
within the image [141]. Indeed, the diffusion behavior of water in the brain is
characterized by its apparent diffusion coefficient (ADC) and this can be viewed
as an ADC map. Tumors with densely packed cells such as lymphomas and
medulloblastomas show restricted diffusion, while mean diffusivity values are
increased in gliomas. More specifically, ADC values for low-grade gliomas are
higher than those for high-grade gliomas, because more highly cellular gliomas
would have a smaller interstitial space and hence more restricted diffusion [142-
144]. Moreover, DWI can usefully distinguish between necrotic tumors and
abscesses [145,146].
Perfusion weighted imaging provides information about tumor tissue
perfusion by measuring cerebral blood volume (CBV), and might be used in the
preoperative classification and grading of gliomas [147]. Indeed, CBV has been
shown to correlate with microvessel cell density [148,149], and varies with tumor
grade in that maximum CBV values of low-grade gliomas seem significantly
lower than those of high-grade gliomas [150-152]. Moreover, perfusion MR
imaging could be helpful in differentiating distinct brain tumor types such as high
grade gliomas and metastasis [114,153,154] or lymphoma [155], in distinguishing
tumors from non-neoplastic lesions [156,157], and in predicting response to
therapy, in particular radiation [158] or anti-angiogenic therapy [159].
Nevertheless, this technique still lacks sensitivity [160]. Thus, it was suggested
that a combination of the perfusion image results with those of DWI and SRM
could improve the reliability of these methods, notably for tumor grading [144].
Chapter III

STUDY OF THE DYNAMIC ORGANIZATION OF

THE BRAIN

A – THE PLASTIC BRAIN

Despite the description by some pioneers of several observations of post-
lesional recovery [161-165], the dogma of a static functional organization of the
brain was settled for more than a century. This vision was essentially based on
anatomo-functional correlations performed in lesional studies, which led to the
view of a brain organized in so-called « eloquent » regions, for which any lesion
induced a neurological deficit (such as the central, Broca’s and Wernicke’s areas,
early identified), and in « non-functional » structures – with no clinical
consequence despite their damage. However, through regular reports of
improvement of the functional status following damages of cortical and/or
subcortical structures considered as « critical », this conception of a « fixed »
central nervous system was called in question in the past decades. Consequently,
many investigations were performed, initially in vitro and in animals, then more
recently in humans since the development of functional mapping methods, in
order to study the mechanisms underlying these compensatory phenomena: the
concept of cerebral plasticity was born.
Therefore, cerebral plasticity could be defined as the continuous processings
allowing short, middle and long-term remodelling of the neurono-synaptic
organization, in order to optimize the functioning of the networks of the brain –
during phylogenesis, ontogeny, physiological learning and following lesions
involving the peripheral as well as the central nervous system [166]. On the basis
of the recent literature, several hypothesis about the pathophysiological
mechanisms underlying plasticity can be considered. At a microscopic scale, these
10 Hugues Duffau

mechanisms seem to be essentially represented by: synaptic efficacy modulations

[167], unmasking of latent connections [168], phenotypic modifications [169] and
neurogenesis [170]. At a macroscopic scale, diaschisis [171], functional
redundancies [172], cross-modal plasticity with sensory substitution [173] and
morphological changes [174] are implicated. Moreover, the behavioral
consequences of such cerebral phenomena have been analyzed in human in the
last decade, both in physiology – ontogeny [175] and learning [176] – and in
pathology [177,178]. In particular, the ability to recover after a lesion of the
nervous system, and the patterns of map reorganization within eloquent area
and/or within distributed network, allowing such a compensation (especially
regarding sensorimotor and language functions), have been extensively studied –
notably in stroke [5,6,179-182].
The goal of the present article is to review the recent advances in the field of
functional brain mapping, and the applications of these technical progresses to the
better understanding of the dynamic reorganization of the eloquent maps induced
by the growth, extension and anaplastic transformation of gliomas.

B – NEW METHODS OF FUNCTIONAL BRAIN MAPPING

1) Preoperative Neurofunctional Imaging

Preoperative non-invasive techniques, including positron emission

tomography (PET) using labeled water, functional MRI (fMRI) and
magnetoencephalography (MEG)/EEG allow to perform a cortical mapping of the
whole brain, and can thus give an estimation of the location of the eloquent areas
in relation to a tumor, in order to decrease the surgical risk [183-185].

a) Positron Emission Tomography

First, cerebral blood flow PET (CBF-PET) has been used for preoperative
brain mapping of eloquent areas in patients undergoing tumor surgery,
particularly to determine the spatial relation between the lesion and the
sensorimotor cortex [186-191], the language areas [192-195] and the visual cortex
[196-198].

b) Functional MRI
However, due to the difficulties to routinely use CBF-PET in clinical practice,
many authors participated in the development of fMRI in the preoperative
 Study of the Dynamic Organization of the Brain 11

mapping of eloquent areas in the last decade [199-214]. Indeed, fMRI is a widely
available technique using the blood oxygenation level-dependent (BOLD) effect
[215,216], based upon the principle which states that functional increases of
oxygen consumption by neuronal cells induce relative increases of the local
perfusion that exceed the relative oxygen consumption changes – then induce a
decrease of the concentration of deoxygenated hemoglobin generating a higher
signal on T2*-weighted images [217,218] (Fig 1). Furthermore, due to the
improvement of the stimulation paradigms, in particular for language mapping –
by combining multiple tasks and multiple repetition of tasks [203,214] –
successful fMRI mapping can be obtained in routine with a high specificity and an
increased sensitivity [185]. Nevertheless, accumulating evidence seems to indicate
that the BOLD response in the vicinity of a brain tumor does not reflect the
neuronal signal as accurately as it does in healthy tissue [219-222], thus with a
still too low sensitivity [223]. Although poorly understood, the mechanisms seem
not to result from reduced neuronal activity, but rather from an alteration of
neurovascular and metabolic coupling [224,225].

Figure 1. Preoperative fMRI during a motor task of the right upper limb, in a patient without
any neurological deficit, harboring a low-grade glioma involving the left SMA. Interestingly,
while the left central area was activated by the movement of opening / closing the right hand,
there was a bilateral recruitment of both SMA (arrow). This pattern of activation suggests a
preoperative functional reorganization induced by the slow-growing tumor, explaining the
absence of deficit. The reshaping may help to perform a complete surgical resection, despite the
transient occurrence of a postoperative SMA syndrome (from Fontaine, Capelle and Duffau
[557]).
12 Hugues Duffau

In this way, to be noted that diffuse optical imaging and near-infrared

spectroscopy (NIRS), which offer the potential of non-invasively quantifying
changes in deoxyhemoglobin and total hemoglobin concentrations, thus enabling
the distinction between oxygen comsumption and blood flow changes during
brain activation [226-228], have been used preoperatively in patients with brain
tumors, and compared to BOLD in order to try to explain false-negative
activations in fMRI [229,230]. It seems that these false-negative fMRI activations
could be caused by atypical evoked-cerebral blood oxygenation changes, i.e. an
increase in deoxyhemoglin due to the lesion, as shown by NIRS [229], instead of
a decrease of deoxyhemoglobin classically induced by neuronal activation in
healthy volunteers [231].

c) Magnetoencephalography
Magnetic source imaging (i.e. magnetoencephalography) (MEG), eventually
combined to electroencephalography, is a non-invasive method of measuring
extracranial magnetic fields generated by intraneuronal electric currents [232]. As
magnetic fields are relatively unaffected by the different electrical conductivities
of the brain, cerebrospinal fluid, skull and skin, MEG can accurately localize the
origin of intraneuronal electric currents that contribute to extracranial magnetic
fields [233]. Interestingly, this technique is becoming available at an increasing
number of clinical centers world-wide as an adjunct in the planning and guidance
of brain tumor surgery: indeed, MEG has been extensively used for sensorimotor
[234-242], language [243-246], auditory [247,248] and visual [249,250] mapping.
Furthermore, it was suggested a possible role of MEG as a measure of tumor
infiltration [251], due to a delta and theta activity located close to the lesion, while
a gamma activity was recorded in the controlateral hemisphere [252]. Also, a
correlation between high signal powers in the delta band and the aggressivity of
the tumor was described, because of the structural damage done by the lesion (but
not by the treatment) on the surrounding white/gray matter [253].

d) Magnetic Transcranial Stimulations

Finally, to be also noted that some authors have suggested to use Transcranial
Magnetic Stimulations (TMS) as a tool for presurgical functional mapping [186,
254-259]. TMS, based on the principle of electromagnetic induction, is a safe,
non-invasive, painless and reversible method for intervening with neural
processes via a pulse of current passing through a coil placed over the skull [260].
This method may represent a useful adjunct to the other functional neuroimaging
techniques both for preoperative planning and decision making, in particular
concerning tumors near rolandic cortex [261,262].
 Study of the Dynamic Organization of the Brain 13

In addition, to be noted that some authors have proposed the combination of

these different preoperative neurofunctional imaging methods [187,196,204,263-
265] and also the combination of metabolic and functional neuroimaging.
Such individual data defining the spatial relation between the lesion and
surrounding eloquent areas are useful for the selection of surgical indications,
depending on the assessment of the feasibility of tumor resection [266-268].
Moreover, when the operation is decided, these techniques participate to the
surgical planning, i.e. (1) the choice of the modalities of surgery, in particular the
selection of patients for awake craniotomy if the tumor is located within the
dominant hemisphere as determined using preoperative neurofunctional imaging
[269-277] (see below, paragraph dedicated to the intraoperative electrical
mapping techniques); (2) the identification of the least traumatic neurosurgical
approach using functional neurosurgical simulation [278] and (3) the
determination of the limits of resection in order to preserve the functional
structures. Nevertheless, these methods are not able to differentiate the areas
essential for the function, which should be surgically preserved, from the
“modulatory” areas, which can be functionally compensated and so potentially
resected without permanent deficit [7]. Also, they do not have the possibility to
map the white matter.

2) Preoperative Diffusion Tensor Imaging

Indeed, although these functional neuroimaging methods are sensitive to

changes in the grey matter, they provide only limited information concerning the
integrity of the white matter structures [279]. Since surgical interruption of these
tracts can lead to major disruptions in neurological functions, it was recently
suggested to use a new pre-operative non-invasive technique of white matter
pathways tracking: the diffusion tensor imaging (DTI). This is a modification of
DWI that is sensitive to the preferential diffusion of brain water along white
matter fibers and can detect subtle changes in white matter tracts in disease
[141,280]. Thus, working on the principle that diffusion of water molecules
parallel to the white matter fibers is less restricted that water diffusion
perpendicular to them – i.e. “diffusion anisotropy” – , this technique is able to
map the main bundles [281-288].
Recently, DTI has been applied to the therapeutical management of patients
harboring a brain tumor. First, measures of mean diffusivity and fractional
anisotropy could be used in order to differentiate normal white matter, edematous
brain and enhancing tumor margins [289,290]. Indeed, the anisotropy is reduced
14 Hugues Duffau

in cerebral lesions, due to the loss of structural organization [291]. It seems that
abnormalities on DTI are larger than those seen on T2-weighted images in (high
grade) gliomas, but not in the metastasis [292]. Some authors have suggested that
measurement of fractional anisotropy value could predict histological
characteristics such as cellularity, vascularity and/or fiber structure in astrocytic
tumors [293]. Such a tool for assessing white matter tracts invasion can improve
the targeting of radiation to visible tumor as well as encompassing “invisible”
tumor infiltrating white matter pathways. Second, DTI may distinguish if the
white matter fibers are displaced [294,295], infiltrated or disrupted by the tumor
[296]. Such a knowledge could participate to the selection of the surgical
indications. Third, DTI is able to identify the subcortical connections [297,298],
eventually in a combination with the functional neuroimaging methods [299,300],
then allowing to map the individual anatomo-functional connectivity. These
informations are very useful for the presurgical planning, by delineating the
spatial relationships of the eloquent structures and lesions, in order to preserve the
functional pathways intraoperatively [301-305].
However, this new method needs currently to be validated before it can be
used routinely in surgical procedures [306].

3) Methods of Intraoperative Functional Brain Mapping

a) Image-guided Surgery: Functional Neuronavigation

Neuronavigation, based upon registration of the physical space of the head of
the patient in the operating room to the virtual space of an MR or CT image set, is
currently widely applied to brain surgery. The integration of PET [307], fMRI
[308-313], MEG [314-319], DTI [320-323], SRM [133] or even multimodal
imaging [324-327] into frameless stereotactic surgery is often referred to as
“functional neuronavigation” [326,328]. In addition, to be noted that integration
of functional brain informations into a stereotactic space is also used for radiation
planning [329].
Nevertheless, despite an accurate registration between the patient’s physical
space and intraoperative images extensively studied and evaluated approximately
between 1 to 4 mm [330,331], it is mandatory to be careful with image-guided
surgery for (voluminous) tumors, because of the high risk of intraoperative brain
shift, due to surgical retraction, mass effect, gravity, extent of the resection or
cerebrospinal fluid leakage [332-336]. Indeed, intrasurgical displacement of the
parenchyma could lead to functional damages, especially concerning the
subcortical pathways along and at the end of the resection. For instance, it was
 Study of the Dynamic Organization of the Brain 15

recently reported the case of a right temporo-insular glioma, operated using

integration of spatial three-dimensional information concerning the pyramidal
tracts acquired using anisotropic diffusion-weighted MRI into a customized
system for frameless neuronavigation: during surgery and tumor decompression,
navigation became inaccurate because of brain shift, and the patient presented
postoperative hemiplegia due to damage of the internal capsule, confirmed by a
control MRI [320].
Several technical improvements have been recently proposed in order to
reduce the effects of brain shift. First, the combination of neuronavigation system
with data from intraoperative ultrasound, which produces real-time imaging, has
provided the opportunity to partially overcome errors caused by tissue movement
[337-347]. Second, the use of mathematical models and computational methods
based on data from intraoperative ultrasound or digital images that track cortical
displacement and movements of known landmarks has been suggested [348-351],
while complex, expensive and time consuming [352]. Third, the recent
development of intraoperative MRI has permitted the acquisition of high-quality,
multiplanar and real-time imaging during surgery [353-370], allowing brain shift
compensation [352,371]. Then, intraoperative MRI was used for surgical decision
making [372], to guide brain biopsy as well as detect any immediate
complications (e.g. haemorraghe) [373-375], and to determine the extent of tumor
removal during tumor surgery, in particular in gliomas: if the resection appears
incomplete, the surgeon can remove the residue during the same procedure, then
optimize the quality of glioma removal [376-383]. Furthermore, this technique has
been improved in efficacy and simplicity due to the development of intraoperative
high-field-strength MR imaging (1.5 T) [364,384-387] replacing the first imagers
based on magnets with field strengths of 0.5 T or less. In addition, the use of
intraoperative functional MRI was recently reported [388].
Finally, to be noted that other non-electrophysiological methods of metabolic
and functional mapping have also been used intraoperatively. First, it was
demonstrated that intrinsic signal optical imaging can be performed during
operative procedures with sufficient spatial resolution to accurately map eloquent
areas, including sensorimotor, memory, and language cortices [389-398]. Also,
enhanced optical imaging obtained intraoperatively before and after injection of
indocyanine green has been shown as facilitating the localization of tumor,
identifying the tumor remaining at the resection margins, and determining the
grade of the tumor [399]. Fluorescence-guided resection of gliomas was also
reported [400-407], with the goal to optimize the quality of tumor removal.
Moreover, it was suggested that intraoperative characterization of gliomas by
NIRS (near-infrared spectroscopy), based on the study of the intratumoral
16 Hugues Duffau

microvascular blood volume and oxygen saturation, possibly related respectively

to angiogenetic activity and non-oxidative glucose metabolism of the lesion,
might represent a prognostic factor [408]. NIRS indocyanine green video
angiography was also used to document the intraoperative blood flow [409].
Finally, the use of a cooling probe (thermal inactivation) as a safe and useful tool
for intrasurgical functional mapping was recently reported [410-412].

b) Invasive Electrophysiological Mapping

Despite the development of functional neuroimaging, but due to its current
limitations, invasive electrophysiological investigations currently remain the
“gold-standard” for brain surgery, in particular concerning tumors located near or
within eloquent cortical and/or subcortical structures [413]. Different methods are
available.
First, the technique of evoked potentials was extensively used. For
intraoperative identification of the sensorimotor region, stimulation of a peripheral
nerve (median nerve or tibial nerve) with recording of the somatosensory evoked
potentials from the cortex can be used [414-422]. However, the reliability of
cortical somatosensory evoked potentials and phase reversal phenomena in the
rolandic sulcus is not optimal, with accurate localization of the central sulcus
reported only between 91% and 94% [416,421-423]. In a recent review, the
overall sensitivity and negative predictive value of somatosensory evoked
potentials monitoring was 79% and 96%, respectively [424]. Moreover, phase
reversal recording identifies only the central sulcus itself, but offers no direct
information on the particular distribution of motor function on the adjacent
exposed cerebral structures [414,416]. Additionally, in case of subcortical tumor
removal, the resection is stopped on the basis of indirect data, i.e. when the
evoked potentials begin to be altered, but this method is unable to provide direct
information about the exact location of the thalamo-cortical ascending pathways,
then a fortiori about the location of the pyramidal descending fibers.
Consequently, there is a permanent double risk, either to detect and/or interpretate
modifications of the evoked potentials while the subcortical tracts are already
damaged, or to have a higher sensitivity of these evoked potentials leading to
interrupt prematurely the glioma removal while the resection is still not in contact
of the functional pathways.
Whereas the method of motor evoked potentials was improved [425-427],
using modification of electrical parameters [428], repetitive intraoperative
stimulations of the motor cortex rather than single stimulation [429] and the
combination with evoked potential phase reversal [416,430,431], several
problems persist. First, when recording compound muscle action potentials, only
 Study of the Dynamic Organization of the Brain 17

the monitored muscles can be controlled, that is, there is an inability to detect and
possibly avoid motor deficits in nonmonitored muscles. For this reason, Cedzich
et al. suggested that monitoring of « all muscle groups at risk » seemed necessary
[416]. However, in case of wide LGG involving subcortical regions, where the
pyramidal tracts converge (such as the corona radiata and the internal capsule), all
parts of the controlateral hemibody should be controlled, without the possibility to
define before resection some « muscle groups at risk » to monitore - and even
with a loss of the classical somatotopy in the internal capsule in some cases of
insular gliomas, thus with an impossibility to predict which muscles need to be
preferentially controlled at the time of the stimulations. Second, as previouly
mentioned concerning somatosensory evoked potentials, motor evoked potentials
give only indirect information about the location of the pyramidal pathways, even
in case of repetitive stimulations, and do not allow the direct identification of
motor tracts when the resection reaches them. In the same way, although a recent
work showed that a reduction in amplitude larger than 80% and a prolonged
latency more than 15% can be interpreted as intraoperative warning signs of risk
of mechanical damage to the motor system leading to stop the resection [429], the
same authors underlined that the occurence of a complete or nearly complete and
sudden nonartifactual reduction in amplitude could be attributed to a lesion of
subcortical pyramidal fibers, and that these irreversible changes in potential
cannot serve as a warning sign in such cases – because they occur only after the
damage [429]. These limitations of the evoked potential techniques may explain
that still 20% of postoperative definitive deficits, mainly due to resection of
subcortical lesions in the immediate vicinity of the pyramidal tract, have been
reported by Cedzich et al., who concluded that « an additional method is
necessary in patients requiring localization deep in the white matter and when
tumors involving motor pathways are to be removed » [416].
Finally, intraoperative evoked potentials are not currently able to map quickly
and with reliability language, memory and other higher functions.
Consequently, in order to have more time to perform numerous functional
tasks, with the goal to benefit from an extensive, reproducible and reliable cortical
mapping, many authors prone the use of extraoperative electrophysiological
recordings and stimulation via the implantation of subdural grids [432-439].
Using this method, the patient is in optimal conditions, in his room, to perform the
tasks: this point is particularly important for children [440]. Moreover, this
technique permits to identify seizure foci, then to plan the extent of the resection,
in patients who will undergo surgery for intractable epilepsy [441-443]. Finally,
recent advances in the interpretation of the electrophysiological signal, such as
electrocorticographic spectral analysis evaluating the event-related
18 Hugues Duffau

synchronization in specific band of frequency [444-447], have allowed a better

understanding of the organization of the functional cortex, and a study of the
connectivity, in particular via the recording of “cortico-cortical evoked potential”
[448].
However, extraoperative electrophysiological mapping usually used grids
with 1 cm-spaced electrodes, thus with a limited accuracy. Moreover, it is not
possible to map the subcortical white matter. Also, it is necessary to perform two
surgical procedures, one to implant grids and a second to resect the lesion. Finally,
there is still a risk of infectious complications due to the presence of subdural
grids during several days [449].
Taking into account the advantages and the limits of these different mapping
techniques, more and more neurosurgeons prone the additional use of
intraoperative direct electrical stimulation (DES), under general or local
anesthesia during surgery of tumors in eloquent areas [450-476] (Fig 2). DES
allows the mapping of motor function (possibly under general anesthesia, by
inducing unvoluntary motor response if stimulation at the level of an eloquent
site), somatosensory function (by eliciting dysesthesia described by the patient
himself intraoperatively), and also the mapping of cognitive functions such as
language (spontaneaous speech, oject naming, comprehension, etc…), calculation,
memory, reading or writing, performed in these cases on awake patients – by
generating transient disturbances if the stimulation is applied at the level of a
functional “epicenter” [477].
Furthermore, DES also permits the study of the anatomo-functional
connectivity by directly stimulating the white matter tracts all along the resection
[198,413,450,478-490] (Fig 2). In this way, it is important that a speech therapist
be present in the operative room, in order to interpret accurately the kind of
disorders induced by the cortical and subcortical stimulations all along the
surgery, for instance speech arrest, anarthria, speech apraxia, phonological
disturbances, semantic paraphasia, perseveration, anomia, and so on [491]. Such
on-line intraoperative anatomo-functional correlations give an unique opportunity
to study the individual effective connectivity, as demonstrated concerning (1)
motor pathways and their somatotopy from the corona radiata to the internal
capsule [482,492] and the superior part of the mesencephalic peduncles [493] (2)
thalamo-cortical somatosensory pathways [492] (3) subcortical visual pathways
[494], and language pathways – concerning loco-regional connectivity, cortico-
cortical connections such as the phonological loop [495], striato-cortical loop such
as the subcallosal medialis fasciculus, as well as long-distance association
language bundles such as the arcuate fasciculus [483] or the inferior fronto-
occiptal fasciculus involved in the semantic connectivity [496].
 Study of the Dynamic Organization of the Brain 19

Figure 2. Preoperative anatomical MRI showing a left LGG involving “Broca’s area” (upper
photographs). Intraoperative views before and after resection of the tumor (middle
photographs). Electrical mapping shows a reshaping of the eloquent maps, with a recruitment of
perilesional language sites (i.e. the ventral premotor cortex, dorsolateral prefrontal cortex and
pars orbitaris of the inferior frontal gyrus, marked by the cortical number tags) allowing the
compensation of the “Broca’s area” here removed. In the depth, the resection was continued up
to the contact of the language pathways, in particular the insulo-frontal connections – marked
by the subcortical number tags (from Duffau, Capelle, Sichez et al. [483]). A = Anterior, P =
Posterior. Postsurgical control MRI, demonstrating a complete glioma removal.

Therefore, DES represents an accurate, reliable and safe technique of on-line

detection of the cortical and subcortical regions essential for the function, at each
place and each moment of the resection. Consequently, in all cases, a functional
disturbance induced by DES with reproducibility must lead to interrupt the
20 Hugues Duffau

resection at this level, both for cortical as well as subcortical structure. The tumor
removal is then performed according to functional boundaries, in order to
optimize the quality of tumor removal while minimizing the risk of postoperative
permanent deficit.
However, DES allows only a loco-regional mapping, and not of the whole
brain, and they are time-consuming, thus with a limitation of the number of tasks
that can be used during surgery.
Therefore, combination with other metabolic and functional non-invasive and
invasive methods seems currently mandatory.

4) Correlations Between Preoperative Neurofunctional Imaging

and Intrasurgical Stimulation

Many studies have tried to correlate intraoperative electrical stimulations and

preoperative neurofunctional imaging [497] – PET [191,192,307,498-499], fMRI
[500-512] and MEG [241,513-519]. These correlations were made using
intraoperative photographs or neuronavigation, by reporting the eloquent cortical
sites detected by stimulations, on a preoperative 3D surfacic reconstruction with
activations identified by fMRI.
Although it was found what could be called “satisfactory” correlations, in our
experience like in some clinical studies, namely with data agreement between
80% to 100%, particularly concerning motor function (87% for Yetkin et al.[520],
87% for Roux et al. [521]; 92% for Lehéricy et al.[522]), discrepancies were also
widely reported – both in physiology using animal experimentations [523], and
also in patients harboring a tumor, notably in language areas (sensitivity of fMRI:
77% for Hirsch et al.[203]; 66% for Roux et al.[223]).
Several sources of error in comparing functional neuroimaging and
intraoperative electrical mapping have been suggested. First, craniotomy and
debulking may induce deformation, which reduces image registration [524,525].
Second, the extent of areas activated by fMRI depends on the statistical thresholds
that were chosen, directly influencing the distance between locations found with
fMRI and those found with electrical mapping [517]. Third, the paradigms applied
for neurofunctional imaging and intraoperative stimulation cannot be exactly the
same because of different setups [504]. Fourth, mapping principles are radically
different: functional neuroimaging shows all brain areas involved during the
performance of a voluntary task, whereas direct electrostimulation only points at
brain tissue essential to the task, by disturbing the function against the will of the
patient.
 Study of the Dynamic Organization of the Brain 21

Nevertheless, despite these factors which can explain discrepancies between

functional neuroimaging and intraoperative stimulation, the lack of complete
concordance raises the question about the exact specificity and sensitivity of
neurofunctional imaging concerning the identification of functional areas in the
field of surgical planning. Since this problem is currently unsolved, it seems that
intraoperative electrical mapping is still mandatory during brain surgery in or near
eloquent areas [223].
Chapter IV

STUDY OF THE DYNAMIC INTERACTIONS

BETWEEN THE TUMOR AND THE BRAIN

A – BRAIN PLASTICITY INDUCED BY THE TUMOR

1) Preoperative Plasticity

It could seem surprising that numerous patients harboring a brain tumor,

especially LGG usually revealed by seizures, have no neurological deficit, in spite
of the frequent invasion of eloquent structures [526]. This means that these slow-
growing lesions have likely induced progressive functional brain reshaping, as
suggested by preoperative neurofunctional imaging [501]. Interestingly, the
patterns of reorganization may differ between patients, a notion very important to
know by the neurosurgeon with regard to both indication of surgery and surgical
planning [527]. Indeed, despite the limitation of the preoperative neurofunctional
imaging previously detailed, these methods have shown that three kinds of
preoperative functional redistribution are possible, in patients without any deficit.
In the first one, due to the infiltrative feature of gliomas, function still persists
within the tumor, thus with a very limited chance to perform a good resection
without inducing postoperative sequelae [268]. In the second one, eloquent areas
are redistributed around the tumor [186,200], thus with a reasonable chance to
perform a near-total resection despite a likely immediate transient deficit – but
with secondary recovery within some weeks to some months. In the third one,
there is already a preoperative compensation by ispsilesional remote areas [528-
530] and/or by the contra-hemispheric homologuous [194,222,501,531-535]:
consequently, the chances to perform a real total resection of this kind of gliomas
are very high, with only a slight and very transient deficit (Fig 1).
24 Hugues Duffau

Therefore, in cases of brain lesions involving eloquent areas (i.e. the

structures supporting the sensorimotor, language or other cognitive functions),
plasticity mechanisms seem to be based on an hierarchically organized model, i.e.:
first with intrinsic reorganization within injured language areas (indice of
favorable outcome) [528]; second, when this reshaping is not sufficient, other
regions implicated in the functional network are recruited, in the ipsilateral
hemisphere (close and even remote to the damaged area) then in the controlateral
hemisphere if necessary.

2) Intraoperative Plasticity

Intraoperative stimulation before any resection has allowed the confirmation

of the existence of a functional reshaping induced by brain lesions (Fig 2), in
particular concerning remapping of the motor homonculus [536].
Moreover, acute reorganization of functional maps was equally observed
during the resection, likely due to the surgical act itself which can generate a loco-
regional hyper-excitability [537] – as already demonstrated in head injury.
Indeed, in several patients harboring a frontal lesion, although stimulation of
the precentral gyrus induced motor responses only at the level of a limited number
of cortical sites before the resection, an acute unmasking of redundant motor sites
located within the same precentral gyrus and eliciting the same movements than
the previous adjacent sites when stimulated, was observed immediately following
lesion removal [537]. Acute unmasking of redundant somatosensory sites was
also regularly observed within the retrocentral gyrus in patients operated on for a
parietal glioma [538]. Furthermore, it was equally possible to detect a
redistribution within a more larger network involving the whole rolandic region,
i.e. with unmasking of functional homologuous located in the precentral gyrus for
the first cortical representation and in the retrocentral gyrus for its redundancy (or
vice versa) [539].
Finally, intraoperative mapping has also a prognostic value concerning the
postoperative recovery [540].

3) Postoperative Plasticity

The mechanisms of such a plasticity induced by surgical resection within

eloquent areas were also studied, by performing postoperative neuroimaging once
the patient has recovered his preoperative functional status [541]. In particular,
 Study of the Dynamic Interactions between the Tumor and the Brain 25

several patients were examined following the resection of gliomas involving the
supplementary motor area (SMA), which has elicited a transient postsurgical
SMA syndrome (see below). Functional MRI showed in these cases, in
comparison to the preoperative imaging, the occurrence of activations of the SMA
and premotor cortex contralateral to the lesion: the contrahemispheric
homologuous then likely participated to the post-surgical functional compensation
and recovery [542] (Fig 3).

Figure 3. Postoperative fMRI during a motor task of the right upper limb, following a total
resection of a LGG involving the left SMA, which have generated a transient SMA syndrome
then a complete recovery. In addition to a classical activation of the left central area, this fMRI
shows a recruitment of a the controlesional SMA and premotor cortex (arrows), likely
implicated in the postsurgical functional compensation (from Krainik, Duffau, Capelle et al.
[542])

B – THE SURGICAL USE OF BRAIN PLASTICITY

Such pre-, intra- and post-operative brain plasticity mechanisms are very
useful for the neurosurgeons, since it is possible to apply this brain dynamic
potential in order to extend the indications and the limits of glioma resection
located in the so-called “eloquent” areas, without inducing a definitive
neurological deficit [7].
26 Hugues Duffau

1) Resection of Gliomas Involving the SMA

The resection of the frequent LGG invading the SMA [543], namely the
frontomesial area located in front of the primary motor area of the inferior limb,
which is involved in the planning of the movement [544-546], induces the
classical “SMA syndrome” [209,431,465,547-553]. This syndrome is
characterized by a complete akinesia and even mutism in cases of lesions of the
left dominant SMA, which occurs approximately thirty minutes following the end
of the resection, as observed in awake patients [554]. Then, this syndrome
suddenly and spontaneously resolves around the tenth day following surgery, even
if some rehabilitation is often needed during 1 to 3 months in order to allow a real
complete functional recovery.
Using preoperative fMRI, it was shown that the occurrence of this syndrome
is not related to the volume of the frontal resection, but directly to the removal of
this specific structure called the “SMA-proper”, detectable on the preoperative
functional neuroimaging (Fig 1). Thus, on the basis of the presurgical fMRI, it is
now possible to predict, before surgery, if a SMA syndrome will occur or not
postoperatively, and to inform the patient and his family [555,556].
Moreover, by coupling preoperative fMRI, the pattern of clinical deficit after
surgery, and the extent of resection on the postoperative MRI, it was demonstrated
the existence of a somatotopy within the SMA-proper – namely, from anterior to
posterior: the representation of language (at least in the dominant hemisphere), the
one of the face, then the superior limb, then the inferior limb (just in front of the
paracentral lobule) [557]. Thus, it is possible to predict before surgery the severity
and the pattern of the postoperative transient deficit, for instance only mutism, or
mutism and akinesia of the superior limb, or akinesia of the entire hemibody. This
has an important impact concerning the planning of a specific rehabilitation.

2) Resection of Gliomas Involving the Insular Lobe

The insular lobe also represents a structure frequently involved by tumors,

especially LGG [543]. While poorly studied during a long time for technical
reasons, it seems that the insula is an anatomical, cyto-architectonic and
functional interface between the allocortex and neocortex [558]. Recent
development of functional mapping methods has allowed to better understand the
implication of this multimodal lobe in many functions, in particular language
[559].
 Study of the Dynamic Interactions between the Tumor and the Brain 27

In brain tumor surgery, preoperative fMRI has regularly showed an activation

of the anterior insular cortex in the dominant hemisphere during language tasks,
as reported in healthy volunteers [560]. Moreover, these results were confirmed
by intraoperative electrical stimulations, which induced language disorders, and
more specifically articulatory disturbances when applied on the insular cortex
[493,561,562], supporting the role of this structure in the complex planning of
speech, as previously suggested in some stroke studies [563]. These data have
important implications for the neurosurgeon, since in left dominant (fronto-
temporo)-insular glioma, resection has a high risk to be incomplete. However, in
gliomas invading the sole left dominant insula, despite its “essential” role in
language, a complete surgical removal was nevertheless possible in several
patients without postoperative aphasia – due to language compensation by the
frontal and temporal operculae, and also deeply by the left putamen, as shown
preoperatively using fMRI and confirmed intraoperatively by electrical
stimulations [564].
Moreover, following resection of LGG involving the right non-dominant
insulo-opercular structures, the induction of a transient Foix-Chavany-Marie
syndrome was observed, i.e. a bilateral facio-linguo-pharyngo-laryngal palsy, with
a unability for the patient to speak and swallow [565]. Again, there is nevertheless
a reversibility of the symptoms, then in practice with the ability to perform
resection of an insular LGG without inducing definitive sequelae.

3) Resection of Gliomas Involving “Broca’s Area”

In the same way, it was regularly possible to remove gliomas involving the
pars opercularis and pars triangularis of the left inferior frontal gyrus, namely
Broca’s area, without generating any aphasia, due to a perilesional reorganization
of language areas, in particular in the ventral premotor cortex – an area
demonstrated to play a major role in articulation [491] – behind the lesion and in
the pars orbitaris of the inferior frontal gyrus in front of the glioma (as
demonstrated by electrical stimulations, which also allowed the preservation of
the insula and subcortical language pathways in the depth of the cavity [7]) (Fig
2).
28 Hugues Duffau

4) Resection of Gliomas Involving the Primary Sensorimotor Area

of the Face

It was also possible to remove the primary sensorimotor area of the face
without eliciting permanent postoperative central facial palsy, but only within the
non-dominant hemisphere [566]. In these cases, the subcortical motor sites which
represented the deep functional boundaries of the resection, corresponded to the
pyramidal pathways of the upper limb, running under the representation of the
face previously removed [492].

5) Resection of Gliomas Involving the (non dominant) Striatum

Concerning subcortical structures, compensation was equally possible, in

particular in low-grade gliomas involving the right fronto-temporo-insular
structures and the striatum, with a total resection without permanent palsy and
without movement disorders [567].
However, to be noted that intraoperative stimulation of the dominant striatum
was recently reported as inducing systematic language disorders, namely
perseveration during stimulation of the head of the caudate nucleus and anarthria
during stimulation of the lentiform nucleus [568]. Consequently, it was suggested
to surgically preserve the dominant striatum, even if invaded by a glioma, until
the understanding of the actual implication of this structure in language and other
cognitive function is improved.

6) Resection of Gliomas Involving the Corpus Callosum

Interestingly, it has also been recently reported that resection of low-grade

gliomas involving the corpus callosum was possible without generating
neurological deficit and without any consequence on the patient’s quality of life,
whatever the location of the “callosectomy” [569].

7) Other Locations

To be mentioned that this list is not exhaustive, and that gliomas involving
other “eloquent” regions have been also removed without generating permanent
neurological deficit, owing to the compensatory ability of the brain studied using
 Study of the Dynamic Interactions between the Tumor and the Brain 29

pre- and intra-operative functional mapping methods, e.g. tumor invading the
frontal eye fields [570-572], the left angular gyrus despite its implication in
calculation [573], the left dominant postero-temporal regions near the
“Wernicke’s area” [574,575], the regions involved in writing [576], reading [577],
bilinguism [578,579], or even control of micturition [580].

C – THE SURGICAL GUIDANCE OF BRAIN PLASTICITY

Recently, the surgical use of long term functional reshaping induced by a first
surgical act itself was also suggested [7].
Indeed, it seems that the intraoperative acute unmasking of redundancies
described during a surgical resection [537,539] could have a real functional role,
i.e. that the “latent” networks desinhibited during tumor removal might be
reinforced and then might lead to a durable remapping. Interestingly, this
functional reorganization generated by the first surgery could be useful to
consider for an eventual re-operation, with a possibility to extend the tumor
removal without eliciting sequelae [581].
For instance, in cases of precentral glioma, homologuous generating the same
motor responses than previous sites, also localized within the precentral gyrus,
were identified by stimulation in some patients, after incomplete resection of the
tumor because of invasion of the primary motor area of the hand. Due to a
recurrence some years later, a new surgery was performed also using
intraoperative electrical mapping. Stimulation showed a motor map reshaping,
with essential areas now corresponding to the unmasked sites during the first
procedure, thus allowing to perform this time a total glioma removal without
deficit [581]. These long-term plasticity phenomena induced by surgical resection,
and maybe also by glioma continued growth, have also been used to extend tumor
removal in other eloquent regions, during a second surgery when total resection
was not possible initially. In particular, removal of primary somatosensory areas
and language sites have been done without permanent deficit in re-operated
patients [581].
In conclusion of this part, it seems important that the neurosurgeon gains a
better knowledge of these plasticity phenomena, and their variability among
patients, in order to try to integrate this potential in the surgical indications and in
a dynamic surgical planning. In other words, the extent of resection and the
number of surgical acts necessary to perform this resection should be adapted to
the individual potential of functional compensation, thus to its limits.
Chapter V

SURGICAL RESULTS

The development of non-invasive and invasive metabolic and functional

mapping methods has allowed the improvement of the results of brain tumor
surgery in the past decade, both on a functional and an oncological point on view.

A – FUNCTIONAL RESULTS
The integration of individual functional mapping, connectivity and plasticity
in the surgical decision and planning has permitted first to extend the indications
of surgery for tumors located in areas considered until now as “inoperable” [582].
Moreover, despite a frequent but transient immediate postoperative functional
worsening (due to the attempt to perform a maximal tumor removal), in a delay of
3 months following the surgery, 95% of patients recovered a normal neurological
examination, even with a possible improvement in comparison with their
preoperative status [241,307,309,455-457,459,463,465,468,473-
476,484,485,501,551,582-585] – and also with a significant decrease of seizures
in 80% of patients with preoperative chronic epilepsia [561]. All these patients
returned to a normal socio-professional life.
Interestingly, in comparison, in series which did not use intraoperative
electrical mapping, the rate of sequelae ranged from 13 to 27.5%, with a mean
around 19 % [586-593].
32 Hugues Duffau

B – NEURO-ONCOLOGICAL RESULTS
Since mapping techniques allow to identify the cortical and subcortical
eloquent structures individually, it seems logical to perform a resection according
to functional boundaries. Indeed, it has been suggested to continue the resection
until the functional structures are detected by DES, and not before, in order to
optimize the quality of resection – without increasing the risk to generate
postoperative permanent deficit [492,582]. This surgical strategy permits a
significative improvement of the quality of tumor removal, despite a higher
number of surgeries within critical areas, and a parallel decrease of the rate of
sequelae [582].
Moreover, while extensive surgery is still controversial, in particular
regarding low-grade gliomas, the current surgical results support the positive
impact of such a “maximalist” treatment strategy, i.e. with a likely benefit on the
natural history of the tumors which seems to be related to the quality of resection
[582]: these results are in accordance with the recent surgical series of the
literature [583,594-606].
Chapter VI

CONCLUSIONS AND PERSPECTIVES

Brain tumor surgery may now benefit from a better understanding of (1) the
dynamic biological behavior of the tumor (2) the dynamic organization of the
brain (3) the dynamic interactions between the growth, extension ± anaplastic
transformation of the glioma and the reactional plastic phenomena of the nervous
system allowing a functional compensation of the damage induced by the lesion
and even by the surgical act itself.
Indeed, this better knowledge is currently possible owing to the important
technical developments in the field of metabolic and functional mapping, using
both non-invasive methods of neuroimaging and intraoperative
electrophysiological investigations. Furthermore, recent progress in neurosciences
allow to integrate new concepts about the functioning of the central nervous
system in the surgical strategy, namely: the study of individual functional brain
organization, of anatomo-functional connectivity, and brain plasticity potential.
All these recent advances are useful for the neurosurgeon, since they allow
(1) the extension of surgical indications, in particular in eloquent brain areas ; (2)
a better quality of glioma resection with a greater neuro-oncological impact ; and
(3) a minimization of the risk of postoperative sequelae, with preservation of the
quality of life.
Several perspectives could be considered to continue to improve brain surgery
in eloquent regions.
34 Hugues Duffau

1) Methodological Perspectives: Improvement of the Reliability of

Neuroimaging

The first perspectives concern methodological developments, especially the

improvement of fMRI reliability. Since the BOLD signal (as PET scan with
labeled water) is an indirect reflect of the neurono-synaptic activity [607] (which
conversely is directly studied using MEG / EEG and electrical stimulations), it is
mandatory to better understand the mechanisms of neuro-vascular coupling if we
want to increase the sensitivity and specificity of fMRI. In this way, recent
biological models, based on the preliminary results of metabolism studies using
FDG-PET or MRS, have shown the likely role of the astrocyte at the interface
between electrical and hemodynamic activities [608], and may help in the
improvement of the interpretation of the BOLD signal, in particular in patients
with brain tumor [609].

2) Pathophysiological Perspectives

In order to improve the understanding of the “effective” connectivity

underlying the functional networks [610], it seems interesting to combine the data
provided by the diffusion tensor MRI (anatomical informations), MEG (temporal
data), fMRI and PET (perioperative functional data), electrophysiology
(intraoperative functional data), with the aim to elaborate an individual and
predictive model of the functioning of neurono-synaptic circuits [611].
Second, it is also mandatory to improve the pre-, intra- and post-operative
functional assessments for each patient, with the goal to better study the spatio-
temporal reshaping of the networks and their functional consequences, namely the
mechanisms of brain plasticity [612].

3) Surgical Perspectives

The first goal is to better select the surgical indications in brain tumors. It
necessitates to increase the homogeneity and the follow-up of surgical series, and
to elaborate prospective studies in order to better evaluate the actual impact on the
natural history of tumors, in particular LGG.
When surgery is decided, the aim is to optimize the Benefit / Risk ratio. On
the basis of the results previously detailed, it seems necessary to use brain
mapping methods, in order to detect then preserve the essential functional areas,
 Conclusions and Perspectives 35

and also to have an evolution toward an individual dynamic planning of multiple

surgeries (1) based on the knowledge of the functional organization of eloquent
areas for each patient (2) based on the use of the plastic potential, and (3) with the
aim to maximize the glioma resection while minimizing the risk of sequelae.

4) Oncological Perspectives

Concerning the neuro-oncological perspectives, the main goal is to better

understand the natural history of tumors, to identify spontaneous prognosis
factors, and to evaluate the impact of treatments (surgery, chemotherapy,
radiotherapy) and their association: thus it is necessary at least to follow very
regularly each patient clinically and by MRI, whatever the therapeutic options.
Second, it is needed to continue to precise the exact role of the surgery in the
therapeutic strategy of this kind of tumors, namely : (1) should the surgery be
performed only if (sub)total resection is possible ? (2) when should the
complementary treatment (chemotherapy / radiotherapy) begin in case of re-
growth following a subtotal resection ? (3) should (new) surgery be considered in
case of response of a glioma under chemotherapy, allowing a better resection ? (4)
is conformational radiotherapy following a resection according to functional
boundaries more risky, due to a potential interaction with brain plasticity ?

5) Quality of Life

Finally, it is mandatory to better evaluate the quality of life [613]. In this way,
it is essential first to improve the pre- intra- and post-operative functional
assessments, namely neurological, neuropsychological and language examinations
by specialists, second to develop objective and subjective scales of evaluation by
the patient himself and his family.
Thus, multidisciplinar multicenter studies are necessary in order to better
understand the dynamic interactions between cerebral function (i.e., the host),
tumor evolution and treatments, with the goal to optimize the therapeutic strategy
in brain tumors.
 REFERENCES

[1] Tzourio-Mazoyer N, Josse G, Crivello F, Mazoyer B. Interindividual

variability in the hemispheric organization for speech. NeuroImage 2004;
21: 422-35.
[2] Xiong J, Rao S, Jerabek P, et al. Intersubject variability in cortical
activations during a complex language task. Neuroimage 2000; 12: 326-39.
[3] Ungerleider LG, Doyon J, Karni A. Imaging brain plasticity during motor
skill learning. Neurobiol Learn Mem. 2002; 78: 553-64.
[4] Hlustik P, Solodkin A, Noll DC, Small SL. Cortical plasticity during three-
week motor skill learning. J Clin Neurophysiol. 2004; 21: 180-91.
[5] Butefisch CM. Plasticity in the human cerebral cortex: lessons from the
normal brain and from stroke. Neuroscientist. 2004; 10: 163-73.
[6] Rijntjes M, Weiller C. Recovery of motor and language abilities after
stroke: the contribution of functional imaging. Prog Neurobiol. 2002; 66:
109-22.
[7] Duffau H, Capelle L, Denvil D, et al. Functional recovery after surgical
resection of low-grade gliomas in eloquent brain: hypothesis of brain
compensation. J Neurol Neurosurg Psychiatry 2003; 74: 901-7.
[8] van der Sanden GAC, Schouten LJ, van Dijck JAAM, et al. Incidence of
primary central nervous system cancers in South and East Netherlands in
1989-1994. Neuroepidemiology 1998; 17 : 247-57.
[9] CBTRUS Statistical reports: primary brain tumors in the United States,
1995-1999. Hinsdale, IL: Central Brain Tumor Registry of the United
States, 2002.
[10] Kleihues P, Cavenee W (eds). Pathology and genetics of tumours of the
nervous system. International Agency for Research on Cancer Press, Lyon
2000.
38 Hugues Duffau

[11] Mandonnet E, Delattre JY, Tanguy ML, et al. Continuous growth of mean
tumor diameter in a subset of grade II gliomas. Ann Neurol 2003; 53 : 524-
8.
[12] Giese A, Bjerkvig R, Berens ME, Westphal M. Cost of migration: invasion
of malignant gliomas and implications for treatment. J Clin Oncol 2003; 21:
1624-36.
[13] Afra D, Osztie E, Sipos L, et al. Preoperative history and postoperative
survival of supratentorial low-grade astrocytomas. Br J Neurosurg 1999 ;
13 : 299-305.
[14] Arienti VM, Botturi A, Boiardi A, et al. Adult brain low-grade
astrocytomas: survival after surgery and radiotherapy. Neurol Sci 2001 ;
22 : 233-8.
[15] Ashby LS, Shapiro WR. Low-grade glioma: supratentorial astrocytoma,
oligodendroglioma, and oligoastrocytoma in adults. Curr Neurol Neurosci
Rep 2004 ; 4 : 211-7.
[16] Bahary JP, Villemure JG, Choi S, et al. Low-grade pure and mixed cerebral
astrocytomas treated in the CT scan era. J Neurooncol 1996 ; 27 : 173-7.
[17] Bauman G, Lote K, Larson D, et al. Pretreatment factors predict overall
survival for patients with low-grade gliomas: a recursive partitioning
abalysis. Int J Radiat Oncol Biol Phys 1999 ; 45 : 923-9.
[18] Eyre HJ, Crowley JJ, Townsend JJ, et al. A randomized trial of radiotherapy
versus radiotherapy plus CCNU for incompletely resected low-grade
gliomas : a Southwest Oncology Group study. J Neurosurg 1993 ; 78 : 909-
14.
[19] Firsching R, Tieben R, Schröder R, et al. Long-term prognosis of low-grade
astrocytoma. Zentralbl Neurochir 1994 ; 55 : 10-5.
[20] Janny P, Cure H, Mohr M, et al. Low grade supratentorial astrocytomas.
Management and prognostic factors. Cancer 1994 ; 73 : 1937-45.
[21] Kaye AH, Walker DG. Low-grade astrocytomas: controversies in
management. J Clin Neurosci 2000 ; 7 : 475-483.
[22] Lindegaard KF, Mork SJ, Eide GE, et al. Statistical analysis of
clinicopathological features, radiotherapy and survival in 170 cases of
oligodendroglioma. J Neurosurg 1987 ; 67 : 224-30.
[23] McCormack BM, Miller DC, Budzilovich GN, et al. Treatment and survival
of low-grade astrocytoma in adults – 1977-1988. Neurosurgery 1992 ; 31 :
636-42.
[24] Nakamura M, Konishi N, Tsunoda S, et al. Analysis of proignostic and
survival factors related to treatment of low-grade astrocytomas in adults.
Oncology 2000 ; 58 : 108-16.
 References 39

[25] Nicolato A, Gerosa MA, Fina P, et al. Prognostic factors in low-grade

supratentorial astrocytomas : an uni-multivariate statistical analysis in 76
surgically treated adult patients. Surg Neurol 1995 ; 44 : 208-23.
[26] North CA, North RB, Epstein JA, et al. Low-grade cerebral astrocytomas.
Survival and quality of life after radiation therapy. Cancer 1990 ; 66 : 6-14.
[27] Piepmeier J, Christofer S, Spencer D, et al. Variations in the natural history
and survival of patients with supratentorial low-grade astrocytomas.
Neurosurgery 1996 ; 38 : 872-9.
[28] Shaw EG, Daumas-Duport C, Scheithauer BW, et al. Radiation therapy in
the management of low-grade supratentorial astrocytomas. J Neurosurg
1989 ; 70 : 853-61.
[29] Shibamato Y, Kitakabu Y, Takahashi M, et al. Supratentorial low-grade
astrocytoma. Correlation of computed tomography findings with effect of
radiation therapy and prognostic variables. Cancer 1993 ; 72 : 190-5.
[30] Soffietti R, Chio A, Giordana MT, et al. Prognostic factors in well-
differentiated cerebral astrocytomas in the adult. Neurosurgery 1989 ; 24 :
686-92.
[31] Touboul E, Schlienger M, Buffat L, et al. Radiation therapy with or whitout
surgery in the management of low-grade brain astrocytomas. A
retrospective study of 120 patients. Bull Cancer Radiother 1995 ; 82 : 388-
95.
[32] Van Veelen MLC, Avezaat CJJ, Kros JM, et al. Supratentorial low grade
astrocytoma: prognostic factors, dedifferentiation, and the issue of early
versus late surgery. J Neurol Neurosurg Psychiatry 1998 ; 64 : 581-7.
[33] Vertosick FT, Selker RG, Arena VC. Survival of patients with well-
differentiated astrocytomas diagnosed in the era of computed tomography.
Neurosurgery 1991 ; 28 : 496-501.
[34] Walker DG, Kaye AH. Low grade glial neoplasms. J Clin Neurosci 2003 ;
10 : 1-13.
[35] Wessels PH, Weber WEJ, Raven G, et al. Supratentorial grade II
astrocytoma: biological features and clinical course. Lancet Neurology 2003
; 2 : 395-403.
[36] Whitton AC, Bloom HJ. Low-grade glioma of the cerebral hemispheres in
adults: a retrospective analysis of 88 cases. Int J Radiat Oncol Biol Phys
1990 ; 18 : 783-86.
[37] Celli P, Nofrone I, Palma L, et al. Cerebral oligodendroglioma : prognostic
factors and life history. Neurosurgery 1994 ; 35 : 1018-34.
40 Hugues Duffau

[38] Kreth FW, Faist M, Rossner R, et al. Supratentorial World Health

Organization grade 2 astrocytomas and oligoastrocytomas. A new pattern of
prognostic factors. Cancer 1997; 79 : 370-9.
[39] Leighton C, Fischer B, Bauman G, et al. Supratentorial low grade glioma in
adults : an analysis of prognostic factors and timing of radiation. J Clin
Oncol 1997 ; 15 : 1294-1301.
[40] Lote K, Egeland T, Hager B, et al. Survival, prognostic factors, and
therapeutic efficacy in low-grade glioma : a retrospective study in 379
patients. J Clin Oncol 1997 ; 15 : 3129-40.
[41] Pignatti F, van den Bent M, Curran D, et al. Prognostic factors for survival
in adult patients with cerebral low-grade glioma. J Clin Oncol 2002 ; 20 :
2076-84.
[42] Stupp R, Janzer RC, Hegi ME, et al. Prognostic factors for low-grade
gliomas. Semin Oncol 2003 ; 30 (6 Suppl 19) : 23-8.
[43] Smith JS, Perry A, et al. Alterations of chromosome arms 1p and 19q as
predictors of survival in oligodendrogliomas, astrocytomas, and mixed
oligoastrocytomas. J Clin Oncol 2000 ; 18 : 636-45.
[44] Van den Bent MJ, Looijenga LH, Langenberg K, et al. Chromosomal
anomalies in oligodendroglial tumors are correlated with clinical features.
Cancer 2003 ; 97 : 1276-84.
[45] Mischel PS, Cloughesy TF, Nelson SF. DNA-microarray analysis of brain
cancer: molecular classification for therapy. Nat Rev Neurosci 2004; 5: 782-
92.
[46] Freije WA, Castro-Vargas FE, Fang Z, Horvath S, Cloughesy T, Liau LM,
Mischel PS, Nelson SF. Gene expression profiling of gliomas strongly
predicts survival. Cancer Res 2004; 64: 6503-10.
[47] Iwadate Y, Sakaida T, Hiwasa T, Nagai Y, Ishikura H, Takiguchi M,
Yamaura A. Molecular classification and survival prediction in human
gliomas based on proteome analysis. Cancer Res 2004; 64: 2496-501.
[48] Shai R, Shi T, Kremen TJ, Horvath S, Liau LM, Cloughesy TF, Mischel PS,
Nelson SF. Gene expression profiling identifies molecular subtypes of
gliomas. Oncogene 2003; 22: 4918-23.
[49] Jbabdi S, Mandonnet E, Duffau H, Capelle L, Swanson KR, Pélégrini-Issac
M, Guillevin R, Benali H. Diffusion tensor imaging allows anisotropic
growth simulations of low grade gliomas. Mag Reson Med 2005; 54: 616-
24.
[50] Swanson KR, Bridge C, Murray JD, Alvord EC Jr. Virtual and real brain
tumors: using mathematical modeling to quantify glioma growth and
invasion. J Neurol Sci 2003; 216: 1-10.
 References 41

[51] Oriuchi N, Tamura N, Shibazaki T, et al. Clinical evaluation of thallium-

201 SPECT in supratentorial gliomas: relationship to histologic grade,
prognosis and proliferative activities. J Nucl Med 1993; 34: 2085-9.
[52] Ishibashi M, Taguchi A, Sugita Y, et al. Thallium-201 in brain tumors:
relationship between tumor cell activity in astrocytic tumor and proliferating
cell nuclear antigen. J Nucl Med 1995; 36 :2201-6.
[53] Bagni B, Pinna L, Tamarozzi R, et al. SPET imaging of intracranial tumours
with 99Tcm-sestamibi. Nucl Med Commun 1995; 16: 258-64.
[54] Nishiyama Y, Yamamoto Y, Fukunaga K, Satoh K, Kunishio K, Ohkawa
M. Comparison of 99Tcm-MIBI with 201Tl chloride SPET in patients with
malignant brain tumours. Nucl Med Commun 2001; 22: 631-9.
[55] Staudenherz A, Fazeny B, Marosi C, et al. Does 99mTc-Sestamibi in high-
grade malignant brain tumors reflect blood-brain barrier damage only?
NeuroImage 2000; 12: 109-11.
[56] Hemm S, Vayssiere N, Zanca M, Ravel P, Coubes P. Thallium SPECT-
based stereotactic targeting for brain biopsies. A technical note. Stereotact
Funct Neurosurg 2004; 82: 70-6.
[57] Dierckx RA, Martin JJ, Dobbeleir A, Crols R, Neetens I, De Deyn PP.
Sensitivity and specificity of thallium-201 single-photon emission
tomography in the functional detection and differential diagnosis of brain
tumours. Eur J Nucl Med 1994; 21: 621-33.
[58] Sun D, Liu Q, Liu W, Hu W. Clinical application of 201Tl SPECT imaging
of brain tumors. J Nucl Med 2000; 41: 5-10.
[59] Staffen W, Hondl N, Trinka E, Iglseder B, Unterrainer J, Ladurner G.
Clinical relevance of 201Tl-chloride SPET in the differential diagnosis of
brain tumours. Nucl Med Commun 1998; 19: 335-40.
[60] Soler C, Beauchesne P, Maatougui K, et al. Technetium-99m sestamibi
brain single-photon emission tomography for detection of recurrent gliomas
after radiation therapy. Eur J Nucl Med 1998; 25: 1649-57.
[61] Yokogami K, Kawano H, Moriyama T, et al. Application of SPET using
technetium-99m sestamibi in brain tumours and comparison with expression
of the MDR-1 gene: is it possible to predict the response to chemotherapy in
patients with gliomas by means of 99mTc-sestamibi SPET? Eur J Nucl Med
1998; 25: 401-9.
[62] Beauchesne P, Pedeux R, Boniol M, Soler C. 99mTc-Sestamibi brain SPECT
after chemoradiotherapy is prognostic of survival in patients with high-
grade glioma. J Nucl Med 2004; 45: 409-13.
42 Hugues Duffau

[63] Soricelli A, Cuocolo A, Varrone A, et al. Technetium-99m-tetrofosmin

uptake in brain tumors by SPECT: comparison with thallium-201 imaging. J
Nucl Med 1998; 39: 802-6.
[64] Weber WA, Dick S, Reidl G, et al. Correlation between postoperative 3-
[(123)I]iodo-L-alpha-methyltyrosine uptake and survival in patients with
gliomas. J Nucl Med 2001; 42: 1144-50.
[65] Kuwert T, Woesler B, Morgenroth C, et al. Diagnosis of recurrent glioma
with SPECT and iodine-123-alpha-methyl tyrosine. J Nucl Med 1998; 39:
23-7.
[66] Bénard F, Romsa J, Hustinx R. Imaging gliomas with positron emission
tomography and single-photon emission computed tomography. Semin Nucl
Med 2003; 33: 148-62.
[67] Schaller B. Usefulness of positron emission tomography in diagnosis and
treatment follow-up of brain tumors. Neurobiol Dis 2004; 15: 437-48.
[68] Herschman HR. Molecular imaging: looking at problems, seeing solutions.
Science 2003; 302: 605-8.
[69] Blasberg RG, Roelcke U, Weinreich R, et al. Imaging brain tumor
proliferative activity with [124I]iododeoxyuridine. Cancer Res 2000; 60:
624-35.
[70] Shields AF, Grierson JR, Dohmen BM, et al. Imaging proliferation in vivo
with [F-18]FLT and positron emission tomography. Nat Med 1998; 4: 1334-
6.
[71] Jacobs A, Tjuvajev JG, Dubrovin M, et al. Positron emission tomography-
based imaging of transgene expression mediated by replication-conditional,
oncolytic herpes simplex virus type 1 mutant vectors in vivo. Cancer Res
2001; 61: 2983-95.
[72] Shinoura N, Nishijima M, Hara T, et al. Brain tumors: detection with C-11
choline PET. Radiology 1997; 202: 497-503.
[73] Hara T, Kondo T, Hara T, Kosaka N. Use of 18F-choline and 11C-choline
as contrast agents in positron emission tomography imaging-guided
stereotactic biopsy sampling of gliomas. J Neurosurg 2003; 99: 474-9.
[74] Kim CK, Alavi JB, Alavi A, Reivich M. New grading system of cerebral
gliomas using positron emission tomography with F-18 fluorodeoxyglucose.
J Neurooncol 1991; 10: 85-91.
[75] Meyer PT, Schreckenberger M, Spetzger U, et al. Comparison of visual and
ROI-based brain tumour grading using 18F-FDG PET: ROC analyses. Eur J
Nucl Med 2001; 28: 165-74.
 References 43

[76] Kaschten B, Stevenaert A, Sadzot B, et al. Preoperative evaluation of 54

gliomas by PET with fluorine-18-fluoro-deoxyglucose and/or carbon-11-
methionine. J Nucl Med 1998; 39: 778-785.
[77] Alavi JB, Alavi A, Chawluk J, et al. Positron emission tomography in
patients with glioma. A predictor of prognosis. Cancer 1988; 62: 1074-8.
[78] Holzer T, Herholz K, Jeske J, Heiss WD. FDG-PET as a prognostic
indicator in radiochemotherapy of glioblastoma. J Comput Assist Tomogr
1993; 17: 681-7.
[79] De Witte O, Lefranc F, Levivier M, Salmon I, Brotchi J, Goldman S. FDG-
PET as a prognostic factor in high grade astrocytoma. J Neurooncol 2000;
49: 157-63.
[80] De Witte O, Oulad Ben Taib N, Branle F, Rorive S, Brotchi J, Goldman S.
Contribution of PET to the management of patients with low-grade glioma.
Neurochirurgie 2004; 50: 468-73.
[81] Levivier M, Goldman S, Pirotte B, et al. Diagnostic yield of stereotactic
brain biopsy guided by positron emission tomography with [18F]fluoro-
deoxyglucose. J Neurosurg 1995; 82: 445-52.
[82] Massager N, David P, Goldman S, et al. Combined magnetic resonance
imaging- and positron emission tomography-guided stereotactic biopsy in
brainstem mass lesions: diagnostic yield in a series of 30 patients. J
Neurosurg 2000; 93: 951-7
[83] Francavilla T, Miletich R, Di Chiro G, Patronas NJ, Rizzoli HV, Wright
DC. Positron emission tomography in the detection of malignant
degeneration of low-grade gliomas. Neurosurgery 1989; 24: 1-5.
[84] De Witte O, Levivier M, Violon P, et al. Prognostic value positron emission
tomography with [18F]fluoro-2-deoxy-D-glucose in the low-grade glioma.
Neurosurgery 1996; 39: 470-6.
[85] Glantz MJ, Hoffman JM, Coleman RE, et al. Identification of early
recurrence of primary central nervous system tumors by
[18F]fluorodeoxyglucose positron emission tomography. Ann Neurol 1991;
29: 347-55.
[86] Buchpiguel CA, Alavi JB, Alavi A, Kenyon LC. PET versus SPECT in
distinguishing radiation necrosis from tumor recurrence in the brain. J Nucl
Med 1995; 36: 159-64.
[87] Brock CS, Young H, O’Reilly SM, et al. Early evaluation of tumour
metabolic response using [18F]fluorodeoxyglucose and positron emission
tomography: a pilot study following the phase II chemotherapy schedule for
temozolomide in recurrent high-grade gliomas. Br J Cancer 2000; 82: 608-
15.
44 Hugues Duffau

[88] Chung JK, Kim YK, Kim SK, et al. Usefulness of 11C-methionine PET in
the evaluation of brain lesions that are hypo- or isometabolic on 18F-FDG
PET. Eur J Nucl Med Mol Imaging 2002; 29: 176-82.
[89] Derlon JM, Chapon F, Noel MH, et al. Non-invasive grading of
oligodendrogliomas: correlation between in vivo metabolic pattern and
histology. Eur J Nucl Med 2000; 27: 778-87.
[90] De Witte O, Goldberg I, Wikler D, et al. Positron emission tomography
with injection of methionine as a prognostic factor in glioma. J Neurosurg
2001; 95: 746-50.
[91] Derlon JM, Petit-Taboue MC, Chapon F, et al. The in vivo metabolic
pattern of low-grade brain gliomas: a positron emission tomographic study
using 18F-fluorodeoxyglucose and 11C-L-methylmethionine. Neurosurgery
1997; 40: 276-87.
[92] Herholz K, Hölzer T, Bauer B, et al. 11C-methionine PET for differential
diagnosis of low-grade gliomas. Neurology 1998; 50 :1316-22.
[93] Ribom D, Eriksson A, Hartman M, et al. Positron emission tomography
(11)C-methionine and survival in patients with low-grade gliomas. Cancer
2001; 92: 1541-9.
[94] Pirotte B, Goldman S, Massager N, et al. Combined use of 18F-
flurodeoxyglucose and 11C-methionine in 45 positron emission
tomographye-guided stereotactic brain biopsies. J Neurosurg 2004; 101:
476-83.
[95] Voges J, Herholz K, Holzer T, et al. 11C-methionine and 18F-2-
fluorodeoxyglucose positron emission tomography: a tool for diagnosis of
cerebral glioma and monitoring after brachytherapy with 125I seeds.
Stereotact Funct Neurosurg 1997; 69: 129-35.
[96] Derlon JM, Bourdet C, Bustany P, et al. [11C]L-methionine uptake in
gliomas. Neurosurgery 1989; 25: 720-8.
[97] Inoue T, Shibasaki T, Oriuchi N, et al. 18F alpha-methyl tyrosine PET
studies in patients with brain tumors. J Nucl Med 1999; 40: 399-405.
[98] Menedez J, Nanda A, Polin RS. PET scan for brain tumors. Sem Neurosurg
2000; 11: 277-86.
[99] de Edelenyi FS, Rubin C, Esteve F, et al. A new approach for analyzing
proton magnetic resonance spectroscopic images of brain tumors: nosologic
images. Nat Med 2000; 6: 1287-9.
[100] Herminghaus S, Pilatus U, Moller-Hartman W, et al. Increased choline
levels coincide with enhanced proliferative activity of human
neuroepithelial brain tumors. NMR Biomed 2002; 15:385-92.
 References 45

[101] Negendank WG, Sauter R, Brown TR, et al. Proton magnetic resonance
spectroscopy in patients with glial tumours: a multicenter study. J
Neurosurg 1996; 84: 449-58.
[102] Howe FA, Barton SJ, Cudlip SA, et al. Metabolic profiles of human brain
tumors using quantitative in vivo 1H magnetic resonance spectroscopy.
Magn Reson med 2003; 49: 223-32.
[103] Michaelis T, Merboldt KD, Bruhn H, Hanicke W, Frahm J. Absolute
concentrations of metabolites in the adult human brain in vivo:
quantification of localized proton MR spectra. Radiology 1993; 187: 219-
27.
[104] Urenjak J, Williams SR, Gadian DG, Noble M. Proton nuclear magnetic
resonance spectroscopy unambiguously identifies different neural cell types.
J Neurosci 1993; 13: 981-9.
[105] Kemp GJ. Non-invasive methods for studying brain energy metabolism:
what they show and what it means. Dev Neurosci 2000; 22: 418-28.
[106] Croteau D, Scarpace L, Hearshen D, et al. Correlation between magnetic
resonance spectroscopy imaging and image-guided biopsies:
semiquantitative and qualitative histopathological analyses of patients with
untreated glioma. Neurosurgery 2001;49:823-9.
[107] Dowling C, Bollen AW, Noworolski SM, et al. Preoperative proton MR
spectroscopy imaging of brain tumors: correlation with histopathologic
analysis of resection specimens. Am J Neuroradiol 2001; 22: 604-12.
[108] McKnight TR, Noworolski SM, Vigneron DB, Nelson SJ. An automated
technique for the quantitative assessment of 3D-MRSI data from patients
with glioma. J Magn Reson Imag 2001; 13: 167-77.
[109] Tate AR, Griffiths JR, Martinez-Perez I, et al. Towards a method for
automated classification of 1H MRS spectra from brain tumours. NMR
Biomed 1998; 11: 177-91.
[110] Butzen J, Prost R, Chetty V, et al. Discrimination between neoplastic and
nonneoplastic brain lesions by use of proton MR spectroscopy: the limits of
accuracy with a logistic regression model. Am J Neuroradiol 2000; 21:
1213-9.
[111] Howe FA, Opstad KS. 1H MR spectroscopy of brain tumours and masses.
NMR Biomed 2003; 16: 123-31.
[112] Pirzkall A, Nelson SJ, McKnight TR, et al. Metabolic imaging of low-grade
gliomas with three-dimensional magnetic resonance spectroscopy. Int J
Radiat Oncol Biol Phy. 2002; 53: 1254-64.
46 Hugues Duffau

[113] Galanaud D, Chinot O, Nicoli F, et al. Use of proton magnetic resonance

spectroscopy of the brain to differentiate gliomatosis cerebri from low-grade
glioma. J Neurosurg 2003; 98: 269-76.
[114] Law M, Cha S, Knopp EA, Johnson G, Arnett J, Litt AW. High-grade
gliomas and solitary metastasis: differentiation by using perfusion and
proton spectroscopic MR imaging. Radiology 2002; 222: 715-21.
[115] Barba I, Moreno A, Martine-Perez I, et al. Magnetic resonance spectroscopy
of brain hemangiopericytomas: high myo-inositol concentrations and
discrimination from meningiomas. J Neurosurg 2001; 94: 55-60.
[116] Murphy M, Loosemore A, Clifton AG, et al. The contribution of 1H MRS to
clinical brain tumour diagnosis. J Neurosurg 2002; 16: 329-34.
[117] Herminghaus S, Dierks T, Pilatus U, et al. Determination of
histopathological tumor grade in neuroepithelial brain tumors by using
spectral pattern analysis of in vivo spectroscopic data. J Neurosurg 2003;
98: 74-81.
[118] Kuztnetsov Y, Caramanos Z, Antel S, et al. Proton magnetic resonance
spectroscopic imaging can predict length of survival in patients with
supratentorial gliomas. Neurosurgery 2003; 53: 565-76.
[119] Sabatier J, Gilard V, Malet-Martino M, et al. Characterisation of choline
compounds with in vitro 1H magnetic resonance spectroscopy for
discrimination of primary brain tumours. Invest Radiol 1999; 34: 230-5.
[120] Shimizu H, Kumabe T, Shirane R, Yoshimoto T. Correlation between
choline level measured by proton MR spectroscopy and Ki-67 labeling
index in gliomas. Am J Neuroradiol 2000; 21: 659-65.
[121] Castillo M, Smith JK, Kwock L. Correlation of myo-inositol levels and
grading of cerebral astrocytomas. Am J Neuroradiol 2000; 21: 1645-9.
[122] Cheng LL, Chang I-Wen, Louis DN, Gonzalez RG. Correlation of high-
resolution magic angle spinning proton magnetic resonance spectroscopy
with histopathology of intact human brain tumor specimens. Cancer Res
1998; 58: 1825-32.
[123] Kuesel AC, Sutherland GR, Halliday W, Smith ICP. 1H MRS of high grade
astrocytomas: mobile lipid accumulation in necrotic tissue. NMR Biomed
1994; 7: 149-55.
[124] Auer DP, Gossl C, Schirmer T, Czisch M. Improved analysis of 1H-MR
spectra in the presence of mobil lipids. Magn Reson Med 2001; 46; 615-18.
[125] Graves EE, Nelson SJ, Vigneron DB, et al. Serial proton MR spectroscopic
imaging of recurrent malignant gliomas after gamma knife radiosurgery. Am
J Neuroradiol 2001; 22: 613-24.
 References 47

[126] Rock JP, Hearshen D, Scarpace L, et al. Correlation between magnetic

resonance spectroscopy and image-guided histopathology, with special
attention to radiation necrosis. Neurosurgery 2002; 51: 912-20.
[127] Rabinov JD, lee PL, Barker FG, et al. In vivo 3-T MR spectroscopy in the
distinction of recurrent glioma versus radiation effects: initial experience.
Radiology 2002; 225: 871-9.
[128] Tedeschi G, Lundbom N, Raman R, et al. Increased choline signal
coinciding with malignant degeneration of cerebral gliomas: a serial proton
magnetic resonance spectroscopy imaging study. J Neurosurg 1997; 87:
516-24.
[129] Hall WA, Martin A, Liu H, Truwit CL. Improving diagnostic yield in brain
biopsy: coupling spectroscopic targeting with real-time needle placement. J
Magn Reson Imaging 2001; 13: 12-5.
[130] Martin AJ, Liu H, Hall WA, Truwit CL. Preliminary assessment of turbo
spectroscopic imaging for targeting in brain biopsy. Am J Neuroradiol
2001; 22: 959-68.
[131] McKnight TR, von dem Bussche MH, Vigneron DB, et al.
Histopathological validation of a three-dimensional magnetic resonance
spectroscopy index as a predictor of tumor presence. J Neurosurg 2002; 97:
794-802.
[132] Liu H, Hall WA, Martin AJ, Maxwell RE, Truwit CL. MR-guided and MR-
monitored neurosurgical procedure at 1.5 T. J Comput Assist Tomogr 2000;
24: 909-18.
[133] Stadlbauer A, Moser E, Gruber S, Nimsky C, Fahlbusch R, Ganslandt O.
Integration of biochemical images of a tumor into frameless stereotaxy
achieved using a magnetic resonance imaging/magnetic resonance
spectroscopy hybrid data set. J Neurosurg 2004; 101:287-94.
[134] Stadlbauer A, Moser E, Gruber S, et al. Improved delineation of brain
tumors: an automated method for segmentation based on pathologic changes
of (1)H-MRSI metabolites in gliomas. Neuroimage 2004; 23: 454-61.
[135] Nelson SJ, Graves E, Pirzkall A, et al. In vivo molecular imaging for
planning radiation therapy of gliomas: an application of 1H MRSI. J Magn
Reson Imaging 2002; 16: 464-76.
[136] Pirzkall A, McKnight TR, Graves EE, et al. MR-spectroscopy guided target
delineation for high-grade gliomas. Int J Radiat Oncol Biol Phys 2001; 50:
915-28.
[137] Utriainen M, Komu M, Vuorinen V, et al. Evaluation of brain tumor
metabolism with [11C]choline PET and 1H-MRS. J Neurooncol 2003; 62:
329-38.
48 Hugues Duffau

[138] Pomper MG, Port JD. New techniques in MR imaging of brain tumors.
Magn Reson Imaging Clin N Am 2000; 8: 691-713.
[139] Rees J. Advances in magnetic resonance imaging of brain tumours. Curr
Opin Neurol 2003; 16: 643-50.
[140] Keston P, Murray AD, Jackson A. Cerebral perfusion imaging using
contrast-enhanced MRI. Clin Radiol 2003; 58: 505-13.
[141] Le Bihan D. Looking into the functional architecture of the brain with
diffusion MRI. Nat Rev Neurosci 2003; 4: 469-80.
[142] Kono K, Inoue Y, Nakayama K, et al. The role of diffusion-weighted
imaging in patients with brain tumors. AJNR Am J Neuroradiol 2001; 22:
1081-8.
[143] Sugahara T, Korogi Y, Kochi M, et al. Usefulness of diffusion-weighted
MRI with echo-planar technique in the evaluation of cellularity in gliomas.
J Magn Reson Imaging 1999; 9: 53-60.
[144] Yang D, Korogi Y, Suguhara T, et al. Cerebral gliomas: prospective
comparison of multivoxel 2D chemical-shift imaging proton MR
spectroscopy, echoplanar perfusion and diffusion-weighted MRI.
Neuroradiology 2002; 44: 656-66.
[145] Kim YJ, Chang KH, Song IC, et al. Brain abscess and necrotic or cystic
brain tumor: discrimination with signal intensity on diffusion-weighted MR
imaging. Am J Roentgenol 1998; 171: 1487-90.
[146] Chang SC, Lai PH, Chen WL, et al. Diffusion-weighted MRI features of
brain abscess and cystic or necrotic brain tumors: comparison with
conventional MRI. Clin Imaging 2002; 26: 227-36.
[147] Sugahara T, Korogi Y, Kochi M, et al. Correlation of MR imaging-
determined cerebral blood volume maps with histological and angiographic
determination of vascularity of gliomas. Am J Roentgenol 1998; 171: 1479-
86.
[148] Lefournier V, Peoc’h M, Usson Y, et al. Magnetic resonance cerebral blood
volume maps. Comparison with histologic findings in different types of
brain lesions. J Neuroradiol 2003; 30: 3-9.
[149] Roberts HC, Roberts TP, Brasch RC, Dillon WP. Quantitative measurement
of microvascular permeability in human brain tumors achieved using
dynamic contrast-enhanced MR imaging: correlation with histologic grade.
Am J Neuroradiol 2000; 21: 891-99.
[150] Knopp EA, Cha S, Johnson G, et al. Glial neoplasms: dynamic contrast-
enhanced T2*-weighted MR imaging. Radiology 1999; 211: 791-8.
 References 49

[151] Ludemann L, Grieger W, Wurm R, Budzisch M, Hamm B, Zimmer C.

Comparison of dynamic contrast-enhanced MRI with WHO tumor grading
for gliomas. Eur Radiol 2001; 11: 1231-41.
[152] Provenzale JM, Wang GR, Breener T, Petrella JR, Sorensen AG.
Comparison of permeability in high-grade and low-grade brain tumors using
dynamic susceptibility contrast MR imaging. Am J Roentgenol 2002; 178:
711-6.
[153] Kremer S, Grand S, Remy C, et al. Cerebral blood volume mapping by MR
imaging in the initial evaluation of brain tumors. J Neuroradiol 2002; 29:
105-13.
[154] Kremer S, Grand S, Berger F, et al. Dynamic contrast-enhanced MRI:
differentiating melanoma and renal carcinoma metastases from high-grade
astrocytomas and other metastases. Neuroradiology 2003; 45: 44-9.
[155] Hartmann M, Heiland S, Harting I, et al. Distinguishing of primary cerebral
lymphoma from high-grade glioma with perfusion-weighted magnetic
resonance imaging. Neurosci Lett 2003; 338: 119-22.
[156] Cha S. Perfusion MR imaging: basic principles and clinical applications.
Magn Reson Imaging Clin N Am. 2003; 11: 403-13.
[157] Chan JH, Tsui EY, Chau LF, et al. Discrimination of an infected brain
tumor from a cerebral abscess by combined MR perfusion and diffusion
imaging. Comput Med Imaging Graph 2002; 26: 19-23.
[158] Fuss M, Wenz F, Essig M, et al. Tumor angiogenesis of low-grade
astrocytomas measured by dynamic susceptibility contrast-enhanced MRI
(DSC-MRI) is predictive of local tumor control after radiation therapy. Int J
Radiat Oncol Biol Phys 2001; 51: 478-82.
[159] Gossmann A, Helbich TH, Kuriyama N, et al. Dynamic contrast-enhanced
magnetic resonance imaging as a surrogate marker of tumor response to
anti-angiogenic therapy in a xenograft model of glioblastoma multiforme. J
Magn Reson Imaging 2002; 15: 233-40.
[160] Lam WW, Chan KW, Wong WL, Poon WS, Metreweli C. Pre-operative
grading of intracranial glioma. Acta Radiol. 2001; 42: 548-54.
[161] Soltmann O. Experimentalle studien über die functionen des grosshirns der
neugeborenen. Jahrb Kinderheilkd 1876 ;9 :106-48.
[162] Barlow T. On a case of double hemiplegia with cerebral symmetrical
lesions. Br Med J 1877;2 :103-4.
[163] von Monakow C: Die lokalisation im groshirn un der abbau der funktion
durch kortikale herde. Wiesbaden, Germany:Bergman JF 26-34, 1914
[164] Kennard MA. Age and other factors in motor recovery from precentral
lesions in monkeys. Am J Physiol 1936 ;115 :138-46
50 Hugues Duffau

[165] Bethe A, Fischer E: Die Anpassungsfähigkeit (Plastizität) des

Nervensystems. In: Handbuch der normalen und pathologischen
Physiologie (Bethe A, von Bergmann G, Emden G, Ellinger A, Hrsg),
Berlin: Springer, Bd 15/2, pp 1045-1130, 1931
[166] Duffau H. Short-term cortical sensorimotor plasticity in humans: a study
using intraoperative electrical stimulation. Ph.D. Thesis in Neurosciences,
Paris, 2000.
[167] Byrne JH. Synapses. Plastic plasticity. Nature 1997;389:791-2.
[168] Jacobs KM, Donoghue JP. Reshaping the cortical motor map by unmasking
latent intracortical connections. Science 1991;251:944-7
[169] Ivanco TL, Greenough WT. Physiological consequences of morphologically
detectable synaptic plasticity: potential uses for examining recovery
following damage. Neuropharmacology 2000 ; 39 : 765-76.
[170] Gross CG. Neurogenesis in the adult brain: death of a dogma. Nat Rev
Neurosci 2000 ; 1 : 67-73.
[171] Nguyen DK, Botez MI. Diaschisis and neurobehavior. Can J Neurol Sci
1998;25:5-12.
[172] Duffau H, Sichez JP, Lehéricy S. Intraoperative unmasking of brain
redundant motor sites during resection of a precentral angioma. Evidence
using direct cortical stimulations. Ann Neurol 2000 ; 47 : 132-5.
[173] Bavelier D, Neville HJ. Cross-modal plasticity: where and how? Nat Rev
Neurosci 2002 ; 3:443-52.
[174] Draganski B, Gasert C, Busch V, et al. Changes in grey matter induced by
training. Nature 2004 ; 427 : 311-2.
[175] Jonhson MH. Development of human brain functions. Biol Psychiatry 2003;
54: 1312-6.
[176] Karni A, Meyer G, Rey-Hipolito C, Jezzard P, Adams MM, Turner R,
Ungerleider LG. The acquisition of skilled motor performance: fast and
slow experience-driven changes in primary motor cortex. Proc Natl Acad
Sci U S A 1998; 95: 861-8.
[177] Chen R, Cohen LG, Hallet M. Nervous system reorganization following
injury. Neuroscience 2002; 111: 761-73.
[178] Kolb B. Overview of cortical plasticity and recovery from brain injury. Phys
Med Rehabil Clin N Am. 2003;14:S7-25
[179] Hallett M. Plasticity of the human motor cortex and recovery from stroke.
Brain Res Brain Res Rev 2001; 36: 169-74.
[180] Nudo RJ. Functional and structural plasticity in motor cortex: implications
for stroke recovery. Phys Med Rehabil Clin N Am 2003;14:S57-76.
 References 51

[181] Rossini PM, Calautti C, Pauri F, Baron JC. Post-stroke plastic

reorganisation in the adult brain. Lancet Neurol 2003;2:493-502.
[182] Thirumala P, Hier DB, Patel P. Motor recovery after stroke: lessons from
functional brain imaging. Neurol Res 2002; 24: 453-8.
[183] Moritz C, Haughton V. Functional MR imaging: paradigms for clinical
preoperative mapping. Magn Reson Imaging Clin N Am 2003; 11: 529-42
[184] Orrison WW Jr. Magnetic source imaging in stereotactic and functional
neurosurgery. Stereotact Funct Neurosurg 1999; 72: 89-94.
[185] Vlieger EJ, Majoie CB, Leenstra S, den Heeten GJ. Functional magnetic
resonance imaging for neurosurgical planning in neurooncology. Eur Radiol
2004; 14: 1143-53.
[186] Wunderlich G, Knorr U, Herzog H, Kiwit JC, Freund HJ, Seitz RJ.
Precentral glioma location determines the displacement of cortical hand
representation. Neurosurgery 1998; 42: 18-27.
[187] Bittar RG, Olivier A, Sadikot AF, Andermann F, Pike GB, Reutens DC.
Presurgical motor and somatosensory cortex mapping with functional
magnetic resonance imaging and positron emission tomography. J
Neurosurg 1999; 91: 915-21.
[188] Bittar RG, Olivier A, Sadikot AF, Andermann F, Reutens DC. Cortical
motor and somatosensory representation: effect of cerebral lesions. J
Neurosurg 2000; 92: 242-8.
[189] Meyer PT, Sturz L, Sabri O, et al. Preoperative motor system brain mapping
using positron emission tomography and statistical parametric mapping:
hints on cortical reorganisation. J Neurol Neurosurg Psychiatry 2003; 74 :
471-8.
[190] Nyberg G, Andersson J, Antoni G, et al. Activation PET scanning in
pretreatment evaluation of patient with cerebral tumours or vascular lesions
in or close to the sensorimotor cortex. Acta Neurochir (Wien) 1996; 138:
684-94.
[191] Schreckenberger M, Spetzger U, Sabri O, et al. Localisation of motor areas
in brain tumour patients: a comparison of preoperative [18F]FDG-PET and
intraoperative cortical electrostimulation. Eur J Nucl Med 2001; 28: 1394-
403.
[192] Bookheimer SY, Zeffiro TA, Blaxton T, et al. A direct comparison of PET
activation and electrocortical stimulation mapping for language localization.
Neurology 1997; 48: 1056-65.
[193] Herholz K, Reulen HJ, von Stockhausen HM, et al. Preoperative activation
and intraoperative stimulation of language-related areas in patients with
glioma. Neurosurgery 1997; 41: 1253-62.
52 Hugues Duffau

[194] Meyer PT, Sturz L, Schreckenberger M, et al. Preoperative mapping of

cortical language areas in adult brain tumor patients using PET and
individual non-normalised SPM analyses. Eur J Nucl Med Mol Imaging
2003; 30: 951-60.
[195] Nariai T, Senda M, Ishii K, et al. Three-dimensional imaging of cortical
structure, function and glioma for tumor resection. J Nucl med 1997; 38:
1563-8.
[196] Fried I, Nenov V, Ojemann SG, Woods RP. Functional MR and PET
imaging of rolandic and visual cortices for neurosurgical planning. J
Neurosurg 1995; 83: 854-61.
[197] Kaplan AM, Bandy DJ, Manwaring KH, et al. Functional brain mapping
using positron emission tomography scanning in preoperative neurosurgical
planning for pediatric brain tumors. J Neurosurg 1999; 91: 797-803.
[198] Vinas FC, Zamorano L, Mueller RA, et al. [15O]-water PET and
intraoperative brain mapping: a comparison in the localization of eloquent
cortex. Neurol Res 1997; 19: 601-8.
[199] Achten E, Jackson GD, Cameron JA, Abbott DF, Stella DL, Fabinyi GC.
Presurgical evaluation of the motor hand area with functional MR imaging
in patients with tumors and dysplastic lesions. Radiology 1999; 210: 529-
38.
[200] Atlas SW, Howard RS, Maldjian J, et al. Functional magnetic resonance
imaging of regional brain activity with intracerebral gliomas: findings and
implications for clinical management. Neurosurgery 1996; 38: 329-38.
[201] Conesa G, Pujol J, Deus J, et al. EPI functional MRI: a useful tool for
preoperative rolandic fissure localization. Front Radiat Ther Oncol 1999;
33: 23-7.
[202] Heilbrun MP, Lee JN, Alvord L. Practical application of fMRI for surgical
planning. Stereotact Funct Neurosurg 2001; 76: 168-74.
[203] Hirsch J, Ruge MI, Kim KHS, et al. An integrated functional magnetic
resonance imaging procedure for preoperative mapping of cortical areas
associated with tactile, motor, language and visual functions. Neurosurgery
2000; 47: 711-22.
[204] Inoue T, Shimizu H, Nakasato N, Kumabe T, Yoshimoto T. Accuracy and
limitation of functional magnetic resonance imaging for identification of the
central sulcus: comparison with magnetoencephalography in patients in
brain tumors. Neuroimage 1999; 10: 738-48.
[205] Krings T, Topper R, Willmes K, Reinges MH, Gilsbach JM, Thron A.
Activation in primary and secondary motor areas in patients with CNS
neoplasms and weakness. Neurology 2002; 58: 381-90.
 References 53

[206] Krings T, Reinges MH, Erberich S,et al. Functional MRI for presurgical
planning: problems, artefacts, and solution strategies. J Neurol Neurosurg
Psychiatry 2001; 70: 749-60.
[207] Lee CC, Ward HA, Sharbrough FW, et al. Assessment of functional MR
imaging in neurosurgical planning. Am J Neuroradiol 1999; 20: 1511-9.
[208] Mueller WM, Yetkin FZ, Hammeke TA, et al. Functional magnetic
resonance imaging mapping of the motor cortex in patients with cerebral
tumors. Neurosurgery 1996; 39: 515-20.
[209] Nelson L, Lapsiwala S, Haughton VM, et al. Preoperative mapping of the
supplementary motor area in patients harbouring tumors in the medial
frontal lobe. J Neurosurg 2002; 97: 1108-14.
[210] Nitschke MF, Melchert UH, Hahn C. Preoperative functional magnetic
resonance imaging (fMRI) of the motor system in patients with tumours in
the parietal lobe. Acta Neurochir (Wien) 1998; 140: 1223-9.
[211] Pujol J, Conesa G, Deus J, et al. Presurgical identification of the primary
sensorimotor cortex by functional magnetic resonance imaging. J
Neurosurg 1996; 84: 7-13.
[212] Roux FE, Boulanouar K, Ranjeva JP, et al. Usefulness of motor functional
MRI correlated to cortical mapping in Rolandic low-grade astrocytomas.
Acta Neurochir (Wien) 1999; 141: 71-9.
[213] Righini A, de Divitiis O, Prinster A, et al. Functional MRI: primary motor
cortex localization in patients with brain tumors. J Comput Assist Tomogr
1996; 20: 702-8.
[214] Rutten GJ, Ramsey NF, van Rijen PC, Noordmans HJ, van Veelen CW.
Development of a functional magnetic resonance imaging protocol for
intraoperative localization of critical temporoparietal language areas. Ann
Neurol 2002; 51: 350-60.
[215] Belliveau JW, Rosen BR, Kantor HL, et al. Functional cerebral imaging by
susceptibility-contrast NMR. Mag Reson Med 1990; 14: 538-46.
[216] Ogawa S, Menon RS, Tank DW, et al. Functional brain mapping by blood
oxygenation level-dependent contrast magnetic resonance imaging. A
comparison of signal characteristics with a biophysical model. Biophys J
1993; 64: 803-812.
[217] HeegerDJ, Ress D. What does fMRI tell us about neuronal activity? Nat Rev
Neurosci 2002; 3: 142-51.
[218] Toronov V, Walker S, Gupta R, et al. The roles of changes in deoxy-
hemoglobin concentration and regional cerebral blood volume in the fMRI
BOLD signal. Neuroimage 2003; 19: 1521-31.
54 Hugues Duffau

[219] Holodny AI, Schulder WC, Liu JA, Maldjian JA, Kalnin AJ. Decreased
BOLD functional MR activation of the motor and sensory cortices adjacent
to a glioblastoma multiforme: implications for image-guided neurosurgery.
Am J Neuroradiol 1999; 20: 609-12.
[220] Holodny AI, Schulder WC, Liu J, Wolko JA, Maldjian, Kalnin AJ. The
effect of brain tumors on BOLD functional MR Imaging activation in the
adjacent motor cortex: implications for image-guided neurosurgery. Am J
Neuroradiol 2000; 21: 1415-22.
[221] Ulmer JL, Krouwer HG, Mueller WM, Ugurel MS, Kocak M, Mark LP.
Pseudo-reorganization of language cortical function at fMR imaging: a
consequence of tumor-induced neurovascular uncoupling. Am J
Neuroradiol 2003; 24: 213-17.
[222] Ulmer JL, Hacein-Bey L, Mathews VP, et al. Lesion-induced pseudo-
dominance at functional magnetic resonance imaging: implications for
preoperative assessments. Neurosurgery 2004; 55: 569-79.
[223] Roux FE, Boulanouar K, Lotterie JA, mejdoubi M, LeSage JP, Berry I.
Language functional magnetic resonance imaging in preoperative
assessment of language areas: correlation with direct cortical stimulation.
Neurosurgery 2003; 52: 1335-45.
[224] Schreiber AU, Hubbe U, Ziyeh S, Hennig J. The influence of gliomas and
nonglial space-occupying lesions on blood-oxygen-level-dependent contrast
enhancement. Am J Neuroradiol 2000; 21: 1055-63.
[225] Aubert A, Costalat R, Duffau H, Benali H. Modeling of pathophysiological
coupling between brain electrical activation, energy metabolism and
hemodynamics: insights for the interpretation of intracerebral tumor
imaging. Acta Biotheoretica 2002; 50: 281-95.
[226] Boas DA, Dale AM, Franceschini MA. Diffuse optical imaging of brain
activation : approaches to optimizing image sensitivity, resolution and
accuracy. NeuroImage 2004; 23: 275-88.
[227] Franceschini MA, Boas DA. Noninvasive measurement of neuronal activity
with near-infrared optical imaging. NeuroImage 2004; 21: 336-72.
[228] Wolf M, Wolf U, Toronov V, et al. Different time evolution of
oxyhemoglobin and deoxyhemoglobin concentration changes in the visual
and motor cortices during functional stimulation: a near-infrared
spectroscopy study. NeuroImage 2002; 16: 704-12.
[229] Fujiwara N, Sakatani K, Katayama Y, et al. Evoked-cerebral blood
oxygenation changes in false-negative activations in BOLD contrast
functional MRI of patients with brain tumors. NeuroImage 2004; 21: 1464-
71.
 References 55

[230] Pouratian N, Sicotte N, Rex D, et al. Spatial/temporal correlation of BOLD

and optical intrinsic signals in humans. Magn Reson Med 2002; 47: 766-76.
[231] Kleinschmidt A, Obrig H, Requardt M, et al. Simultaneous recording of
cerebral blood oxygenation changes during human brain activation by
magnetic resonance imaging and near-infrared spectroscopy. J Cereb Blood
Flow Metab 1996; 16: 817-26.
[232] Cohen D. Magnetoencephalography: detection of the brain’s electrical
activity with a superconducting magnetometer. Science 1072; 175: 664-6.
[233] Barth DS, Sutherling WW, Engel J, Beatty J. Neuromagnetic localization of
epileptiform spike activity in the human brain. Scienc. 1982; 218: 891-4.
[234] Alberstone CD, Skirboll SL, Benzel EC, et al. Magnetic source imaging and
brain surgery: presurgical and intraoperative planning in 26 patients. J
Neurosurg 2000; 92: 79-90.
[235] Gallen CC, Schwartz BJ, Bucholz RD, et al. Presurgical localization of
functional cortex using magnetic source imaging. J Neurosurg 1995; 82:
988-94.
[236] Ganslandt O, Fahlbush R, Nimsky C, et al. Functional neuronavigation with
magnetoencephalography: outcome in 50 patients with lesions around the
motor cortex. J Neurosurg 1999; 91: 73-9.
[237] Kucharczyk J, Anson J, Benzel E, et al. Evaluation of magnetic source
imaging for presurgical mapping of brain neoplasms: a two-center
retrospective technology assessment study. Acad Radiol 1996;3 Suppl 1:
S131-4.
[238] Morioka T, Shigeto H, Ishibashi H, et al. Magnetic source imaging of the
sensory cortex on the surface anatomy MR scanning. Neurol Res 1998; 20:
235-41.
[239] Oishi M, Fukuda M, Kameyama S, Kawaguchi T, Masuda H, Tanaka R.
Magnetoencephalographic representation of the sensorimotor hand area in
cases of intracerebral tumour. J Neurol Neurosurg Psychiatry 2003; 74:
1649-54.
[240] Roberts TPL, Howley HA. Magnetic source imaging as a tool for
presurgical functional brain mapping. Neurosurg Clin N Am 1997; 8: 421-
38.
[241] Schiffbauer H, Berger MS, Ferrari P, Freudenstein D, Rowley HA, Roberts
TPL. Preoperative magnetic source imaging for brain tumor surgery: a
quantitative comparison with intraoperative sensory and motor mapping. J
Neurosurg 2002; 97: 1333-42.
56 Hugues Duffau

[242] Sobel DF, Galen CC, Schwartz BJ, et al. Locating the central sulcus:
comparison of MR anatomic and magnetoencephalographic functional
methods. Am J Neuroradiol 1993; 14: 915-25.
[243] Castillo EM, Simos PG, Venkataraman V, Breier JI, Wheless JW,
Papanicolaou AC. Mapping of expressive language cortex using magnetic
source imaging. Neurocase 2001; 7: 419-22.
[244] Maestu F, Ortiz T, Fernandez A, et al. Spanish language mapping using
MEG: a validation study. Neuroimage 2002; 17: 1579-86.
[245] Papanicolaou AC, Simos PG, Breier JI, et al. Magnetoencephalographic
mapping of the language-specific cortex. J Neurosurg 1999; 90: 85-93.
[246] Simos PG, Papanicolaou AC, Breier JI, et al. Localization of language-
specific cortex by using magnetic source imaging and electrical stimulation
mapping. J Neurosurg 1999; 91: 787-96.
[247] Nakasato N, Kumabe T, Kanno A, Ohtomo S, Mizoi K, Yoshimoto T.
Neuromagnetic evaluation of cortical auditory function in patients with
temporal lobe tumors. J Neurosurg 1997; 86: 610-8.
[248] Stippich C, Freitag P, Kassubek J, et al. Motor, somatosensory and auditory
cortex localization by fMRI and MEG. Neuroreport 1998; 9: 1953-7.
[249] Nakasato N, Seki K, Fujita S, et al. Clinical application of visual evoked
fields using an MRI-linked whole head MEG system. Frontiers Med Biol
Engng 1996; 7: 275-83.
[250] Nakasato N, Yoshimito T. Somatosensory, auditory, and visual evoked
magnetic fields in patients with brain diseases. J Clin Neurophysiol 2000;
17: 201-11.
[251] Roberts TPL, Tran Q, Ferrari P, Berger MS. Increased somatosensory
neuromagnetic fields ipsilateral to lesions in neurosurgical patients.
Neuroreport. 2002; 13: 699-702.
[252] de Jongh A, de Munck JC, Baayen JC, Jonkman EJ, Heethaar RM, van Dijk
BW. The localization of spontaneous brain activity: first results in patients
with cerebral tumors. Clin Neurophysiol 2001; 112: 378-85.
[253] de Jongh A, Baayen JC, de Munck JC, Heethaar RM, Vandertop WP, Stam
CJ. The influence of brain tumor treatment on pathological delta activity in
MEG. Neuroimage 2003; 20: 2291-301.
[254] Black P, Jaaskelainen J, Chabrerie A, Golby A, Gugino L. Minimalist
approach: functional mapping. Clin Neurosurg 2002; 49: 90-102.
[255] Chabrerie A, Nabavi A, Ozlen F, et al. Three-dimensional reconstruction for
cortical surgery: the Brigham and Women’s Hospital experience. Tech
Neurosurg 2001; 7: 61-9
 References 57

[256] Gugino LD, Aglio L, Potts G, et al. Perioperative use of transcranial

magnetic stimulation. Tech Neurosurg 2001; 7: 33-51.
[257] Krings T, Buchbinder BR, Butler WE, et al. Stereotactic transcranial
magnetic stimulation: correlation with direct electrical cortical stimulation.
Neurosurgery 1997; 41: 1319-1326.
[258] Krings T, Foltys H, Reinges MH, et al. Navigated transcranial magnetic
stimulation for presurgical planning: correlation with functional MRI.
Minim Invasive Neurosurg 2001; 44: 234-9.
[259] Macdonnell RA, Jackson GD, Curatolo JM, et al. Motor cortex localization
using functional MRI and transcranial magnetic stimulation. Neurology
1999; 53: 1462-7.
[260] Kobayashi M, Pascual-Leone A. Transcranial magnetic stimulation in
neurology. Lancet Neurol 2003; 2: 145-56.
[261] Krings T, Chiappa KH, Foltys H, Reinges MH, Cosgrove GR, Thron A.
Introducing navigated transcranial magnetic stimulation as a refined brain
mapping methodology. Neurosurg Rev 2001; 24: 171-9.
[262] Roberts DR, Vincent DJ, Speer AM, et al. Multi-modality mapping of
motor cortex: comparing echoplanar BOLD fMRI and transcranial magnetic
stimulation. Short communication. J Neurol Transm 1997; 104: 833-43.
[263] Kober H, Nimsky C, Moller M, Hastreiter P, Fahlbusch R, Ganslandt O.
Correlation of sensorimotor activation with functional magnetic resonance
imaging and magnetoencephalography in presurgical functional imaging: a
spatial analysis. Neuroimage. 2001; 14: 1214-28.
[264] Morioka T, Yamamoto T, Mizushima A, et al. Comparison of
magnetoencephalography, functional MRI, and motor evoked potentials in
the localization of the sensory-motor cortex. Neurol Res 1995; 17: 361-7.
[265] Roberts TPL, Rowley HA. Mapping of the sensorimotor cortex: functional
MR and magnetic source imaging. Am J Neuroradiol 1997; 18: 871-80.
[266] Hund M, Rezai AR, Kronberg E, et al. Magnetoencephalographic mapping:
basis of a new functional risk profile in the selection of patients with
cortical brain lesions. Neurosurgery 1997; 40: 936-43.
[267] Nakasato N, Seki K, Kawamura T, et al. Cortical mapping using an MRI-
linked whole head MEG system and presurgical decision making.
Electroencephalogr Clin Neurophysiol Suppl 1996; 47: 333-41.
[268] Schiffbauer H, Ferrari P, Rowley HA, Berger MS, Roberts TP. Functional
activity within brain tumors: a magnetic source imaging study.
Neurosurgery 2001; 49: 1313-20.
58 Hugues Duffau

[269] Benson RR, FitzGerald DB, LeSueur LL, et al. Language dominance
determined by whole brain functional MRI in patients with brain lesions.
Neurology 1999; 52: 798-809.
[270] Breier JI, Simos PG, Zouridakis G, et al. Language dominance determined
by magnetic source imaging. A comparison with the Wada procedure.
Neurology 1999; 53: 938-45.
[271] Breier JI, Simos PG, Zouridakis G, Papanicolaou AC. Lateralization of
activity associated with language function using magnetoencephalography.
A reliability study. J Clin Neurophysiol 2000; 17: 503-10.
[272] Hirata M, Kato A, Taniguchi M, et al. Determination of language
dominance with synthetic aperture magnetometry: comparison with the
Wada test. Neuroimage 2004; 23: 46-53.
[273] Kober H, Möller M, Nimsky C, Vieth J, Fahlbusch R, Ganslandt O. New
approach to localize speech relevant brain areas and hemispheric dominance
using spatially filtered magnetoencephalography. Hum Brain Mapping
2001; 14: 236-50.
[274] Lehéricy S, Cohen L, Bazin B, et al. Functional MR evaluation of temporal
and frontal language dominance compared with the Wada test. Neurology
2000; 54: 1625-33.
[275] Papanicolaou AC, Simos PG, Castillo EM, et al. Magnetocephalography: a
noninvasive alternative to the Wada procedure. J Neurosurg 2004; 100:
867-76.
[276] Simos PG, Breier JI, Zouridakis G, Papanicolaou PG. Assessment of
functional cerebral laterality for language using magnetoencephalography. J
Clin Neurophysiol 1998; 15: 364-72.
[277] Szymanski MD, Perry DW, Gage NM, et al. Magnetic source imaging of
late evoked field responses to vowels: toward an assessment of hemispheric
dominance for language. J Neurosurg 2001; 94: 445-53.
[278] Kamada K, Takeuchi F, Kuriki S, Oshiro O, Houkin K, Abe H. Functional
neurosurgical simulation with brain surface magnetic resonance images and
magnetoencephalography. Neurosurgery 1993; 33: 269-72.
[279] Clark CA, Barrick TR, Murphy MM, Bell BA. White matter fiber tracking
in patients with space-occupying lesions of the brain: a new technique for
neurosurgical planning? Neuroimage 2003; 20: 1601-8.
[280] Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion
tensor from the NMR spin echo. J Magn Reson B 1994; 103: 247-54.
[281] Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A. In vivo fiber
tractography using DT-MRI data. Magn Res Med 2000; 44: 625-32.
 References 59

[282] Catani M, Howard RJ, Pajevic S, Jones DK. Virtual in vivo interactive
dissection of white matter fasciculi in the human brain. Neuroimage 2002;
17: 77-94.
[283] Conturo TE, Lori NF, Cull TS, et al. Tracking neuronal fiber pathways in
the living human brain. Proc Natl Acad Sci USA 1999; 96: 10422-7.
[284] Mori S, Crain BJ, Chacko VP, van Zijl PC. Three-dimensional tracking of
axonal projections in the brain by magnetic resonance imaging. Ann Neurol
1999; 45: 265-9.
[285] Mori S, van Zijl PC. Fiber tracking principles and strategies: a technical
review. NMR Biomed 2002; 15: 468-80.
[286] Pierpaoli C, Basser PJ. Toward a quantitative assessment of diffusion
anisotropy. Magn Reson Med 1996; 36: 893-906.
[287] Pajevic S, Pierpaoli C. Color schemes to represent the orientation of
anisotropic tissues from diffusion tensor data: application to white matter
fiber tract mapping in the human brain. Magn Reson Med 1999; 42: 526-40.
[288] Poupon C, Clark CA, Frouin V, et al. Regularization of diffusion-based
direction maps for the tracking of brain white matter fascicles. Neuroimage
2000; 12: 184-95.
[289] Lu S, Ann D, Johnson G, Cha S. Peritumoral diffusion tensor imaging of
high-grade gliomas and metastatic brain tumors. Am J Neuroragiol 2003;
24: 937-41.
[290] Sinha S, Bastin ME, Whittle IR, Wardlaw JM. Diffusion tensor MR
Imaging of high-grade cerebral gliomas. Am J Neuroradiol 2002; 23: 520-7.
[291] Wieshmann UC, Clark CA, Symms MR, et al. Reduced anisotropy of water
diffusion in structural cerebral abnormalities demonstrated with diffusion
tensor imaging. Magn Reson Imaging 1999; 17: 1269-74.
[292] Price SJ, Burnet NG, Donovan T, et al. Diffusion tensor imaging of brain
tumors at 3 T : a potential tool for assessing white matter tract invasion?
Clin Radiol 2003; 58: 455-62.
[293] Beppu T, Inoue T, Shibata Y, et al. Measurement of fractional anisotropy
using diffusion tensor MRI in supratentorial astrocytic tumors. J
Neurooncol 2003; 63: 109-16.
[294] Gossl C, Fahrmeir L, Putz B, Auer LM, Auer DP. Fiber tracking from DTI
using linear state space models: detectability of the pyramidal tract.
Neuroimage 2002; 16: 378-88.
[295] Wieshmann UC, Symms MR, Parker GJ, et al. Diffusion tensor imaging
demonstrates deviation of fibres in normal appearing white matter adjacent
to a brain tumour. J Neurol Neurosurg Psychiatry 2000; 68: 501-3.
60 Hugues Duffau

[296] Witwer BP, Moftakhar R, Hasan KM, et al. Diffusion-tensor imaging of

white matter tracts in patients with cerebral neoplasm. J Neurosurg 2002;
97: 568-75.
[297] Jones DK, Simmons A, Williams SC, Horsfield MA. Non-invasive
assessment of axonal fiber connectivity in the human brain via diffusion
tensor MRI. Magn Reson Med 1999; 42: 37-41.
[298] Lehéricy S, Ducros M, Van de Moortele, et al. Diffusion tensor fiber
tracking shows distinct corticostriatal circuits in humans. Ann Neurol 2004;
55: 522-9.
[299] Hendler T, Pianka P, Sigal M, et al. Delineating gray and white matter
involvement in brain lesions: three-dimensional alignment of functional
magnetic resonance and diffusion-tensor imaging. J Neurosurg 2003; 99:
1018-27.
[300] Krings T, Reinges MH, Thiex R, Gilsbach JM, Thron A. Functional and
diffusion-weighted magnetic resonance images of space-occupying lesions
affecting the motor system: imaging the motor cortex and pyramidal tracts.
J Neurosurg 2001; 95: 816-24.
[301] Berman JI, Berger MS, Mukherjee P, Henry RG. Diffusion-tensor imaging-
guided tracking of fibers of the pyramidal tract combined with
intraoperative cortical stimulation mapping in patients with gliomas. J
Neurosurg 2004; 101: 66-72.
[302] Henry RG, Berman JI, Nagarajan SS, Mukherjee P, Berger MS. Subcortical
pathways serving cortical language sites: initial experience with diffusion
tensor imaging fiber tracking combined with intraoperative language
mapping. Neuroimage 2004; 21: 616-22.
[303] Holodny AI, Ollenschleger M, Liu WC, Schulder M. Identification of the
corticospinal tracts achieved using blood-oxygen-level-dependent and
diffusion functional MR imaging in patients with brain tumors. Am J
Neuroradiol 2001; 22: 83-8.
[304] Holodny AI, Ollenschleger M. Diffusion imaging in brain tumors.
Neuroimaging Clin N Am 2002; 12: 107-24.
[305] Tummala RP, Chu RM, Liu H, Hall WA. Application of duffusion tensor
imaging to magnetic-resonance-guided brain tumor resection. Pediatr
Neurosurg 2003; 39: 39-43.
[306] Lin CP, Tseng WY, Cheng HC, Chen JH. Validation of diffusion tensor
magnetic resonance axonal fiber imaging with registered manganese-
enhanced optic tracts. Neuroimage 2001; 14: 1035-47.
[307] Sobottka SB, Bredow J, Beuthien-Baumann B, Reiss G, Schackert G,
Steinmeier R. Comparison of functional brain PET images and
 References 61

intraoperative brain-mapping data using image-guided surgery. Comput

Aided Surg 2002; 7: 317-25.
[308] Gumprecht H, Ebel GK, Auer DP, Lumenta CB. Neuronavigation and
functional MRI for surgery in patients with lesion in eloquent brain areas.
Minim Invasive Neurosurg 2002; 45: 151-3.
[309] Roux FE, Ibarrola D, Tremoulet M, et al. Methodological and technical
issues for integrating functional magnetic resonance imaging data in a
neuronavigational system. Neurosurgery 2001; 49: 1145-56.
[310] Rutten GJ, Ramsey N, Noordmans HJ, et al. Toward functional
neuronavigation: implementation of functional magnetic resonance imaging
data in a surgical guidance system for intraoperative identification of motor
and language cortices. Technical note and illustrative case. Neurosurg
Focus 2003; 15: E6.
[311] Stapleton SR, Kiriakopoulos E, Mikulis D, et al. Combined utility of
functional MRI, cortical mapping, and frameless stereotaxy in the resection
of lesions in eloquent areas of brain in children. Pediatr Neurosurg 1997;
26: 68-82.
[312] Wilkinson ID, Romanowski CA, Jellinek DA, Morris J, Griffiths PD. Motor
functional MRI for preoperative and intraoperative neurosurgical guidance.
Br j Radiol 2003; 76: 98-103.
[313] Yoo SS, Talos IF, Golby AJ, Black PM, Panych LP. Evaluating
requirements for spatial resolution of fMRI for neurosurgical planning. Hum
Brain Mapp 2004; 21 : 34-43.
[314] Firsching R, Bondar I, Heinze HJ, et al. Practicability of
magnetoencephalography-guided neuronavigation. Neurosurg Rev 2002;
25: 73-8.
[315] Ganslandt O, Steinmeier R, Kober H, et al. Magnetic source imaging
combined with image-guided frameless stereotaxy: a new method in surgery
around the motor strip. Neurosurgery 1997; 41: 621-8.
[316] Mäkelä JP, Kirveskari E, Seppa M, et al. Three-dimensional integration of
brain anatomy and function to facilitate intraoperative navigation around the
sensorimotor strip. Hum Brain Mapp 2001; 12: 180-92.
[317] Nimsky C, Ganslandt O, Fahlbusch R. Functional neuronavigation and
intraoperative MRI. Adv Tech Stand Neurosurg 2004; 29: 229-63.
[318] Rezai AR, Hund M, Kronberg E, et al. The interactive use of
magnetoencephalography in stereotactic image-guided neurosurgery.
Neurosurgery1996; 39: 92-102.
62 Hugues Duffau

[319] Rezai AR, Mogilner AY, Cappell J, Hund M, Llinas RR, Kelly PJ.
Integration of functional brain mapping in image-guided neurosurgery. Acta
Neurochir Suppl (Wien) 1997; 68: 85-9.
[320] Coenen VA, Krings T, Mayfrank L, et al. Three-dimensional visualization
of the pyramidal tract in a neuronavigation system during brain tumor
surgery: first experiences and technical note. Neurosurgery 2001; 49: 86-92.
[321] Coenen VA, Krings T, Axer H, et al. Intraoperative three-dimensional
visualization of the pyramidal tract in a neuronavigation system (PTV)
reliably predicts true position of principal motor pathways. Surg Neurol
2003; 60: 381-90.
[322] Holodny AI, Schwartz TH, Ollenschleger M, Liu WC, Schulder M. Tumor
involvement of the corticospinal tract: diffusion magnetic resonance
tractography with intraoperative correlation. J Neurosurg 2001; 95: 1082.
[323] Möller-Hartmann W, Krings T, Coenen VA, et al. Preoperative assessment
of motor cortex and pyramidal tracts in central cavernoma employing
functional and diffusion-weighted magnetic resonance imaging. Surg
Neurol. 2002; 58: 302-7.
[324] Jannin P, Morandi X, Fleig OJ, et al. Integration of sulcal and functional
information for multimodal neuronavigation. J Neurosurg 2002; 96: 713-23.
[325] McDonald JD, Chong BW, Lewine JD, et al. Integration of preoperative and
intraoperative functional brain mapping in a frameless stereotactic
environment for lesions near eloquent cortex. Technical note. J Neurosurg
1999; 90: 591-8.
[326] Nimsky C, Ganslandt O, Kober H, et al. Integration of functional magnetic
resonance imaging supported by magnetoencephalography in functional
neuronavigation. Neurosurgery 1999; 44: 1249-55.
[327] Sabbah P, Foehrenbach H, Dutertre G, et al. Multimodal anatomic,
functional and metabolic brain imaging for tumor resection. Clin Imaging
2002; 26: 6-12.
[328] Kamada K, Houkin K, Takeuchi F, et al. Visualization of the eloquent
motor system by integration of MEG, functional and anisotropic diffusion-
weighted MRI in functional neuronavigation. Surg Neurol 2003; 59: 353-
62.
[329] Aoyama H, Kamada K, Shirato H, et al. Integration of functional brain
information into stereotactic irradiation treatment planning using
magnetoencephalography and magnetic resonance axonography. Int J
Radiat Oncol Biol Phys 2004; 58: 1177-83.
 References 63

[330] Dorward NL, Alberti O, Palmer JD, Kitchen ND, Thomas DGT. Accuracy
of true frameless stereotaxy: in vivo measurement and laboratory phantom
studies. J Neurosurg 1999; 90: 160-68.
[331] Gumprecht HK, Widenka DC, Lumenta CB. BrainLab VectorVision
neuronavigation system: technology and clinical experience in 131 cases.
Neurosurgery 1999; 44: 97-105.
[332] Hartkens T, Hill DL, Castellano-Smith AD, et al. Measurement and analysis
of brain deformation during neurosurgery. IEEE Trans Med Imaging 2003;
22: 82-92.
[333] Hill DL, Maurer CR Jr, Maciunas RJ, Barwise JA, Fitzpatrick JM, Wang
MY. Measurement of intraoperative brain surface deformation under a
craniotomy. Neurosurgery 1998; 43: 514-26.
[334] Navabi A, Black PMcL, Gering DT, et al. Serial intraoperative MR imaging
of brain shift. Neurosurgery 2001; 48: 787-98.
[335] Reinges MH, Nguyen HH, Krings T, Hutter BO, Rohde V, Gilsbach JM.
Course of brain shift during microsurgical resection of supratentorial
cerebral lesions: limits of conventional neuronavigation. Acta Neurochir
(Wien) 2004; 146: 369-77.
[336] Roberts DW, Hartov A, Kennedy FE, Miga MI, Paulsen KD. Intraoperative
brain shift and deformation: a quantitative analysis of cortical displacement
in 28 cases. Neurosurgery 1998; 43: 749-58.
[337] Comeau RM, Sadikot AF, Fenster A, Peters TM. Intraoperative ultrasound
for guidance and tissue shift correction in image-guided neurosurgery. Med
Phys 2000; 27: 787-800.
[338] Giorgi C, Casolino DS. Preliminary clinical experience with intraoperative
stereotactic ultrasound imaging. Stereotact Funct Neurosurg 1997; 68: 54-8.
[339] Gronningsaeter A, Kleven A, Ommedal S, et al. SonoWand, an ultrasound-
based neuronavigation system. Neurosurgery 2000; 47: 1373-9.
[340] Jodicke A, Deinsberger W, Erbe H, Kriete A, Boker DK. Intraoperative
three-dimensional ultrasonography: an approach to register brain shift using
multidimensional image processing. Minim Invasive Neurosurg 1998; 41:
13-9.
[341] Keles GE, Lamborn KR, Berger MS. Coregistration accuracy and detection
of brain shift using intraoperative sononavigation during resection of
hemispheric tumors. Neurosurgery 2003; 53: 556-564.
[342] Lindseth F, Lango T, Bang J, Nagelhus Hernes TA. Accuracy evaluation of
a 3D ultrasound-based neuronavigation system. Comput Aided Surg 2002;
7: 197-222.
64 Hugues Duffau

[343] Lindseth F, Kaspersen JH, Ommedal S, et al. Multimodal image fusion in

ultrasound-based neuronavigation: improving overview and interpretation
by integrating preoperative MRI with intraoperative 3D ultrasound. Comput
Aided Surg 2003; 8: 49-69.
[344] Pallatroni H, Hartov A, McInerney J, et al. Coregistered ultrasound as a
neurosurgical guide. Stereotact Funct Neurosurg 1999; 73: 143-7.
[345] Tuominen J, Yrjana SK, Katisko JP, Heikkila J, Koivukangas J.
Intraoperative imaging in a comprehensive neuronavigation environment for
minimally invasive brain tumor surgery. Acta Neurochir Suppl 2003; 85:
115-20.
[346] Trantakis C, Meixensberger J, Lindner D, et al. interactive neuronavigation
using 3D ultrasound.: a feasibility study. Neurol Res 2002; 24: 666-70.
[347] Unsgaard C, Ommedal S, Muller T, Gronningsaeter A, Nagelhus Hernes
TA. Neuronavigation by intraoperative three-dimensional ultrasound: initial
experience during brain tumor resection. Neurosurgery 2002; 50: 804-12.
[348] Miga MI, Paulsen KD, Hoopes PJ, et al, Kennedy FE, Hartov A, Roberts
DW. In vivo modeling of interstitial pressure in the brain under surgical
load using finite elements. J Biomech Eng 2000; 122: 354-63.
[349] Platenik LA, Miga MI, Roberts DW, et al. In vivo quantification of
retraction deformation modeling for updated image-guidance during
neurosurgery. IEEE Trans Biomed Eng 2002; 49: 823-35.
[350] Roberts DW, Miga MI, Hartov A, et al. Intraoperative updated
neuroimaging using brain modeling and sparse data. Neurosurgery 1999;
45: 1199-207.
[351] Roberts DW, Lunn K, Sun H, et al. Intra-operative image updating.
Stereotact Funct Neurosurg 2001; 76: 148-50.
[352] Nimsky C, Ganslandt O, Hastreiter P, Fahlbusch R. Intraoperative
compensation for brain shift. Surg Neurol 2001; 56: 357-64.
[353] Albayrak B, Samdani AF, Black PM. Intra-operative magnetic resonance
imaging in neurosurgery. Acta Neurochir (Wien) 2004; 146: 543-56.
[354] Black PM, Moriarty T, Alexander E 3rd, et al. Development and
implementation of intraoperative magnetic resonance imaging and its
neurosurgical applications. Neurosurgery 1997; 41: 831-42.
[355] Chu RM, Tummala RP, Kucharczyk J, Truwit CL, Maxwell RE. Minimally
invasive procedures. Interventional MR image-guided functional
neurosurgery. Neuroimaging Clin N Am 2001; 11: 715-25.
[356] Fenchel S, Boll DT, Lewin JS. Intraoperative MR imaging. Magn Reson
Imaging Clin N Am 2003; 11: 431-47.
 References 65

[357] Gluch L, Walker DG. Intraoperative magnetic resonance: the future of

surgery. ANZ J Surg 2002;72:426-36.
[358] Jolesz FA, Talos IF, Schwartz RB, et al. Intraoperative magnetic resonance
imaging and magnetic resonance imaging-guided therapy for brain tumors.
Neuroimaging Clin N Am 2002; 12: 665-83.
[359] Kahn T. Intraoperative MRI in nueorsurgery: becoming mature. Eur Radiol
2002; 12: 2617-8.
[360] Keles GE. Intracranial neuronavigation with intraoperative magnetic
resonance imaging. Curr Opin Neuro. 2004; 17: 497-500.
[361] Lewin JS, Metzger A, Selman WR. Intraoperative magnetic resonance
image guidance in neurosurgery. J Magn Reson Imaging 2000; 12: 512-24.
[362] Lipson AC, Gargollo PC, Black PM. Intraoperative magnetic resonance
imaging: considerations for the operating room of the future. J Clin
Neurosci 200l; 8: 305-10.
[363] Nimsky C, Ganslandt O, Kober H, Buchfelder M, Falbusch R.
Intraoperative magnetic resonance imaging combined with neuronavigation:
a new concept. Neurosurgery 2001; 48: 1082-9.
[364] Nimsky C, Ganslandt O, von Keller B, Romstöck J, Fahlbusch R.
Intraoperative high-field-strength MR imaging: implementation and
experience in 200 patients. Radiology 2004; 233: 67-78.
[365] Ram Z, Hadani M. Intraoperative imaging--MRI. Acta Neurochir Suppl
2003; 88: 1-4.
[366] Schwartz RB, Hsu L, Wong TZ, et al. Intraoperative MR imaging guidance
for intracranial neurosurgery: experience with the first 200 cases. Radiology
1999; 211: 477-88.
[367] Seifert V. How to choose a magnet: reflections on the development of MRI-
guided neurosurgery. Acta Neurochir Suppl 2003; 85: 15-20.
[368] Steinmeier R, Fahlbusch R, Ganslandt O, et al. Intraoperative magnetic
resonance imaging with the magnetom open scanner: concepts,
neurosurgical indications, and procedures: a preliminary report.
Neurosurgery 1998; 43: 739-47.
[369] Tronnier VM, Wirtz CR, Knauth M, et al. Intraoperative diagnostic and
interventional magnetic resonance imaging in neurosurgery. Neurosurgery
1997; 40: 891-900.
[370] Wirtz CR, Knauth M, Staubert A, et al. Clinical evaluation and follow-up
results for intraoperative magnetic resonance imaging in neurosurgery.
Neurosurgery 2000; 46: 1112-20.
[371] Nimsky C, Ganslandt O, Cerny S, Hastreiter P, Greiner G, Fahlbusch R.
Quantification of, vizualisation of, and compensation fro brain shift using
66 Hugues Duffau

intraoperative magnetic resonance imaging. Neurosurgery 2000; 47: 1070-

80.
[372] Hall WA, Liu H, Maxwell RE, Truwit CL. Influence of 1.5-Tesla
intraoperative MR imaging on surgical decision making. Acta Neurochir
Suppl 2003; 85: 29-37.
[373] Bernays RL, Kollias SS, Khan N, Brandner S, Meier S, Yonekawa Y.
Histological yield, complications, and technological considerations in 114
consecutive frameless stereotactic biopsy procedures aided by open
intraoperative magnetic resonance imaging. J Neurosurg 2002; 97: 354-62.
[374] Hall WA, Liu H, Martin AJ, Truwit CL. Minimally invasive procedures.
Interventional MR image-guided neurobiopsy. Neuroimaging Clin N Am
2001; 11: 705-13.
[375] Tronnier V, Staubert A, Wirtz R, Knauth M, Bonsanto M, Kunze S. MRI-
guided brain biopsies using a 0.2 Tesla open magnet. Minim Invasive
Neurosurg 1999; 42: 118-22.
[376] Alexander E 3rd. Optimizing brain tumor resection. Midfield interventional
MR imaging. Neuroimaging Clin N Am 2001; 11: 659-72.
[377] Bohinski RJ, Kokkino AK, Warnick RE, et al. Glioma resection in a shared-
resource magnetic resonance operating room after optimal image-guided
frameless stereotactic resection. Neurosurgery 2001; 48: 731-42.
[378] Bradley WG. Achieving gross total resection of brain tumors: intraoperative
MR imaging can make a big difference. Am J Neuroradiol 2002; 23: 348-9.
[379] Knauth M, Wirtz CR, Tronnier VM, Aras N, Kunze S, Sartor K.
Intraoperative MR imaging increases the extent of tumor resection in
patients with high-grade gliomas. Am J Neuroradiol 1999; 20: 1642-6.
[380] Nimsky C, Ganslandt O, Tomandl B, Buchfelder M, Fahlbusch R. Low-
field magnetic resonance imaging for intraoperative use in neurosurgery: a 5
year experience. Eur Radiol 2002; 12: 2690-703.
[381] Nimsky C, Ganslandt O, Buchfelder M, Fahlbusch R. Glioma surgery
evaluated by intraoperative low-field magnetic resonance imaging. Acta
Neurochir Suppl 2003; 85: 55-63.
[382] Schneider JP, Schultz T, Schmidt F, et al. Gross-total surgery of
supratentorial low-grade gliomas under intraoperative MR guidance. Am J
Neuroradiol 2001; 22: 89-98.
[383] Tummala RP, Chu RM, Liu H, Truwit CL, Hall WA. Optimizing brain
tumor resection. High-field interventional MR imaging. Neuroimaging Clin
N Am 2001; 11: 673-83.
 References 67

[384] Hall WA, Liu H, Martin AJ, Pozza CH, Maxwell RE, Truwit CL. Safety,
efficacy, and functionality of high-field-strengh interventional magnetic
resonance imaging fir neurosurgery. Neurosurgery 2000; 46: 632-42.
[385] Martin AJ, Hall WA, Liu H, et al. Brain tumor resection: intraoperative
monitoring with high-field-strength MR imaging-initial results. Radiology
2000; 215: 221-8.
[386] Sutherland GR, Kaibara T, Louw D, Hoult DI, Tomanek B, Saunders J. A
mobile high-field magnetic resonance system for neurosurgery. J Neurosurg
1999; 91: 804-13.
[387] Truwit CL, Hall WA. Intraoperative MR systems. High-field approaches.
Neuroimaging Clin N Am 2001; 11: 645-50.
[388] Liu H, Hall WA, Truwit CL. The roles of functional MRI in MR-guided
neurosurgery in a combined 1.5 Tesla MR-operating room. Acta Neurochir
Suppl 2003; 85: 127-35.
[389] Cannestra AF, Black KL, Martin NA, et al. Topographical and temporal
specificity of human intraoperative optical intrinsic signals. Neuroreport
1998; 9: 2557-63.
[390] Cannestra AF, Bookheimer SY, Pouratian N, et al. Temporal and
topographical characterization of language cortices using intraoperative
optical intrinsic signals. Neuroimage 2000; 12: 41-54.
[391] Cannestra AF, Pouratian N, Bookheimer SY, Martin NA, Beckerand DP,
Toga AW. Temporal spatial differences observed by functional MRI and
human intraoperative optical imaging. Cereb Cortex 2001; 11: 773-82.
[392] Haglund MM, Ojemann Ga, Hochman DW. Optical imaging of epileptiform
and functional activity in human cerebral cortex. Nature 1992; 358: 668-71.
[393] Haglund MM. Intraoperative optical imaging of epileptiform and functional
activity. Neurosurg Clin N Am 1997; 8: 413-20.
[394] Pouratian N, Bookheimer SY, O’Farrell AM, et al. Optical imaging of
bilingual cortical representations. J Neurosurg 2000; 93: 676-81.
[395] Pouratian N, Sheth S, Bookheimer SY, Martin NA, Toga AW. Applications
and limitations of perfusion-dependent functional brain mapping for
neurosurgical guidance. Neurosurg Focus 2003; 15: E2.
[396] Pouratian N, Sheth S, Martin NA, Toga AW. Shedding light on brain
mapping: advances in human optical imaging.Trends Neurosci. 2003; 26:
277-82.
[397] Sato K, Nariai T, Sasaki S, et al. Intraoperative intrinsic optical imaging of
neuronal activity from subdivisions of the human primary somatosensory
cortex. Cereb Cortex 2002; 12: 269-80
68 Hugues Duffau

[398] Schwartz TH, Chen LM, Friedman RM, Spencer DD, Roe AW.
Intraoperative optical imaging of human face cortical topography: a case
study. Neuroreport 2004; 15: 1527-31.
[399] Haglund MM, Berger MS, Hochman DW. Enhanced optical imaging of
human gliomas and tumor margins. Neurosurgery 1996; 38: 308-17.
[400] Kabuto M, Kabuto T, Kobayashi H, et al. Experimental and clinical study of
detection of glioma at surgery using fluorescent imaging by a surgical
microscope after fluorescein administration. Neurol Res 1997; 19: 9-16.
[401] Kuroiwa T, Kajimoto Y, Ohta T. Comparison between operative findings on
malignant glioma by a fluorescein surgical microscopy and histological
findings. Neurol Res 1999; 21: 130-4.
[402] Lin WC, Toms SA, Johnson M, Jansen ED, Mahadevan-Jansen A. In vivo
brain tumor demarcation using optical spectroscopy. Photochem Photobiol
2001; 73: 396-402.
[403] Sakatani K, Kashiwasake-Jibu M, Terada H, Zuo H. Development of
surgical confocal scanning microscope for intraoperative imaging of brain
tumors using near infrared fluorescence: technical note. Neurol Res 2000;
22: 533-6.
[404] Shinoda J, Yano H, Yoshimura SI, et al. Fluorescence-guided resection of
glioblastoma multiforme by using high-dose fluorescein sodium. J
Neurosurg 2003; 99: 597-603.
[405] Stummer W, Steep H, Möller G, Ehrhardt A, Leonhard M, Reulen HJ.
Technical principles for protoporphyrin-IX-fluorescence guided
microsurgical resection of malignant glioma tissue. Acta Neurochir (Wien)
1998; 140: 995-1000.
[406] Stummer W, Novotny A, Stepp H, Goetz C, Bise A, Reulen HJ.
Fluorescence-guided resection of glioblastoma multiforme by using 5-
aminolevulinic acid-induced porphyrins: a prospective study in 52
consecutive patients. J Neurosurg 2000; 93: 1003-13.
[407] Stummer W, Reulen HJ, Novotny A, Stepp H, Tonn JC. Fluorescence-
guided resections of malignant gliomas: an overview. Acta Neurochir Suppl
2003; 88: 9-12.
[408] Agari S, Rohrborn HJ, Engelhorn T, Stolke D. Intraoperative
characterization of gliomas by near-infrared spectroscopy: possible
association with prognosis. Acta Neurochir (Wien) 2003; 145: 453-9.
[409] Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V. Near-infrared
indocyanine green video angiography: a new method for intraoeprative
assessment of vascular flow. Neurosurgery 2003; 52: 132-9.
 References 69

[410] Bakken HE, Kawasaki H, Oya H, Greenlee JDW, Howard MA. A device
for cooling localized regions of human cerebral cortex. J Neurosurg 2003;
99: 604-8.
[411] Lee GP, Loring DW, Smith JR, Flanigin HF. Intraoperative hippocampal
cooling and Wada memory testing in the evaluation of amnesia risk
following anterior temporal lobectomy. Arch Neurol 1995; 52: 857-61.
[412] Lee GP, Smith JR, Loring DW, Flanigin HF. Intraoperative thermal
inactivation of the hippocampus in an effort to prevent global amnesia after
temporal lobectomy. Epilepsia 1995; 36: 892-8.
[413] Keles GE, Berger MS. Advances in neurosurgical technique in the current
management of brain tumors. Semin Oncol 2004; 31: 659-65.
[414] Allison T, McArthy G, Wood CC, Darcey TM, Spencer DD, Williamson
PD. Human cortical potentials evoked by stimulation of the median nerve. I.
Cytoarchitectonic areas generating short latency activity. J Neurosurg 1989;
62: 694-710.
[415] Babu KS, Chandy MJ: Reliability of somatosensory evoked potentials in
intraoperative localization of the central sulcus in patients with perirolandic
mass lesions. Br J Neurosurg 1997; 11: 411-417.
[416] Cedzich C, Taniguchi M, Schäfer S, Schramm J. Somatosensory evoked
potential phase reversal and direct motor cortex stimulation during surgery
in and around the central region. Technical application. Neurosurgery 1996;
38: 962-971.
[417] Grant GA, Farrell D, Silbergeld DL. Continuous somatosensory evoked
potential monitoring during brain tumor resection. Report of four cases and
review of the literature. J Neurosurg 2002; 97: 709-13.
[418] Helmers SL. Evoked potentials for cortical mapping in children and adults,
in Loftus CM, Batjer HH, eds: Techniques in Neurosurgery. Philadelphia:
Lippincott Williams & Wilkins, 2001, Vol 7, pp 4-11.
[419] McCarthy G, Allison T, Spencer DD: Localization of the face area of
human sensorimotor cortex by intracranial recording of somatosensory
evoked potentials. J Neurosurg 1993; 79: 874-84.
[420] Mine S, Oka N, Yamaura, Nakajima Y. Presurgical functional localization
of primary somatosensory cortex by dipole tracing method of scalp-skull-
brain head model applied to somatosensory evoked potential.
Electroencephalogr Clin Neurophysiol 1998; 108: 226-33.
[421] Romstöck J, Fahlbusch R, Ganslandt O, Nimsky C, Strauss C. Localisation
of the sensorimotor cortex during surgery for brain tumours: feasibility and
waveform patterns of somatosensory evoked potentials. J Neurol Neurosurg
Psychiatry 2002; 72: 221-9.
70 Hugues Duffau

[422] Wood CC, Spencer DD, Allison D, McCarthy G, Williamson PD, Goff WR.
Localization of human sensorimotor cortex during surgery by cortical
surface recording of somatosensory evoked potentials. J Neurosurg 1988;
68: 99-111.
[423] King RB, Schell GR: Cortical localization and monitoring during cerebral
operations. J Neurosurg 1987; 67: 210-9.
[424] Wiedemayer H, Sandalcioglu IE, Armbruster W, Regel J, Schafer H, Stolke
D. False negative findings in intraoperative SEP monitoring: analysis of 658
consecutive neurosurgical cases and review of published reports. J Neurol
Neurosurg Psychiatry 2004; 75: 280-6.
[425] Neuloh G, Schramm J. Motor evoked potential monitoring for the surgery
of brain tumours and vascular malformations. Adv Tech Stand Neurosurg
2004; 29:171-228.
[426] Neuloh G, Pechstein U, Cedzich C, Schramm J. Motor evoked potential
monitoring with supratentorial surgery. Neurosurgery 2004; 54: 1061-70.
[427] Sala F, Lanteri P. Brain surgery in motor areas: the invaluable assistance of
intraoperative neurophysiological monitoring. J Neurosurg Sci 2003; 47:
79-88.
[428] Taniguchi M, Cedzich C, Schramm J. Modification of cortical stimulation
for motor evoked potentials under general anesthesia: technical description.
Neurosurgery 1993; 32: 219-26.
[429] Kombos T, Suess O, Ciklatekerlio O, Brock M. Monitoring of
intraoperative motor evoked potentials to increase the safety of surgery in
and around the motor cortex. J Neurosurg 2001; 95: 608-14.
[430] Kombos T, Suess O, Funk T, Kern BC, Brock M. Intraoperative mapping of
the motor cortex during surgery in and around the motor cortex. Acta
Neurochir 2000; 142: 263-8.
[431] Zentner J, Hufnagel A, Pechstein U, Wolf HK, Schramm J. Functional
results after resective procedures involving the supplementary motor area. J
Neurosurg 1996; 85: 542-549.
[432] Ikeda A, Miyamoto S, Shibasaki H. Cortical motor mapping in epilepsy
patients: information from subdural electrodes in presurgical evaluation.
Epilepsia 2002; 43 Suppl 9: S56-60.
[433] Lesser RP, Lüders H, Klem G, et al. Extraoperative cortical functional
localization in patients with epilepsy. J Clin Neurophysiol 1987; 4: 27-53.
[434] Lesser RP, Arroyo S, Crone N, Gordon B. Motor and sensory mapping of
the frontal and occipital lobes. Epilepsia 1998; 39 Suppl 4: S69-80.
 References 71

[435] Lüders H, Lesser RP, Dinner DS, Morris HH, Wyllie E, Godoy J.
Localization of cortical function: new information from extraoperative
monitoring of patients with epilepsy. Epilepsia 1988; 29 Suppl 2: S56-65.
[436] Nii Y, Uematsu S, Lesser RP, Gordon B. Does the central sulcus divide
motor and sensory functions? Cortical mapping of human hand areas as
revealed by electrical stimulation through subdural grid electrodes.
Neurology 1996; 46: 360-7.
[437] Schlaffer L, Lüders HO, Beck GJ. Quantitative comparison of language
deficits produced by extraoperative electrical stimulation of Broca’s,
Wernicke’s, and basal temporal language areas. Epilepsia 1996; 37: 463-75.
[438] Uematsu S, Lesser R, Fisher RS, et al. Motor and sensory cortex in humans:
topography studied with chronic subdural stimulation. Neurosurgery 1992;
31: 59-71.
[439] Urasaki E, Uematsu S, Gordon B, Lesser RP. Cortical tongue area studied
by chronically implanted subdural electrodes--with special reference to
parietal motor and frontal sensory responses. Brain 1994; 117: 117-32.
[440] Chitoku S, Otsubo H, Harada Y, et al. Extraoperative cortical stimulation of
motor function in children. Pediatr Neurol 2001; 24: 344-50.
[441] Adelson PD, Black PM, Madsen JR, et al. Use of subdural grids and strip
electrodes to identify a seizure focus in children. Pediatr Neurosurg 1995;
22: 174-80.
[442] Cohen-Gadol AA, Britton JW, Collignon FP, Bates LM, Cascino GD,
Meyer FB. Nonlesional central lobule seizures: use of awake cortical
mapping and subdural grid monitoring for resection of seizure focus. J
Neurosurg 2003; 98: 1255-62.
[443] Lesser RP. Remission of intractable partial epilepsy following implantation
of intracranial electrodes. Neurology 2002; 58: 1317.
[444] Krone NE, Miglioretti DL, Gordon B, et al. Functional mapping of human
sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha
and beta event-related desynchronization. Brai. 1998; 121: 2271-99.
[445] Krone NE, Miglioretti DL, Gordon B, Lesser RP. Functional mapping of
human sensorimotor cortex with electrocorticographic spectral analysis. II.
Event-related synchronization in the gamma band. Brain 1998; 121: 2301-
15.
[446] Krone NE. Functional mapping with ECoG spectral analysis. Adv Neurol
2000; 84: 343-51.
[447] Kirsch HE, Sepkuty JP, Crone NE. Multimodal functional mapping of
sensorimotor cortex prior to resection of an epileptogenic perirolandic
lesion. Epilepsy Behav 2004; 5: 407-10.
72 Hugues Duffau

[448] Matsumoto R, Mair DR, LaPresto E, et al. Functional connectivity in the

human language system: a cortico-cortical evoked potential study. Brain
2004; 127: 2316-30.
[449] Onal C, Otsubo H, Araki T, et al. Complications of invasive subdural grid
monitoring in children with epilepsy. J Neurosurg 2003; 98: 1017-26.
[450] Berger MS, Rostomily RC. Low-grade gliomas: Functional mapping
resection strategies, extent of resection, and outcome. J Neurooncol 1997;
34: 85-101.
[451] Black PM, Ronner SF. Cortical mapping for defining the limits of tumor
resection. Neurosurgery 1987; 25: 786-92.
[452] Danks RA, Rogers M, Aglio LS, Gugino LD, Black PM. Patient tolerance
of craniotomy performed with the patient under local anesthesia and
monitored conscious sedation. Neurosurgery 1998; 42: 28-36.
[453] Danks RA, Aglio LS, Gugino LD, Black PM. Craniotomy under local
anesthesia and monitored conscious sedation for the resection of tumors
involving eloquent cortex. J Neurooncol 2000; 49:131-9.
[454] Duffau H, Capelle L, Sichez JP, et al. Intraoperative direct electrical
stimulations of the central nervous system: the Salpêtrière experience with
60 patients. Acta Neurochir (Wien) 1999; 141:1157-67.
[455] Ebel H, Ebel M, Schillinger G, Klimik M, Sobesky J, Klug N. Surgery of
intrinsic cerebral neoplasms in eloquent areas under local anesthesia. Minim
Invasive Neurosurg 2000; 43: 192-6.
[456] Ebeling U, Schmid UD, Ying H, Reulen HJ. Safe surgery of lesions near the
motor cortex using intraoperative mapping techniques: a report on 50
patients. Acta Neurochir (Wien) 1992; 119: 23-8.
[457] Fukaya C, Katayama Y, Yoshino A, Kobayashi K, Kasai M, Oshima H.
Intraoperative wake-up procedure with propofol and laryngeal mask for
optimal excision of brain tumor in eloquent areas. J Clin Neurosci
2001;8:253-5.
[458] Horstmann GA, Talies S, Westermann B, Reinhardt HF.
Microstereometrically guided cortical stimulation for the intraoperative
identification of the central motor strip. Stereotact Funct Neurosurg 1995;
65: 130-5.
[459] Krombach GA, Spetzger U, Rohde V, Gilsbach JM. Intraoperative
localization of functional regions in the sensorimotor cortex by
neuronavigation and cortical mapping. Comput Aided Surg 1998; 32: 64-73.
[460] Lanier WL. Brain tumor resection in the awake patient. Mayo Clin Proc
2001; 76: 677-87.
 References 73

[461] Lumenta CB, Gumprecht HK, Leonardi MA, Gerstner W, Brehm B. Three-
dimensional computer-assisted stereotactic-guided microneurosurgery
combined with cortical mapping of the motor area by direct
electrostimulation. Minim Invasive Neurosurg 1997; 40: 50-4.
[462] Manninen PH, Tan TK. Postoperative nausea and vomiting after craniotomy
for tumor surgery: a comparison between awake craniotomy and general
anesthesia. J Clin Anesth 2002;14:279-83.
[463] Meyer FB, Bates LM, Goerss BS, et al. Awake craniotomy for aggressive
resection of primary gliomas located in eloquent brain. Mayo Clin Proc
2001; 76: 677-87.
[464] Nikas DC, Danks RA, Black PM. Tumor surgery under local anesthesia, in
Loftus CM, Batjer HH, eds: Techniques in Neurosurgery. Philadelphia:
Lippincott Williams & Wilkins, 2001, Vol 7, pp 70-84.
[465] Peraud A, Meschede M, Eisner W, Ilmberger J, Reulen HJ. Surgical
resection of grade II astrocytomas in the superior frontal gyrus.
Neurosurgery 2002; 50: 966-77.
[466] Peraud A, Ilmberger J, Reulen HJ. Surgical resection of gliomas WHO
grade II and III located in the opercular region. Acta Neurochir (Wien)
2004; 146: 9-17.
[467] Reithmeier T, Krammer M, Gumprecht H, Gerstner W, Lumenta CB.
Neuronavigation combined with electrophysiological monitoring for
surgery of lesions in eloquent brain areas in 42 cases: a retrospective
comparison of the neurological outcome and the quality of resection with a
control group with similar lesions. Minim Invasive Neurosurg 2003; 46: 65-
71.
[468] Reulen HJ, Schmid UD, Ilmberger J, Eisner W, Bise K. Tumor surgery of
the speech cortex in local anesthesia. Neuropsychological and
neurophysiological monitoring during operations in the dominant
hemisphere. Nervenarzt 1997; 68: 813-24.
[469] Sarang A, Dinsmore J. Anesthesia for awake craniotomy – evolution of a
technique that facilitates awake neurological testing. Br J Anaesth
2003;90:161-5.
[470] Signorelli F, Guyotat J, Isnard J, Schneider F, Mohammedi R, Bret P. The
value of cortical stimulations applied to the surgery of malignant gliomas in
language areas. Neurol Sci 2001; 22: 3-10.
[471] Signorelli F, Guyotat J, Mottolese C, Schneider F, D'Acunzi G, Isnard J.
Intraoperative electrical stimulation mapping as an aid for surgery of
intracranial lesions involving motor areas in children. Childs Nerv Syst
2004; 20: 420-6.
74 Hugues Duffau

[472] Suess O, Kombos T, Hoell T, Baur S, Pietilae T, Brock M. A new cortical

electrode for neuronavigation-guided intraoperative neurophysiological
monitoring: technical note. Acta Neurochir (Wien) 2000; 142: 329-32.
[473] Taylor MD, Bernstein M. Awake craniotomy with brain mapping as a
routine surgical approach to treating patients with supratentorial intraaxial
tumors: a prospective trial of 200 cases. J Neurosurg 1999; 90: 35-41.
[474] Wagner W, Tschiltschke W, Niendorf WR, Schroeder HW, Gaab MR.
Infrared-based neuronavigation and cortical motor stimulation in the
management of central-region tumors. Stereotact Funct Neurosurg 1997; 68
:112-6.
[475] Walsh AR, Schmidt RH, Marsh HT. Cortical mapping and resection under
local anesthetic as an aid to surgery of low and intermediate grade gliomas.
Br J Neurosurg 1990; 4: 485-91.
[476] Whittle IR, Borthwick S, Haq N. Brain dysfunction following « awake »
craniotomy, brain mapping and resection of glioma. Br J Neurosurg 2003;
17: 130-7.
[477] Mesulam MM. From sensation to cognition. Brain 1998; 121: 1013-52.
[478] Berger MS, Ojemann GA, Lettich E. Neurophysiological monitoring during
astrocytoma surgery. Neurosurg Clin N Am 1990; 1: 65-70.
[479] Berger MS, Ojemann GA. Intraoperative brain mapping techniques in
neuro-oncology. Stereotactic Funct Neurosurg 1992; 58: 153-61.
[480] Berger MS. Lesions in functional (« eloquent ») cortex and subcortical
white matter. Clin Neurosurg 1994; 41: 444-63.
[481] Berger MS. Functional mapping-guided resection of low-grade gliomas.
Clin Neurosurg 1995; 42:437-52.
[482] Duffau H. Intraoperative direct subcortical stimulation for identification of
the internal capsule, combined with an image-guided stereotactic system
during surgery for basal ganglia lesions. Surg Neurol 2000; 53: 250-4.
[483] Duffau H, Capelle L, Sichez N, et al. Intraoperative mapping of the
subcortical language pathways using direct stimulations. An anatomo-
functional study. Brain 2002; 125: 199-214.
[484] Eisner W, Burtsher J, Bale R, et al. Use of neuronavigation and
electrophysiology in surgery of subcortically located lesions in the
sensorimotor strip. J Neurol Neurosurg Psychiatry 2002; 72: 378-81.
[485] Haglund M, Berger M, Shamseldin M, Lettich E, Ojemann GA. Cortical
localization of temporal lobe language sites in patients with gliomas.
Neurosurgery 1994; 34: 567-74.
 References 75

[486] Haglund MM, Berger M. Functional mapping of motor sensory, and

language pathways during low-grade glioma removal. Tech Neurosurg
1996; 2: 141-9.
[487] Keles GE, Lundin DA, Lamborn KR, Chang EF, Ojemann G, Berger MS.
Intraoperative subcortical stimulation mapping for hemispherical
perirolandic gliomas located within or adjacent to the descending motor
pathways: evaluation of morbidity and assessment of functional outcome in
294 patients. J Neurosurg 2004;100: 369-75.
[488] Matz PG, Cobbs C, Berger MS. Intraoperative cortical mapping as a guide
to the surgical resection of gliomas. J Neurooncol 1999; 42: 233-45.
[489] Skirboll SS, Ojemann GA, Berger MS, Lettich E, Winn HR. Functional
cortex and subcortical white matter located within gliomas. Neurosurgery
1996; 38: 678-84.
[490] Yingling C, Ojemann S, Dobson B, Harrington MJ, Berger MS.
Identification of motor pathways during tumor surgery facilitated by
multichannel electromyographic recording. J Neurosurg 1999; 91: 922-7.
[491] Duffau H, Capelle L, Denvil D, et al. The role of dominant premotor cortex
in language: a study using intraoperative functional mapping in awake
patients. Neuroimage 2003; 20: 1903-14.
[492] Duffau H, Capelle L, Denvil D, et al. Usefulness of intraoperative electrical
sub-cortical mapping in surgery of low-grade gliomas located within
eloquent regions: functional results in a consecutive series of 103 patients. J
Neurosurg 2003; 98: 764-78.
[493] Duffau H, Capelle L, Lopes M, Faillot T, Sichez JP, Fohanno D. The insular
lobe: physiopathological and surgical considerations. Neurosurgery 2000;
47: 801-10.
[494] Duffau H, Velut S, Mitchell MC, Gatignol P, Capelle L. Intra-operative
mapping of the subcortical visual pathways using direct electrical
stimulations. Acta Neurochir (Wien) 2004; 146: 265-9.
[495] Duffau H, Gatignol P, Denvil D, Lopes M, Capelle L. The articulatory loop:
study of the subcortical connectivity by electrostimulation. Neuroreport
2003; 14: 2005-8.
[496] Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N,
Capelle L. New insights into the anatomo-functional connectivity of the
semantic system: a study using cortico-subcortical electrostimulations.
Brain, 2005; 128: 797-810.
[497] Steinmeier R, Sobottka SR, Reiss G, Bredow J, Gerber J, Schackert G.
Surgery of low-grade gliomas near speech-eloquent regions: brainmapping
versus preoperative functional imaging. Onkologie 2002;25: 552-7.
76 Hugues Duffau

[498] Bittar RG, Olivier A, Sadikot AF, et al. Localization of somatosensory

function by using positron emission tomography scanning: a comparison
with intraoperative cortical stimulation. J Neurosurg 1999; 91: 478-83.
[499] Braun V, Dempf S, Tomczak R, Wunderlich A, Weller R, Richter HP.
Functional cranial neuronavigation. Direct integration of fMRI and PET
data. J Neuroradiol 2000; 27: 157-163.
[500] Brannen JH, Badie B, Moritz CH, Quigley M, Meyerand ME, Haughton
VM. Reliability of functional MR Imaging with word-generation tasks for
mapping Broca’s area. AJNR 2001; 22: 1711-8.
[501] Fandino J, Kollias SS, Wieser HG, Valavanis A, Yonekawa Y.
Intraoperative validation of functional magnetic resonance imaging and
cortical reorganization patterns in patients with brain tumors involving the
primary motor cortex. J Neurosurg1999; 91: 238-50.
[502] FitzGerald DB, Cosgrove GR, Ronner S, et al. Location of language in the
cortex: a comparison between functional MR imaging and electrocortical
stimulation. AJNR 1997; 18: 1529-39.
[503] Jack JR, Thompson RM, Butts RK, et al. Sensory motor cortex: correlation
of presurgical mapping with functional MR imaging and invasive cortical
mapping. Radiology 1994; 190: 85-92.
[504] Lurito JT, Lowe MJ, Sartorius C, Mathews VP. Comparison of fMRI and
intraoperative direct cortical stimulation in localization of receptive
language areas. J Comput Assist Tomogr 2000; 24: 99-105.
[505] Puce A, Constable RT, Luby ML, et al. Functional magnetic resonance
imaging of sensory and motor cortex: comparison with electrophysiological
localization. J Neurosurg 1995; 83: 262-70.
[506] Pujol J, Conesa G, Deus J, Lopez-Obarrio L, Isamat F, Capdevila A.
Clinical application of functional magnetic resonance imaging in
presurgical identification of the central sulcus. J Neurosurg 1998; 88: 863-
9.
[507] Ruge MI, Victor J, Hosain S, et al. Concordance between functional
magnetic resonance imaging and intraoperative language mapping.
Stereotact Funct Neurosurg 1999; 72: 95-102.
[508] Rutten GJ, van Rijen PC, van Veelen CW, Ramsey NF. Language area
localization with three-dimensional functional magnetic resonance imaging
matches intrasulcal electrostimulation in Broca’s area. Ann Neurol 1999;
46: 405-8.
[509] Schlosser M, Luby M, Spencer DD, Awad IA, McCarthy G. Comparative
localization of auditory comprehension by using functional magnetic
resonance imaging and cortical stimulation. J Neurosurg 1999; 91: 626-635.
 References 77

[510] Schulder M, Maldjian LA, Liu WC, et al. Functional image-guided surgery
of intracranial tumors located near the sensorimotor cortex. J Neurosurg
1998; 89: 412-418.
[511] Signorelli F, Guyotat J, Schneider F, Isnard J, Bret P. Technical refinements
for validating functional MRI-based neuronavigation data by electrical
stimulation during cortical language mapping. Minim Invasive Neurosurg
2003; 46: 265-8.
[512] Yousry TA, Schmid UD, Jassoy AG, et al. Topography of the cortical motor
hand area: prospective study with functional MR imaging and direct motor
mapping at surgery. Radiology 1995; 195: 23-9.
[513] Castillo EM, Simos PG, Wheless JW, et al. Integrating sensory and motor
mapping in a comprehensive MEG protocol: clinical validity and
replicability. Neuroimage. 2004; 21: 973-83.
[514] Morioka T, Mizushima A, Yamamoto T, et al. Functional mapping of the
sensorimotor cortex: combined use of magnetoencephalography, functional
MRI, and motor evoked potentials. Neuroradiology 1995; 37: 526-30.
[515] Ishibashi H, Morioka T, Nishio S, Shigeto H, Yamamoto T, Fukui M.
Magnetoencephalographic investigation of somatosensory homunculus in
patients with peri-Rolandic tumors. Neurol Res 2001; 23: 29-38.
[516] Roberts TP, Zusman E, Mcdermott M, Barbaro N, Rowley HA. Correlation
of functional magnetic source imaging with intraoperative cortical
stimulation in neurosurgical patients. J Image Guid Surg 1995; 1: 339-47.
[517] Roberts TP, Ferrari P, Perry D, Rowley HA, Berger MS. Presurgical
mapping with magnetic source imaging: comparisons with intraoperative
findings. Brain Tumor Pathol 2000; 17: 57-64.
[518] Schiffbauer H, Berger MS, Ferrari P, Freudenstein D, Rowley HA, Roberts
TP. Preoperative magnetic source imaging for brain tumor surgery: a
quantitative comparison with intraoperative sensory and motor mapping.
Neurosurg Focus 2003;15:E7.
[519] Simos PG, Breier JI, Maggio WW, et al. Atypical temporal lobe language
representation: MEG and intraoperative stimulation mapping correlation.
Neuroreport 1999; 10: 139-42.
[520] Yetkin FZ, Mueller WM, Morris GL, et al. Functional MR activation
correlated with intraoperative cortical mapping. AJNR 1997; 18: 1311-5.
[521] Roux FE, Ibarrola D, Tremoulet M, et al. Methodological and technical
issues for integrating functional magnetic resonance imaging data in a
neuronavigational system. Neurosurgery 2001; 49: 1145-57.
[522] Lehéricy S, Duffau H, Cornu P, et al. Correspondence between functional
magnetic resonance imaging somatotopy and individual brain anatomy of
78 Hugues Duffau

the central region: comparison with intraoperative stimulation in patients

with brain tumors. J Neurosurg 2000; 92: 589-98.
[523] Disbrow EA, Slutsky DA, Roberts TPL, Krubitzer LA. Functional MRI at
1.5 tesla: a comparison of the blood oxygenation level-dependent signal and
electrophysiology. Proc Natl Acad Sci USA 2000; 97: 9718-23.
[524] Hill DLG, Castellano Smith AD, Simmons A, et al. Sources of error in
comparing functional magnetic resonance imaging and invasive
electrophysiological recordings. J Neurosurg 2000; 93: 214-23.
[525] Krings T, Schreckenberger M, Rohde V, et al. Metabolic and
electrophysiological validation of functional MRI. J Neurol Neurosurg
Psychiatry 2001; 71: 762-71.
[526] DeAngelis LM. Brain tumors. N Engl J Med 2001; 344: 114-23.
[527] Carpentier, Constable RT, Schlosser MJ, et al. Patterns of functional
magnetic resonance imaging activation in association with structural lesions
in the rolandic region: a classification system. J Neurosurg 2001; 94: 946-
54.
[528] Heiss WD, Thiel A, Kessler J, Herholz K. Disturbance and recovery of
language function: correlates in PET activation studies. NeuroImage 2003;
20 Suppl 1: S42-9.
[529] Seitz RJ, Huang Y, Knorr U, Tellmann L, Herzog H, Freund HJ. Large-
scale plasticity of the human motor cortex. Neuroreport 1995; 6: 742-4.
[530] Thiel A, Herholz K, Koyuncu A, et al. Plasticity of language networks in
patients with brain tumors: a positron emission tomography activation
study. Ann Neurol 2001; 50: 620-9.
[531] Baciu M, Le Bas JF, Segebarth C, Benabid AL. Presurgical fMRI
evaluation of cerebral reorganization and motor deficit in patients with
tumors and vascular malformations. Eur J Radiol 2003; 46: 139-46.
[532] Caramia MD, Telera S, Piattella MC, et al. Ipsilateral motor activation in
patients with cerebral gliomas. Neurology 1998; 51: 196-202.
[533] Holodny AI, Schulder M, Ybasco A, Liu WC. Translocation of Broca's area
to the contralateral hemisphere as the result of the growth of a left inferior
frontal glioma. J Comput Assist Tomogr 2002; 26: 941-3.
[534] Roux FE, Boulanouar K, Ibarrola D, Tremoulet M, Chollet F, Berry I.
Functional MRI and intraoperative brain mapping to evaluate brain
plasticity in patients with brain tumours and hemiparesis. J Neurol
Neurosurg Psychiatry 2000; 69: 453-63.
[535] Taniguchi M, Kato A, Ninomiya H, et al. Cerebral motor control in patients
with gliomas around the central sulcus studied with spatially filtered
 References 79

magnetoencephalography. J Neurol Neurosurg Psychiatry 2004; 75: 466-

71.
[536] Branco DM, Coelho TM, Branco BM, et al. Functional variability of the
human cortical motor map: electrical stimulation findings in perirolandic
epilepsy surgery. J Clin Neurophysiol 2003; 20: 17-25.
[537] Duffau H. Acute functional reorganisation of the human motor cortex
during resection of central lesions: a study using intraoperative brain
mapping. J Neurol Neurosurg Psychiatry 2001; 70: 506-13.
[538] Duffau H, Capelle L. Functional recuperation after resection of gliomas
infiltrating primary somatosensory fields. Study of intraoperative electric
stimulation. Neurochirurgie 2001; 47: 534-41.
[539] Duffau H, Sichez JP, Lehéricy S. Intraoperative unmasking of brain
redundant motor sites during resection of a precentral angioma: evidence
using direct cortical stimulation. Ann Neurol 2000; 47: 132-5.
[540] Duffau H. Recovery from complete hemiplegia following resection of a
retrocentral metastasis: the prognostic value of intraoperative cortical
stimulation. J Neurosurg 2001; 95: 1050-2.
[541] Kamada K, Sawamura Y, Takeuchi F, et al. Gradual recovery from dyslexia
and related serial magnetoencephalographic changes in the lexicosemantic
centers after resection of a mesial temporal astrocytomas. Case report. J
Neurosurg 2004; 100: 1101-6.
[542] Krainik A, Duffau H, Capelle L, et al. Role of the healthy hemisphere in
recovery after resection of the supplementary motor area. Neurology 2004;
62: 1323-32.
[543] Duffau H, Capelle L. Preferential brain locations of low-grade gliomas.
Cancer 2004; 100: 2622-6.
[544] Freund H. Supplementary Sensorimotor Area. Historical overview. Adv
Neurol 1996; 70: 17-27.
[545] Lim SH, Dinner DS, Pillay PK, et al. Functional anatomy of the
supplementary sensorimotor area: results of extraoperative electrical
stimulation. Electroencephalogr Clin Neurophysiol 1994; 91: 179-93.
[546] Picard N, Strick PL. Imaging the premotor areas. Curr Opin Neurobiol
2001; 11: 663-72.
[547] Bannur U, Rajshekhar V. Postoperative supplementary motor area
syndrome : clinical features and outcome. Br J Neurosurg 2000; 14: 204-10.
[548] Bleasel A, Comair Y, Lüders H. Surgical ablation of the mesial frontal lobe
in humans. Supplementary Sensorimotor Area. Lüders H. Philadelphia,
Lippincott-Raven: 1996; pp 217-35.
80 Hugues Duffau

[549] Fukaya C, Katayama Y, Kobayashi K, Kasai M, Oshima H, Yamamoto T.

Impairment of motor function after frontal lobe resection with preservation
of the primary motor cortex. Acta Neurochir Suppl 2003; 87: 71-4.
[550] Laplane D, Talairach J, Meininger V, Bancaud J, Orgogozo JM. Clinical
consequences of corticectomies involving the Supplementary Motor Area in
man. J Neurol Sci 1977; 34 : 301-14.
[551] Rostomily RC, Berger MS, Ojemann GA, Lettich E. Postoperative deficits
and functional recovery following removal of tumors involving the
dominant hemisphere supplementary motor area. J Neurosurg 1991; 75: 62-
8.
[552] Russell SM, Kelly PJ. Incidence and clinical evolution of postoperative
deficits after volumetric stereotactic resection of glial neoplasm involving
the supplementary motor area. Neurosurgery 2003; 52: 506-16.
[553] Yamane F, Muragaki Y, Maruyama T, et al. Preoperative mapping for
patients with supplementary motor area epilepsy: multimodality brain
mapping. Psychiatry Clin Neurosci 2004; 58: S16-21.
[554] Duffau H, Lopes M, Denvil D, Capelle L. Delayed onset of the
supplementary motor area syndrome after surgical resection of the mesial
frontal lobe: a time course study using intraoperative mapping in an awake
patient. Stereotact Funct Neurosurg 2001; 76: 74-82.
[555] Krainik A, Lehéricy S, Duffau H, et al. Role of the supplementary motor
area in motor deficit following medial frontal lobe surgery. Neurology 2001;
57: 871-8.
[556] Krainik A, Lehéricy S, Duffau H, et al. Postoperative speech disorder after
medial frontal surgery: role of the supplementary motor area. Neurology
2003; 60: 587-94.
[557] Fontaine D, Capelle L, Duffau H. Somatotopy of the supplementary motor
area: evidence from correlation of the extent of surgical resection with the
clinical patterns of deficit. Neurosurgery 2002; 50: 297-303.
[558] Augustine JR. Circuitery and functional aspects of the insular lobe in
primates including humans. Brain Research Reviews 1996; 22: 229-44.
[559] Ackermann H, Riecker A. The contribution of the insula to motor aspects of
speech production: a review and a hypothesis. Brain Lang 2004; 89: 320-8.
[560] Wise RJ, Greene J, Buchel C, Scott SK. Brain regions involved in
articulation. Lancet 1999; 353: 1057-61.
[561] Duffau H, Capelle L, Lopes M, Bitar A, Sichez JP, Van Effenterre R.
Medically intractable epilepsy from insular low-grade gliomas:
improvement after an extended lesionectomy. Acta Neurochir (Wien) 2002;
144: 563-73.
 References 81

[562] Duffau H, Fontaine D. Successful resection of a left insular cavernous

angioma using neuronavigation and intraoperative language mapping. Acta
Neurochir (Wien), in press
[563] Dronkers NF. A new brain region for coordinating speech articulation.
Nature 1996; 384: 159-61.
[564] Duffau H, Bauchet L, Lehericy S, Capelle L. Functional compensation of
the left dominant insula for language. Neuroreport 2001; 12: 2159-63.
[565] Duffau H, Karachi C, Gatignol P, Capelle L. Transient Foix-Chavany-Marie
syndrome following surgerical resection of a right insulo-opercular low-
grade glioma: case report. Neurosurgery 2003; 53: 426-31.
[566] LeRoux PD, Berger MS, Haglund MM, Pilcher WH, Ojemann GA.
Resection of intrinsic tumors from nondominant face motor cortex using
stimulation mapping: report of two cases. Surg Neurol 1991; 36: 44-8.
[567] Duffau H, Denvil D, Capelle L. Absence of movement disorders after
surgical resection of glioma invading the right striatum. J Neurosurg 2002;
97:3 63-9.
[568] Gil Robles S, Gatignol P, Capelle L, Mitchell MC, Duffau H. The role of
dominant striatum in language: a study using intraoperative electrical
stimulations. J Neurol Neurosurg Psychiatry 2005; 76: 940-6.
[569] Duffau H, Khalil I, Gatignol P, Denvil D, Capelle L. Surgical removal of
corpus callosum infiltrated by low-grade glioma: functional outcome and
oncological considerations. J Neurosurg 2004; 100: 431-7.
[570] Milea D, Lobel E, Lehéricy S, et al. Intraoperative frontal eye field
stimulation elicits ocular deviation and saccade suppression. Neuroreport
2002; 13: 1359-64.
[571] Blanke O, Seeck M. Direction of saccadic and smooth eye movements
induced by electrical stimulation of the human frontal eye field: effect of
orbital position. Exp Brain Res 2003; 150: 174-83.
[572] Lobel E, Kahane P, Leonards U, et al. Localization of human frontal eye
fields: anatomical and functional findings of functional magnetic resonance
imaging and intracerebral electrical stimulation. J Neurosurg 2001; 95: 804-
15.
[573] Duffau H, Denvil D, Lopes M, et al. Intraoperative mapping of the cortical
areas involved in multiplication and subtraction: an electrostimulation study
in a patient with a left parietal glioma. J Neurol Neurosurg Psychiatry 2002;
73: 733-8.
[574] Gatignol P, Capelle L, Le Bihan R, Duffau H. Double dissociation between
picture naming and comprehension: an electrostimulation study.
Neuroreport 2004; 15: 191-5.
82 Hugues Duffau

[575] Boatman D, Gordon B, Hart J, Selnes O, Miglioretti D, Lenz F.

Transcortical sensory aphasia: revisited and revised. Brain 2000; 123: 1634-
42.
[576] Roux FE, Boetto S, Sacko O, Chollet F, Tremoulet M. Writing, calculating,
and finger recognition in the region of the angular gyrus: a cortical
stimulation study of Gerstmann syndrome. J Neurosurg 2003; 99: 716-27.
[577] Roux FE, Lubrano V, Lauwers-Cances V, Tremoulet M, Mascott CR,
Demonet JF. Intra-operative mapping of cortical areas involved in reading
in mono- and bilingual patients. Brain 2004; 127: 1796-810.
[578] Lucas TH, McKhann GM, Ojemann GA. Functional separation of
languages in the bilingual brain: a comparison of electrical stimulation
language mapping in 25 bilingual patients and 117 monolingual control
patients. J Neurosurg 2004; 101: 449-57.
[579] Roux FE, Tremoulet M. Organization of language areas in bilingual
patients: a cortical stimulation study. J Neurosurg 2002; 97: 857-64.
[580] Duffau H, Capelle L. Incontinence after brain glioma surgery: new insights
into the cortical control of micturition and continence. J Neurosurg, in
press.
[581] Duffau H, Denvil D, Capelle L. Long term reshaping of language, sensory,
and motor maps after glioma resection: a new parameter to integrate in the
surgical strategy. J Neurol Neurosurg Psychiatry 2002; 72: 511-6.
[582] Duffau H, Lopes M, Arthuis F, et al. Contribution of intraoperative
electrical stimulations in surgery of low-grade gliomas: a comparative study
between two series without (1985-1996) and with (1996-2003) functional
mapping in the same institution. J Neurol Neurosurg Psychiatry 2005; 102:
148-51.
[583] Berger MS, Deliganis AV, Dobbins JD, Keles GE. The effect of extent of
resection on recurrence in patients with low grade cerebral hemisphere
gliomas. Cancer 1994; 74: 1784-91.
[584] Cukiert A, Gronich G, Marino Junior R. Surgical approaches to tumors and
epileptogenic zones close to Wernicke’s area. Arq Neuropsiquiatr 1995; 53:
587-91.
[585] Nikas DC, Bello L, Zamani AA, et al. Neurosurgical considerations in
supra-tentorial low-grade gliomas: experience with 175 patients. Neurosurg
Focus 1998; 4: 4.
[586] Apuzzo MLJ. Brain surgery. Complication avoidance and management.
Churchill Livingstone, New York, 1993, Vol 1, pp 379-90.
[587] Brell M, Ibanez J, Caral L, et al. Factors influencing surgical complications
of intra-axial brain tumours. Acta Neurochir (Wien) 2000; 142: 739-50.
 References 83

[588] Cabantog AM, Berstein M. Complications of first craniotomy for intra-axial

brain tumour. Can J Neurol Sci 1994; 21: 213-8.
[589] Cedzich C, Taniguchi M, Schäfer S, et al. Somatosensory evoked potential
phase reversal and direct motor cortex stimulation during surgery in and
around the central region. Technical application. Neurosurgery 1996; 38:
962-71.
[590] Fadul C, Wood J, Thaler H, et al. Morbidity and mortality of craniotomy for
excision of supratentorial gliomas. Neurology 1988; 38: 1374-9.
[591] Sawaya R, Hammoud M, Schoppa D, et al. Neurological outcomes in a
modern series of 400 craniotomies for treatment of parenchymal tumors.
Neurosurgery 1998; 42: 1044-56.
[592] Tandon P, Mahapatra AK, Khosla A. Operations on gliomas involving
speech centres. Acta Neurochir Suppl (Wien) 1993; 56: 67-71.
[593] Vives KP, Piepmeier JM. Complications and expected outcome of glioma
surgery. J Neurooncol 1999; 42: 289-302.
[594] Berger MS, Rostomily RC. Low grade gliomas: functional mapping
resection strategies, extent of resection, and outcome. J Neurooncol 1997;
34: 85-101.
[595] Capelle L, Duffau H, Lopes M, et al. Supra-tentorial hemispheric WHO
grade 2 gliomas in adults : a study of prognostic factors with special
emphasis on the role of surgery. J Neuro-oncol 2002; 4 (Suppl 1):S17, 69.
[596] Keles GE, Anderson B, Berger MS. The effect of extent of resection on
time to tumor progression and survival in patients with glioblastoma
multiforme of the cerebral hemisphere. Surg Neurol 1999; 52: 371-9.
[597] Keles GE, Lamborn KR, Berger MS. Low-grade hemispheric gliomas in
adults: a critical review of extent of resection as a factor influencing
outcome. J Neurosurg 2001; 95: 735-45.
[598] Lacroix M, Abi-Said D, Fourney DR, et al. A multivariate analysis of 416
patients with glioblastoma multiforme: prognosis, extent of resection, and
survival. J Neurosurg 2001; 95: 190-8.
[599] Laws ER, Shaffrey ME, Morris A, Anderson FA Jr. Surgical management
of intracranial gliomas: does radical resection improve outcome? Acta
Neurochir Suppl 2003; 85: 47-53.
[600] Lo SS, Cho KH, Hall WA, et al. Does the extent of surgery have an impact
on the survival of patients who receive postoperative radiation therapy for
supratentorial low-grade gliomas? Int J Cancer 2001; 96 Suppl: 71-8.
[601] Nakamura M, Konishi N, Tsunoda S, et al. Analysis of prognostic and
survival factors related to treatment of low-grade astrocytomas in adults.
Oncology 2000; 58: 108-16.
84 Hugues Duffau

[602] Nicolato A, Gerosa MA, Pina P, Iuzzolino P, Giorgiutti F, Bricolo A.

Prognostic factors in low-grade supratentorial astrocytomas: a uni-
multivariate statistical analysis in 76 surgically treated adult patients. Surg
Neurol 1995; 44: 208-21
[603] Peraud A, Ansari H, Bise K, Reulen HJ. Clinical outcome of supratentorial
astrocytoma WHO grade II. Acta Neurochir (Wien) 1998; 140: 1213-22.
[604] Rostomily RC, Keles GE, Berger MS. Radical surgery in the management
of low-grade and high-grade gliomas. Baillieres Clin Neurol 1996; 5: 345-
69.
[605] Scerrati M, Roselli R, Iacoangeli M, Pompucci A, Rossi GF. Prognostic
factors in low grade (WHO grade II) gliomas of the cerebral hemispheres:
the role of surgery. J Neurol Neurosurg Psychiatry. 1996; 61: 291-6.
[606] Schmidt MH, Berger MS, Lamborn KR, et al. Repeated operations for
infiltrative low-grade gliomas without intervening therapy. J Neurosurg
2003; 98: 1165-9.
[607] Logothetis NK, Wandell BA. Interpreting the BOLD signal. Annu Rev
Physiol 2004; 66: 735-69.
[608] Pellerin L, Magistretti PJ. Neuroenergetics: calling upon astrocytes to
satisfy hungry neurons. Neuroscientist 2004; 10: 53-62.
[609] Aubert A, Costalat R. A model of the coupling between brain electrical
activity, metabolism, and hemodynamics: application to the interpretation of
functional neuroimaging. Neuroimage 2002; 17: 1162-81.
[610] Horwitz B. The elusive concept of brain connectivity. Neuroimage 2003;
19: 466-70.
[611] Penny WD, WD, Stephan KE, Mechelli A, Friston KJ. Modelling functional
integration: a comparison of structural equation and dynamic causal models.
Neuroimage 2004; 23 Suppl 1: S264-74.
[612] Buonomano DV, Merzenich MM. Cortical plasticity: from synapses to
maps. Annu Rev Neurosci 1998; 21: 149-86.
[613] Taphoorn MJB, Klein M. Cognitive deficits in adult patients with brain
tumours. Lancet Neurol 2004; 3 : 159-68.
 INDEX

anatomy, 55, 61, 77, 79

# angiogenesis, 49
angiography, 16, 68
2D, 48
angioma, 50, 79, 81
animals, 9
A anisotropic, 15, 40, 59, 62
anisotropy, 13, 59
abnormalities, 6, 14, 59 antagonist, vii
abscess, 48, 49 anterior, 26, 27, 69
accuracy, vii, 18, 45, 54, 63 anti-angiogenic, 7, 49
acid, 5, 68 antigen, 41
action potential, 16 aphasia, 27, 82
activation, 11, 12, 25, 27, 51, 54, 55, 57, 77, application, 41, 47, 52, 56, 59, 69, 76, 83, 84
78 apraxia, 18
acute, 1, 24, 29 arrest, 18
Adams, 50 articulation, 27, 80, 81
adaptation, 1 assessment, vii, 13, 45, 47, 54, 55, 58, 59, 60,
ADC, 7 62, 68, 75
administration, 68 astrocyte, 34
adult, 39, 40, 45, 50, 51, 52, 84 astrocytes, 84
adults, 38, 39, 40, 69, 83 astrocytoma, 38, 39, 43, 74, 84
aid, 73, 74 Atlas, 52
akinesia, 26 attention, 47
alpha, 5, 42, 44 atypical, 12
alternative, 58 auditory cortex, 56
amino, 5 avoidance, 82
amino acid, 5 axonal, 59, 60
amnesia, 69
amplitude, 17
anaplastic transformation, 3, 4, 10, 33
86 Index

capacity, 1
B capsule, 15, 17, 18, 74
carbon, 43
basal ganglia, 74
carcinoma, 49
behavior, v, 3, 7
case study, 68
beta, 71
causal model, 84
bilateral, 11, 27
CBF, 10
bilingual, 67, 82
cell, 7, 41, 45
biochemical, 6, 47
cells, 7, 11
biological, v, 1, 3, 7, 33, 34, 39
central nervous system, 1, 3, 9, 33, 37, 43, 72
biological behavior, 1, 3, 7, 33
central nervous system (CNS), 1, 3, 9, 33, 37,
biological models, 34
43, 52, 72
biology, 4
cerebral blood flow, 10
biophysical, 53
cerebral blood volume (CBV), 7, 48, 53
biopsies, 5, 6, 41, 44, 45, 66
cerebral function, 35
biopsy, 4, 6, 15, 42, 43, 47, 66
cerebral hemisphere, 39, 82, 83, 84
blood, 7, 10, 11, 12, 16, 41, 48, 49, 53, 54, 55,
cerebral mapping, 4
60, 78
cerebrospinal fluid (CSF), 12, 14
blood flow, 10, 12, 16
chemical, 48
blood oxygenation level-dependent, 11, 53, 78
chemotherapy, 4, 5, 35, 41, 43
blood-brain barrier (BBB), 41
children, 17, 61, 69, 71, 72, 73
BOLD, 11, 12, 34, 53, 54, 55, 57, 84
chloride, 41
brachytherapy, 44
chromosome, 40
brain, v, vii, viii, 1, 3, 4, 5, 6, 7, 9, 10, 11, 12,
chronic, 31, 71
13, 14, 15, 16, 20, 21, 23, 24, 25, 27, 28,
chronically, 71
29, 31, 33, 34, 35, 37, 38, 39, 40, 41, 42,
classical, 1, 4, 17, 25, 26
43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53,
classification, 7, 40, 45, 78
54, 55, 56, 57, 58, 59, 60, 61, 62, 63, 64,
clinical, vii, 4, 5, 9, 10, 12, 20, 26, 39, 40, 46,
65, 66, 67, 68, 69, 70, 72, 73, 74, 76, 77,
49, 51, 52, 63, 68, 77, 79, 80
78, 79, 80, 81, 82, 83, 84
cluster of differentiation (CD), 55
brain abscess, 48
Co, 76
brain activity, 52, 56
cognition, 74
brain functions, 50
cognitive, 18, 24, 28
brain injury, 50
cognitive function, 18, 24, 28
brain tumor, vii, viii, 1, 3, 4, 5, 6, 7, 11, 12,
coil, 12
13, 23, 27, 31, 34, 35, 40, 41, 42, 44, 45,
communication, 57
46, 47, 48, 49, 52, 53, 54, 55, 56, 57, 59,
compensation, viii, 4, 10, 15, 19, 23, 25, 27,
60, 62, 64, 65, 66, 68, 69, 72, 76, 77, 78
28, 29, 33, 37, 64, 65, 81
brainstem, 43
complementary, 4, 7, 35
complications, 15, 18, 66, 82
C compounds, 5, 46
comprehension, 18, 76, 81
cancer, 40 computed tomography, 39, 42
Cancer, 38, 39, 40, 42, 43, 44, 46, 79, 82, 83 computer, 73
cancers, 37 concentration, 11, 53, 54
 Index 87

conception, 1, 9 dendritic cell (DC), 37, 38, 43, 51, 63, 73, 82
concordance, 21 density, 5, 7
conformational, 35 deoxyhemoglobin, 12, 54
Congress, iv detection, 19, 41, 42, 43, 55, 63, 68
connectivity, vii, viii, 14, 18, 31, 33, 34, 60, deviation, 59, 81
72, 75, 84 diagnosis, 4, 42, 44, 46
consumption, 11 diagnostic, 4, 43, 47, 65
contralateral, 25, 78 differential diagnosis, 4, 41, 44
contralateral hemisphere, 78 differentiation, 46
contrast agent, 42 diffusion, 7, 13, 15, 34, 48, 49, 58, 59, 60, 62
control, 15, 19, 29, 49, 73, 78, 82 diffusion tensor imaging (DTI), 13, 14, 59, 60
control group, 73 diffusion-weighted imaging (DWI), 7, 13, 48
controlled, 17 diffusivity, 7, 13
cooling, 16, 69 digital images, 15
corona, 17, 18 dipole, 69
corpus callosum, 3, 28, 81 discrimination, 6, 46, 48
correlation, 12, 44, 45, 48, 54, 55, 57, 62, 76, disorder, 80
77, 80 displacement, 14, 15, 51, 63
correlations, 9, 18, 20 dissociation, 81
cortex, 10, 12, 16, 18, 19, 25, 27, 37, 50, 51, distribution, 5, 16
52, 53, 54, 55, 56, 57, 60, 62, 67, 69, 70, DNA, 40
71, 72, 73, 74, 75, 76, 77, 78, 79, 80, 81, 83 dominance, 54, 58
cortical, vii, 9, 10, 15, 16, 17, 18, 19, 20, 24, dorsolateral prefrontal cortex, 19
32, 37, 50, 51, 52, 53, 54, 56, 57, 60, 61, DSC, 49
63, 67, 68, 69, 70, 71, 72, 73, 74, 75, 76, dyslexia, 79
77, 79, 81, 82
corticospinal, 60, 62
coupling, 11, 26, 34, 47, 54, 84 E
craniotomy, 13, 20, 63, 72, 73, 74, 83
E6, 61
CT, 14, 38
E7, 77
CT scan, 38
EEG, 10, 34
current limit, 16
efficacy, 10, 15, 40, 67
electric current, 12
D electrical, vii, viii, 12, 13, 16, 18, 20, 21, 27,
29, 31, 34, 50, 54, 55, 56, 57, 71, 72, 73,
data set, 47 75, 77, 79, 81, 82, 84
death, 50 electrodes, 18, 70, 71
decision making, 12, 15, 57, 66 electroencephalography, 12
decompression, 15 electromagnetic, 12
deficit, vii, viii, 1, 11, 13, 20, 23, 26, 29, 32, electronic, iv
78, 80 electrophysiological, 15, 16, 17, 18, 33, 73,
deficits, 17, 71, 80, 84 76, 78
deformation, 20, 63, 64 electrophysiology, 34, 74, 78
degree, 4 electrostatic, iv
delta, 12, 56 emission, 10, 41, 42, 43, 44
88 Index

emitters, 4
energy, 6, 45, 54
G
environment, 62, 64
ganglia, 74
epilepsy, 17, 70, 71, 72, 79, 80
gene, 4, 41
event-related desynchronization, 71
gene expression, 4
evidence, 11, 79, 80
gene therapy, 4
evoked potential, 16, 17, 18, 57, 69, 70, 72,
general anesthesia, 18, 70, 73
77, 83
generation, 76
evolution, 3, 35, 54, 73, 80
genetics, 37
examinations, 35
Germany, 49
excision, 72, 83
glatiramer acetate (GA), 69, 72, 74, 75, 80,
excitability, 24
81, 82
expert, iv
glial, 39, 45, 48, 80
extracranial, 12
glioblastoma, 43, 49, 54, 68, 83
eye, 29, 81
glioblastoma multiforme, 49, 54, 68, 83
eye movement, 81
glioma, 3, 4, 6, 11, 15, 16, 19, 24, 25, 27, 28,
eye movements, 81
29, 33, 35, 38, 39, 40, 41, 42, 43, 44, 45,
46, 47, 49, 51, 52, 68, 74, 75, 78, 81, 82, 83
F gliomas, 3, 4, 5, 6, 7, 10, 14, 15, 17, 23, 25,
26, 27, 28, 38, 40, 41, 42, 43, 44, 46, 47,
facial palsy, 28 48, 49, 52, 54, 59, 60, 66, 68, 72, 73, 74,
factor i, 43, 44, 83 75, 78, 79, 82, 83, 84
false, 12, 54 gliosis, 6
family, 26, 35 glucose, 5, 16, 43
FDG, 5, 34, 42, 43, 44, 51 glucose metabolism, 16
fiber, 14, 58, 59, 60 goals, vii
fibers, 13, 14, 16, 17, 60 gold, 16
flow, 68 grading, 7, 42, 44, 46, 49
fluid, 12, 14 gravity, 14
fluorescence, 68 gray matter, 12
fluorine, 43 grey matter, 13, 50
fMRI, vii, 10, 11, 12, 14, 20, 25, 26, 27, 34, grids, vii, 17, 18, 71
52, 53, 56, 57, 61, 76, 78 groups, 17
follow-up, 34, 42, 65 growth, 1, 3, 4, 10, 29, 33, 35, 38, 40, 78
fractional anisotropy, 13, 59 guidance, 5, 12, 29, 61, 63, 64, 65, 66, 67
frontal lobe, 53, 79, 80 gyrus, 24, 27, 29, 73, 82
functional architecture, 48
functional aspects, 80
functional imaging, 37, 57, 75
H
functional magnetic resonance imaging
head, 14, 24, 28, 56, 57, 69
(MRI), 10, 15, 51, 52, 53, 54, 57, 58, 61,
head injury, 24
62, 67, 76, 77, 78, 81
hemiparesis, 78
fusion, 64
hemiplegia, 15, 49, 79
 Index 89

hemisphere, 3, 12, 13, 24, 26, 27, 28, 73, 78, inflammation, 6
79, 80, 82, 83 infrared, 68
hemodynamic, 34 injection, 15, 44
hemodynamics, 54, 84 injury, iv, 1, 24, 50
hemoglobin, 11, 12, 53 inositol, 46
herpes, 42 integration, 6, 14, 15, 31, 61, 62, 76, 84
herpes simplex, 42 integrity, 13
herpes simplex virus type 1, 42 intensity, 48
heterogeneity, 4 interaction, 35
heterogeneous, 5 interactions, v, vii, viii, 1, 2, 4, 23, 33, 35
high grade glioma, 3, 6, 7 interface, 26, 34
high risk, 14, 27 interleukin (IL), 37
hippocampal, 69 International Agency for Research on Cancer,
hippocampus, 69 37
histological, 3, 14, 48, 68 interpretation, 17, 34, 54, 64, 84
histology, 5, 44 interstitial, 7, 64
histopathology, 46, 47 intracerebral, 52, 54, 55, 81
homogeneity, 34 intracranial, 41, 49, 65, 69, 71, 73, 77, 83
host, vii, 1, 35 intracranial tumors, 77
human, 10, 37, 40, 44, 45, 46, 48, 50, 55, 59, intraoperative, vii, 13, 14, 15, 16, 17, 18, 20,
60, 67, 68, 69, 70, 71, 72, 78, 79, 81 21, 24, 27, 28, 29, 31, 33, 34, 50, 51, 52,
human brain, 45, 46, 48, 50, 55, 59, 60 53, 55, 60, 61, 62, 63, 64, 65, 66, 67, 68,
human cerebral cortex, 37, 67, 69 69, 70, 72, 74, 75, 76, 77, 78, 79, 80, 81, 82
humans, 9, 50, 55, 60, 71, 79, 80 intravenous (IV), 23
hybrid, 47 intrinsic, 15, 24, 55, 67, 72, 81
hypothesis, 9, 37, 80 invasive, vii, 16, 20, 31, 44, 45, 60, 64, 66, 72,
76, 78
iodine, 42
I ipsilateral, 24, 56
irradiation, 62
identification, 6, 13, 16, 17, 21, 52, 53, 61, 72,
74, 76
images, 6, 11, 14, 44, 47, 60 J
imaging, vii, 4, 7, 10, 12, 13, 14, 15, 20, 21,
23, 25, 37, 40, 41, 42, 45, 46, 47, 48, 49, JI, 56, 58, 60, 77
51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, JT, 76
62, 63, 64, 65, 66, 67, 68, 75, 76, 77
immunohistochemical, 6
implementation, 61, 64, 65 K
in vitro, 9, 46
KH, 48, 52, 57, 83
in vivo, 42, 44, 45, 46, 59, 63
Ki-67, 46
inactivation, 16, 69
King, 70
indication, viii, 23
induction, 12, 27
infectious, 18
inferior frontal gyrus, 19, 27
90 Index

magnetic, iv, 12, 43, 44, 45, 46, 47, 48, 49,
L 51, 52, 53, 55, 56, 57, 58, 59, 60, 62, 64,
65, 66, 67, 76, 77
labeling, 46
magnetic field, 12, 56
Langerhans cells (LC), 43
magnetic resonance, 43, 44, 45, 46, 47, 48, 49,
language, 10, 11, 12, 15, 17, 18, 19, 20, 24,
51, 52, 53, 55, 58, 59, 60, 62, 64, 65, 66,
26, 27, 28, 29, 35, 37, 51, 52, 53, 54, 56,
67, 76
58, 60, 61, 67, 71, 72, 73, 74, 75, 76, 77,
magnetic resonance image, 58, 60, 65
78, 81, 82
magnetic resonance imaging (MRI), 6, 7, 10,
latency, 17, 69
15, 19, 25, 26, 34, 35, 43, 47, 48, 49, 51,
laterality, 58
52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62,
lead, 13, 14, 19, 29
64, 65, 66, 67, 76, 77, 78, 81
leakage, 14
magnetic resonance spectroscopy (MRS), 5, 6,
learning, 1, 9, 37
34, 45, 46, 47
lesion, vii, viii, 1, 3, 5, 6, 9, 10, 12, 13, 16, 17,
magnetoencephalography, 10, 12, 52, 55, 57,
18, 24, 25, 27, 33, 54, 61, 71
58, 61, 62, 77, 79
lesions, 1, 5, 6, 7, 9, 14, 17, 23, 24, 26, 43, 44,
magnetometry, 58
45, 48, 49, 51, 52, 54, 55, 56, 57, 58, 60,
magnets, 15
61, 62, 63, 69, 72, 73, 74, 78, 79
malignant, 5, 38, 41, 43, 46, 47, 68, 73
limitation, 20, 23, 52
management, 5, 13, 38, 39, 43, 52, 69, 74, 82,
limitations, 17, 67
83, 84
linear, 59
manganese, 60
lipid, 46
mapping, vii, viii, 1, 4, 9, 10, 11, 12, 13, 14,
lipids, 6, 46
15, 16, 17, 18, 19, 20, 21, 24, 26, 29, 31,
literature, 4, 9, 32, 69
32, 33, 34, 49, 51, 52, 53, 55, 56, 57, 59,
lobectomy, 69
60, 61, 62, 67, 69, 70, 71, 72, 73, 74, 75,
local anesthesia, 18, 72, 73
76, 77, 78, 79, 80, 81, 82, 83
local anesthetic, 74
mask, 72
localization, 15, 16, 17, 51, 52, 53, 55, 56, 57,
mathematical, 15, 40
69, 70, 72, 74, 76
MDR, 41
location, vii, 10, 16, 17, 28, 51
mean, 3, 7, 13, 31, 38
long-distance, 18
measurement, 14, 48, 54, 63
longitudinal study, viii
measures, 13
long-term, viii, 1, 9, 29
mechanical, iv, 17
low-grade glioma, 1, 3, 5, 6, 7, 11, 28, 32, 37,
median, 3, 16, 69
38, 40, 43, 44, 45, 46, 66, 74, 75, 79, 80,
medulloblastomas, 7
81, 82, 83, 84
MEG, vii, 10, 12, 14, 20, 34, 56, 57, 62, 77
lymphoma, 7, 49
melanoma, 49
lymphomas, 7
memory, 1, 15, 17, 18, 69
MET, 5
M metabolic, 4, 5, 6, 11, 13, 15, 20, 31, 33, 43,
44, 62
magnet, 65, 66 metabolic changes, 5, 6
metabolism, 6, 7, 16, 34, 45, 47, 54, 84
metabolite, 6
 Index 91

metabolites, 45, 47 natural, 1, 3, 32, 34, 35, 39

metastases, 49 natural killer cell (NK), 84
metastasis, 6, 7, 14, 46, 79 nausea, 73
metastatic, 59 near-infrared optical imaging, 54
metastatic brain tumor, 59 near-infrared spectroscopy, 12, 15, 54, 55, 68
methionine, 5, 43, 44 necrosis, 4, 5, 6, 43, 47
microscope, 68 neocortex, 26
microscopy, 68 neoplasm, 60, 80
microvascular, 16, 48 neoplasms, 1, 4, 39, 48, 52, 55, 72
migration, 38 neoplastic, 6, 7, 45
MLC, 39 nerve, 16, 69
modalities, 13 nervous system, 1, 3, 9, 10, 33, 37, 43, 72
modality, 57 Netherlands, 37
modeling, 40, 64 network, 10, 24
models, 15, 59 neurofunctional imaging methods, 13
molecular biology, 4 neurogenesis, 10
molecules, 13 neuroimaging, vii, viii, 4, 12, 13, 14, 16, 20,
monkeys, 49 21, 24, 26, 33, 34, 64, 84
morbidity, 75 neuroimaging techniques, vii, 12
morphological, 10 neurological deficit, 1, 9, 11, 23, 25, 28
mortality, 83 neuronal cells, 11
motion, 7 neurons, 5, 84
motor area, 25, 26, 29, 51, 52, 53, 70, 73, 79, neurosurgeon, vii, 23, 27, 29, 33
80 neurosurgeons, 18, 25
motor control, 78 neurosurgery, 51, 54, 61, 62, 63, 64, 65, 66,
motor function, 16, 18, 20, 53, 71, 80 67
motor stimulation, 74 neurosurgical, viii, 5, 13, 47, 51, 52, 53, 56,
motor system, 17, 51, 53, 60, 62 58, 61, 64, 65, 67, 69, 70, 77
motor task, 11, 25 neurovascular, 11, 54
movement, 11, 15, 26, 28, 81 New York, iii, iv, 82
movement disorders, 28, 81 NIRS, 12, 15
multidimensional, 63 NMR, 44, 45, 46, 53, 58, 59
multiple sclerosis (MS), 6, 54, 55, 56, 57, 60, non-invasive, vii, 6, 10, 12, 13, 20, 31, 33
63, 68, 69, 72, 74, 75, 77, 80, 81, 82, 83, 84 norepinephrine (NE), 71
multiplication, 81 normal, 13, 31, 37, 59
multivariate, 39, 83, 84 nuclear, 41, 45
muscle, 16 nuclear magnetic resonance, 45
muscles, 17 nucleus, 28
mutant, 42
myo-inositol, 46
O

N observations, 9
occipital, 70
NAA, 5 occipital lobe, 70
naming, 18, 81 ocular, 81
92 Index

oligodendroglioma, 38, 39 phenotypic, 10

Oncogene, 40 Philadelphia, 69, 73, 79
oncological, 31, 33, 35, 81 phonological, 18
oncology, 74 photographs, 19, 20
Oncology, 38, 83 photon, 41, 42
oncolytic, 42 phylogenesis, 9
on-line, vii, 18, 19 physiological, vii, 1, 9
optic, 60 physiology, 10, 20
optical, 12, 15, 54, 55, 67, 68 pilot study, 5, 43
optical imaging, 12, 15, 54, 67, 68 planar, 48
organization, v, vii, 1, 2, 9, 14, 18, 33, 35, 37 planning, vii, 6, 12, 13, 14, 21, 23, 26, 27, 29,
orientation, 59 31, 35, 47, 51, 52, 53, 55, 57, 58, 61, 62
oxidative, 16 plastic, vii, viii, 1, 2, 9, 33, 35, 51
oxygen, 11, 12, 16, 54, 60 plasticity, vii, viii, 1, 9, 23, 24, 25, 29, 31, 33,
oxygen consumption, 11 34, 35, 37, 50, 78, 84
oxygen saturation, 16 play, 27
oxygenation, 12, 54, 55 poor, 5
oxyhemoglobin, 54 porphyrins, 68
positron, 4, 10, 42, 43, 44, 51, 52, 76, 78
positron emission tomography (PET), vii, 5, 7,
P 10, 14, 20, 34, 42, 43, 44, 47, 51, 52, 60,
76, 78
parameter, 3, 82
postoperative, vii, viii, 1, 4, 11, 15, 17, 20, 23,
parenchyma, 14
24, 26, 27, 28, 31, 32, 33, 38, 42, 80, 83
parenchymal, 83
powers, 12
parenchymal tumors, 83
prediction, 40
parietal lobe, 53
predictive model, 34
Paris, 50
predictors, 40
pathology, 10
prefrontal cortex, 19
pathophysiological, 9, 34, 54
premotor cortex, 19, 25, 27, 75
pathophysiological mechanisms, 9
preoperative, 7, 10, 11, 12, 13, 20, 23, 24, 26,
pathophysiology, viii, 4
27, 31, 51, 52, 54, 61, 62, 64, 75
pathways, vii, 3, 13, 14, 16, 17, 18, 19, 27, 28,
preparation, iv
59, 60, 62, 74, 75
pressure, 64
patients, viii, 1, 4, 10, 12, 13, 17, 18, 20, 23,
primary brain tumor, 37
24, 25, 26, 27, 29, 31, 34, 38, 39, 40, 41,
primary brain tumors, 37
42, 43, 44, 45, 46, 48, 51, 52, 53, 54, 55,
primates, 80
56, 57, 58, 60, 61, 65, 66, 68, 69, 70, 71,
probe, 16
72, 74, 75, 76, 77, 78, 80, 82, 83, 84
procedures, 5, 14, 15, 18, 64, 65, 66, 70
pediatric, 52
production, 80
performance, 20, 50
prognosis, 4, 5, 35, 38, 41, 43, 68, 83
perfusion, 7, 11, 46, 48, 49, 67
prognostic, 3, 4, 5, 16, 24, 38, 39, 40, 41, 43,
peripheral nerve, 16
44, 79, 83
permeability, 48, 49
prognostic factors, 3, 38, 39, 40, 83
PET scan, 5, 34, 44, 51
prognostic value, 24, 79
ph, 41, 42
 Index 93

progression, 6 relationships, vii, 14

progressive, 1, 23 relevance, 41
proliferation, 4, 42 reliability, vii, 4, 7, 16, 17, 34, 58, 69, 76
property, iv remodelling, 9
propofol, 72 renal, 49
proteome, 40 replicability, 77
protocol, 53, 77 replication, 42
pseudo, 54 research, 1, 4
pulse, 12 resection, vii, viii, 5, 6, 11, 13, 14, 15, 16, 17,
pyramidal, 15, 16, 17, 28, 59, 60, 62 18, 19, 23, 24, 25, 26, 27, 28, 29, 32, 33,
35, 37, 45, 50, 52, 60, 61, 62, 63, 64, 66,
67, 68, 69, 71, 72, 73, 74, 75, 79, 80, 81,
Q 82, 83
resolution, 6, 15, 46, 54, 61
quality of life, 28, 33, 35, 39
response, 4, 5, 6, 7, 11, 18, 35, 41, 43, 49
risk, vii, viii, 1, 2, 4, 10, 14, 16, 17, 18, 20, 27,
R 32, 33, 35, 57, 69
risk factor, 4
radiation, 4, 5, 6, 7, 14, 39, 40, 41, 43, 47, 49, risk factors, 4
83 risk profile, 57
radiation damage, 6 ROI, 42
radiation therapy, 4, 6, 39, 41, 47, 49, 83
radical, 83
S
radioactive tracer, 4
radiological, 4
safety, 70
radiotherapy, 6, 35, 38
sampling, 42
rain, 52
Sartorius, 76
Raman, 47
scalp, 69
range, 6
Schmid, 72, 73, 77
reading, 18, 29, 82
sclerosis, 6
real-time, 15, 47
sedation, 72
recognition, 82
seeds, 44
reconstruction, 20, 56
segmentation, 47
recovery, 1, 9, 23, 24, 25, 26, 37, 49, 50, 51,
seizure, 17, 71
78, 79, 80
seizures, 23, 31, 71
recurrence, 4, 5, 6, 29, 43, 82
semantic, 18, 75
redistribution, viii, 1, 23, 24
sensation, 74
reduction, 5, 6, 17
sensitivity, 6, 7, 11, 16, 20, 21, 34, 54
redundancy, 24
sensorimotor cortex, 10, 51, 53, 57, 69, 70,
regional, 18, 20, 24, 52, 53
71, 72, 77
Registry, 37
sensory cortices, 54
regression, 45
separation, 82
regular, 9
sequelae, vii, 23, 27, 29, 31, 32, 33, 35
rehabilitation, viii, 26
series, 31, 32, 34, 43, 75, 82, 83
relationship, 4, 41
services, iv
94 Index

severity, 26 66, 68, 69, 70, 72, 73, 74, 75, 77, 79, 80,
short-term, vii, 50 82, 83, 84
sign, 17 surgical, vii, viii, 1, 3, 4, 10, 11, 13, 14, 15,
signals, 55, 67 18, 21, 23, 24, 25, 27, 29, 31, 32, 33, 34,
signs, 17 37, 52, 61, 64, 66, 68, 74, 75, 80, 81, 82
simulation, 13, 58 surgical resection, 11, 24, 29, 37, 75, 80, 81
simulations, 40 survival, 3, 4, 5, 6, 38, 39, 40, 41, 42, 44, 46,
sites, vii, 19, 20, 24, 28, 29, 50, 60, 74, 79 83
skin, 12 susceptibility, 49, 53
slow-growing glioma, 4 symptom, 4
SMA, 11, 25, 26 symptoms, 27
sodium, 68 synapses, 84
solution, 53 synaptic plasticity, 50
solutions, 42 synchronization, 18, 71
somatosensory, 16, 17, 18, 24, 29, 51, 56, 67, syndrome, 11, 25, 26, 27, 79, 80, 81, 82
69, 70, 76, 77, 79 synthetic, 58
somatosensory function, 18, 76 systematic, 28
spatial, 5, 6, 10, 13, 14, 15, 57, 61, 67 systems, 6, 67
spatial analysis, 57
specialists, 35
specificity, 11, 21, 34, 41, 67 T
SPECT, 4, 41, 42, 43
tactile, 52
spectra, 45, 46
technetium, 41
spectral analysis, 17, 71
technological, 66
spectroscopy, 5, 45, 46, 47, 48, 68
technology, 55, 63
speech, 18, 27, 37, 58, 73, 75, 80, 81, 83
temporal, 27, 29, 34, 55, 56, 58, 67, 69, 71,
spin, 58
74, 77, 79
statistical analysis, 39, 84
temporal lobe, 56, 69, 74, 77
strategies, 53, 59, 72, 83
Tesla, 66, 67
strength, 15, 65, 67
thallium, 41, 42
striatum, 28, 81
therapeutic, 35, 40
stroke, 1, 6, 10, 27, 37, 50, 51
therapy, 4, 5, 6, 7, 39, 40, 41, 47, 49, 65, 83,
subcortical structures, 9, 16, 28
84
subcutaneous (SC), 48, 60
thermal, 16, 69
subjective, 35
theta, 12
substitution, 10
three-dimensional (3D), 15, 20, 45, 47, 60, 62,
substrates, 5
63, 64, 76
subtraction, 81
thresholds, 20
Sun, 41, 64
time, 1, 2, 3, 4, 5, 15, 17, 20, 26, 29, 54, 80,
superconducting, 55
83
suppression, 81
time consuming, 15
surgeries, 32, 35
timing, 40
surgery, iii, vii, viii, 1, 2, 6, 10, 12, 13, 14, 15,
tissue, 7, 11, 15, 20, 46, 63, 68
16, 17, 18, 20, 21, 23, 26, 27, 29, 31, 32,
tissue perfusion, 7
33, 34, 35, 38, 39, 55, 56, 61, 62, 64, 65,
tissues, 59
 Index 95

tolerance, 72
tracers, 4, 5
V
tracking, 13, 58, 59, 60
validation, 47, 56, 76, 78
tractography, 58, 62
validity, 77
training, 50
values, 7
transcranial magnetic stimulation, 57
variability, vii, 1, 29, 37, 79
transformation, 3, 4, 6, 10, 33
variables, 39
transgene, 42
vascular, 34, 51, 68, 70, 78
treatment, 3, 6, 12, 32, 35, 38, 42, 56, 62, 83
video, 16, 68
trial, 38, 74
virus, 42
tumo(u)r, v, vii, viii, 1, 3, 4, 5, 6, 7, 10, 11,
visible, 14
12, 13, 15, 16, 19, 20, 23, 27, 29, 31, 32,
vision, 3, 9
33, 34, 35, 38, 41, 42, 43, 46, 47, 48, 49,
visual, 10, 12, 18, 42, 52, 54, 56, 75
51, 52, 54, 55, 56, 59, 60, 62, 64, 66, 67,
visualization, 62
68, 69, 72, 73, 75, 77, 83
vomiting, 73
tumor cells, 6
tumor mapping, 4
tumor progression, 6, 83 W
tumor proliferation, 4
tumo(u)rs, vii, viii, 1, 3, 4, 5, 6, 7, 12, 14, 16, water, 7, 10, 13, 34, 52, 59
17, 18, 26, 31, 32, 34, 35, 37, 40, 41, 42, water diffusion, 13, 59
43, 44, 45, 46, 47, 48, 49, 51, 52, 53, 54, weakness, 52
56, 57, 59, 60, 63, 65, 66, 68, 69, 70, 72, white matter, 3, 13, 17, 18, 59, 60, 74, 75
74, 76, 77, 78, 80, 81, 82, 83, 84 World Health Organization (WHO), 3, 40, 49,
turnover, 5 73, 83, 84
tyrosine, 4, 5, 42, 44 writing, 18, 29

U X
ultrasonography, 63 xenograft, 49
ultrasound, 15, 63, 64
United States, 37
unmasking, 10, 24, 29, 50, 79 Y
updating, 64
yield, 43, 47, 66