Table Of ContentN ew Trends and
Advanced Techniques in
Clinical Neurophysiology
EDITED BY
PAOLO M. ROSSINI
Associate Professor of Clinical Neurophysiology,
Second University of Rome 'Tor Vergata/ Rome (Italy)
and
FRANgOIS MAUGUIERE
Professor of Neurology, Claude Bernard University, Lyon (France)
ELECTROENCEPHALOGRAPHY AND CLINICAL NEUROPHYSIOLOGY
SUPPLEMENT NO. 41
1990
ELSEVIER
AMSTERDAM · NEW YORK · OXFORD
Electroenceph. din. Neurophysiol., 1990, Suppl. 41
© 1990, ELSEVIER SCIENCE PUBLISHERS B.V. (BIOMEDICAL DIVISION)
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Library of Congress Cataloglng-ln-PublIcatlon Data
Advanced evoked potentials and related techniques In clinical
neurophysiology / edited by Paolo M. Rossini and Frangols Mauguiere.
p. cm. — (Electroencephalography and clinical
neurophysiology. Supplement ; no. 41)
Includes bibliographical references.
Includes Index.
ISBN 0-444-Č1352-7
1. Evoked potentials (Elecirophyslology)—Diagnostic use.
I. Rossini, Paolo M. II. Mauguiere, Franfols. III. Series.
[DNLM: 1. Evoked Potentials. 2. Neurophysiology—methods. WI
EL3251 no. 41 / WL 102 A2443]
RC386.6.E86A35 1990
616.8'047'547—dc20
DNLM/DLC
for Library of Congress 90-14150
CIP
Printed in The Netherlands
New Trends and Advanced Techniques in Clinical Neurophysiology (EEG Suppl. 41)
Editors: P.M. Rossini and F. Mauguiere
© 1990, Elsevier Science Publishers, B.V. (Biomedical Division)
Foreword
When the contributors to this volume met at the International Symposium on Evoked Potentials
and Related Techniques, held in Rome in May 1989, they converged onto the opinion that the
time had come to publish a book updating the reader with review articles on the newest
techniques of Clinical Neurophysiology and their diagnostic applications. The authors, whose
expertise in their field is outstanding, were entirely free to organise their chapter and to add as
much review and original material as they needed in order to cover their topic exhaustively. This
resulted in a volume of reasonable length, neither excessively heavy, to avoid discouraging the
naive readers, nor too light in substance, so as to hold the interest of the most experienced ones.
Clinical neurophysiologists will discover in this volume comprehensive reviews which could
not have been included in the Journal of EEG and Clinical Neurophysiology because of the
considerable and growing pressure for printing space; in that respect it corresponds to what a
Supplement Volume to the Journal of EEG and Clinical Neurophysiology should be.
The book was divided into sections to highlight the topics that have been the most actively
debated for the past two years in the Clinical Neurophysiology literature. Indeed there is no
doubt that new methods of signal processing, magneto-encephalography, brain stimulation,
reflexology, neuro-monitoring, as well as clinical neurophysiology of pain, spasticity, motor
and sensory deficits, movement disorders, cognition and language belong in this category.
There is no doubt either that the clinical utility of evoked potential studies in AIDS deserved
two review chapters in this book.
The editors are indebted to all the contributors for their efforts in transmitting their knowledge
of the treated topics and in also providing, where necessary, original unpublished data to more
clearly define and to complete their individual chapters. We hope that the readers will experience
the same pleasure as we did when editing the manuscripts.
Paolo M. Rossini
Frangois Mauguiere
New Trends and Advanced Techniques in Clinical Neurophysiology (EEG Suppl. 41)
Editors: P.M. Rossini and F. Mauguiere
© 1990, Elsevier Science Publishers, B.V. (Biomedical Division) Vll
List of Contributors
Abbruzzese, G., 145 Crisci, C, 292
Abbruzzese, M., 73 Cruccu, G., 140
Amabile, G., 216
Amassian, V.E., 134 D'Alessio, C, 216
Arendt, G., 370 Dall'Agata, D., 145
Deacon, D.L., 202
Balbi, P., 149 De Lean, J., 223
Baratto, F., 330 Desmedt, J.E., 22
Barzi, E., 172 Deuschl, G., 84
Bazzano, S., 183 Dillmann, U., 314
Begleiter, Ç., 177 Dolenc, V.V., 348
Berardelli, Á., 140 Dona, B., 330
Beretta, Ĺ., 172
Bemardi, G., 286 Edgar, M.A., 342
Bertrand, 0., 51 Eghbal, R., 314
Besser, R., 314 Elidan, J., 119
Bianchi, Á., 28 Elsing, C, 370
Bohorquez, J., 51
Boom, H.B.K., 34 Facco, E., 330
Bouchard, J.P., 223 Famarier, G., 355
Buettner, U.W., 309 Fattapposta, F., 216
Favale, E., 73, 145
Caekebeke, J.F.V., 168 Ferracci, F., 183
Campbell, K.B., 202 Forest, L., 236
Caramia, M.D., 286 Fomara, C, 28
Caruso, G., 149, 292 Foti, Á., 216
Cathala, H.P., 243 Freeman, S., 119
Cerutti, S., 28 Freund, H.-J., 370
Chiarenza, G.A., 172 Fulgente, Ô., 183
Cicinelli, P., 286
Comi, G., 28 Gäbet, J.Y., 223
Cracco, J.B., 134 García-Larrea, L., 102
Cracco, R.Q., 134 Ghilardi, M.F., 183
Girón, G.P., 330 Opsomer, R.J., 298
Guérit, J.M., 298 Ozaki, I., 22
Halonen, J.-P., 342 Pauletti, G., 140
Hari, R., 3 Pelosi, L., 149, 292
Hefter, Ç., 370 Penicaud, Á., 243
Hoemberg, V., 370 Pemier, J., 51
Perretti, Á., 292
Ibañez, V., 274 Peters, M.J., 34
Inghilleri, M., 140 Pierrot-Deseilligny, E., 264
Porjesz, B., 177
Jones, S.J., 342 Prestor, B., 348
Ptito, M., 236
Kimura, J., 13
Koehler, J., 314 Rang, M., 306
Kutas, M., 155 Ransford, A.O., 342
Reni, L., 73, 145
Laffont, F., 243 Rimpel, J., 306
Lafreniére, L., 236 Romani, G.L., 298
Lanzillo, B., 292 Rossini, P.M., 124, 286, 298
Laureau, E., 236 Rothwell, J.C, 251
Le Canuet, P., 243
Lehmann, H.J., 306 Sabouraud, P., 223
Leibner, Ĺ., 119 Sela, M., 119
Liberati, D., 28 Sohmer, H., 119, 323
Locatelli, Ô., 28 Somma-Mauvais, H., 355
Lopes da Silva, F.H., 34 Spekreijse, H.J., 34
Lucking, C.H., 84 Stanzione, P., 216
Ludwig, B., 314 Stok, C.J., 34
Suffield, J.B., 202
Maccabee, P.J., 134
Malatesta, G., 183 Tagliati, M., 216
Malessa, R., 306 Terwort, Á., 306
Manfredi, M., 140 Timmann, D., 309
Marciani, M.G., 216 Tomberg, C, 22
Mathieu, J., 223 Trivelli, G., 145
Mauguiere, F., 102, 223, 274
Meunier, S., 243 Vanasse, M., 223, 236
Meyer, S.T., 306 Van Cangh, P.J., 298
Morena, Ě., 145 Van Dijk, J.G., 168
Munari, Ě., 330 Van Petten, C, 155
Van Sweden, Â., 168
Nelles, H.-W., 370 Villa, Ě., 172
Nitzan, M., 119
Nobilio, D., 183 Yamada, Ô., 13
Noel, P., 22
Zarola, F., 286, 298
2gur, T., 348
Onofrj, M.C, 183
New Trends and Advanced Techniques in Clinical Neurophysiology (EEG Suppl. 41)
Editors: P.M. Rossini and F. Mauguiere
© 1990. Elsevier Science Publishers, B.V. (Biomedical Division)
Magnetic Evoked Fields of the Human Brain:
Basic Principles and Applications
RIITTA HARI
Low Temperature Laboratory, Helsinki University of Technology, SF-02150 Espoo (Finland)
Introduction the model, the electric potentials are dispersed and
smeared whereas the magnetic pattern is unchanged.
In magnetoencephalography, MEG (Williamson and Since the electric potential distributions are influenced
Kaufman 1981; Had and Lounasmaa 1989), weak by the location of the reference electrode, inteφreta-
magnetic fields, typically 100-1000 fT, are de tion of the patterns in terms of generators is difficult
tected non-invasively outside the head. The best- whereas no corresponding problem exists in the mag
quality recordings are carried out within magnetically netic recordings. Consequently, MEG has good spatial
shielded rooms, usually made of mu-metal and alu resolution; under favourable conditions the location of
minium. Superconducting SQUIDs, immersed within the equivalent dipole, best explaining the measured
liquid helium, are used as detectors of the magnetic magnetic field pattern, can be determined with a pre
field. cision of a few millimeters (Hari et al. 1988). The
Fig. 1 illustrates a typical experimental situation. physiological inteφretation of the single-dipole model
The subject is lying with his head supported by a is synchronous activation of a cortical layer with a di
vacuum cast and the dewar, containing the detectors, ameter of up to 2 cm.
is placed close to the head. All moving magnetic ma Only tangential dipoles produce magnetic field out
terials must be avoided near the subject. Otherwise side the sphere, whereas both tangential and radial cur
the situation resembles conventional EEG or evoked rents cause potentials on the surface. This means that
potential recordings, and the signal-to-noise ratios of MEG suits well for studies of fissural cortex. When
EEG and MEG are at present comparable. To lo the depth of the source increases, the magnetic sig
cate sources, signals must be recorded from 30 to 50 nals decrease relatively more rapidly in amplitude than
locations to determine the field pattern. Multichan the electric potentials. A source in the centre of the
nel instrumentation is rapidly improving, allowing the sphere does not cause any external magnetic field at
whole field pattern to be measured with a single shot all, whereas electric potentials can still be recorded on
(Kajola et al. 1989). the surface. Therefore, MEG should be considered a
To understand some important differences between tool to mainly study cortical activity.
EEG and MEG, let us consider a current dipole, i.e., This review illustrates applicability of MEG to stud
current condensed within a small area, in a conduct ies of auditory and somatosensory systems, with ex
ing sphere. Fig. 2 shows that there are important dif amples of results obtained by the neuromagnetism
ferences between the resulting EEG and MEG. The group at the Low Temperature Laboratory of Helsinki
electric and magnetic field patterns are rotated by University of Technology. At present, 30-40 labora
90° with respect to each other. When concentric elec tories all over the world are carrying out MEG mea
tric inhomogeneities, simulating extracerebral tissues surements.
(cerebrospinal fluid, skull and scalp), are added to
Somatomotor system
preamplifiers
(1) Action fields
The probable sources of cerebral magnetic fields
are postsynaptic currents in synchronously activated
pyramidal neurones of fissural cortex. However, it
has become recently possible to also record magnetic
fields associated with compound action potentials of
human peripheral nerves (Wikswo et al. 1985; Eme et
al. 1988; Hari et al. 1989a).
SQUIDS within
niobium shields Fig. 3 shows non-invasively recorded compound
gradiometer action fields (CAEs) of one subject at cubita, about
coils
6 msec after median nerve stimulation at the wrist.
The response is at most locations monophasic, with
opposite polarities on the medial and lateral sides of
the nerve, and the onset and peak latencies increase
from distal to proximal channels.
channel
configuration Currents associated with an action potential can be
described with a current quadrupole consisting of 2
Fig. 1. Schematic illustration of a typical experimental situation opposite intracellular dipoles, one at the depolariza
for auditory measurements with a 7-channel 1st order SQUID
tion and the other at the repolarization front (Fig. 3).
gradiometer. The dewar, containing the flux transformers and
The polarities of our CAEs correspond to the direction
the SQUIDs, is placed close to the subject. Adapted from Hari
of the intracellular current flow at the leading front of
and Lounasmaa (1989).
the action potential volley, whereas the other phase,
if present, is very flat and lasts longer than the first.
It is probable that spatial asynchrony of AFs in fi
bres of different calibers leads to an asymmetry of the
quadrupole source and therefore to dominance of the
dipole term when the field is measured at a distance
(Stegeman and De Weerd 1982). Clear responses were
also detected at the brachial plexus, and conduction
velocities calculated from the magnetic signals were
in good agreement with the conventional surface elec
trode recordings. Since CAEs are less contaminated
by non-uniform resistivities of the volume conductor
than the corresponding CAEs, they can give more di
rect information about neural currents and might be
useful when response amplitudes are of importance.
(2) Responses from SI
The first cortical magnetic response, N20m, peaks
MAGNETIC FIELD ELECTRIC POTENTIAL
18-20 msec after median nerve stimulation (Fig. 4).
Fig. 2. Above: a current dipole produces a magnetic field with field The responses have opposite polarities at the upper
lines following the right hand rule. Below: magnetic field pattern and lower end of the rolandic fissure, suggesting a
over the sphere and electric potential distribution over the surface tangential current source at the primary somatosen
due to a current dipole in a 4-layer sphere model simulating the
sory hand area (Brodmann area 3b). N20m is rather
head. The patterns are rotated by 90° with respect to each other. The
insensitive to the stimulus repetition rate whereas the
continuous lines refer to magnetic flux oriented out of the sphere
next large deflection P30m, at 27-30 msec, increases
or to positive potential.
depolarization
Fig. 3. Compound action fields after electric stimulation of the right median nerve at the wrist. The measurements were made at 2 sites with
the 7-channel gradiometer. Passband is 0.05-2000 Hz and responses from 2 successive measurements are superimposed. Each trace is the
average of about 1000 responses. The insert on the left illustrates intracellular current flow in a nerve fibre during an action potential and the
associated magnetic field around the nerve; the asymmetry illustrates the fact that repolarization currents are distributed along a wider area
than the dense depolarization currents. The insert on the right shows (with a time scale from 2 to 27 msec) responses of the same subject
to median nerve stimulation at cubita, plexus, and somatosensory cortex. From Hari et al. (1989a).
clearly in amplitude when the repetition rate is de The sites of the equivalent dipoles, activated by
creased from 5 to 2 Hz (Tiihonen et al. 1989a). Ac stimulation of different parts of the body, correspond
tivity continues around SI for about 150 msec. to the somatotopic organization of SI. For lower limb
The responses in Fig. 4 also illustrate a deflection stimulation, the first response peaks at 40 msec with
at 22 msec, the probable magnetic counteφart of the a source at the mesial wall of the hemisphere. For
electric P22. P22 is assumed to be generated by radial cutaneous stimulation of fingers, the source is about
sources, which would not generate detectable mag 1 cm more lateral for the thumb than the little fin
netic ñelds outside a sphere. The detection of P22m ger (Hari and Kaukoranta 1985). The distributions of
indicates that even a slight tangential component of the early somatosensory evoked fields (SEFs) to ulnar
source currents can generate an extracranial magnetic and median nerve stimulation also follow the somato-
field, big enough to be measured with a low-noise topical order but during the late deflections, at about
instrument. P22m reversed polarity between the up 80 msec, no such differences are observed (Huttunen
per and lower measurement locations, but due to the et al. 1987). Interaction between afferent input is ev
small size of the response and its superimposition on ident from an experiment where rare (10%) median
the N20m-P30m slope, its precise source could not nerve stimuli were presented among frequently (90%)
be determined. repeated ulnar nerve stimuli (ISI 1 sec) or vice versa
second somatosensory area SII at the upper bank c
the sylvian fissure (Hari et al. 1984b; Kaukoranta et al.
1986). This area is activated by both lower and upper
limb stimuli, presented either contra- or ipsilaterally.
The main response at SII peaks about 100 msec after
cutaneous stimulation of the middle finger, and it
is significantly increased in amplitude if the site of
stimulation is infrequently and unpredictedly changed
from one finger to another (Hari et al. 1990). In this
200 fT
respect SII differs clearly from SI.
(4) Noxious stimulation
Selective activation of pain afferents evokes strong
magnetic signals. After electric stimulation of the
frontal incisor, the response peaks at about 90 msec
with an equivalent source in the frontal operculum
(Hari et al. 1983b). After carbon dioxide stimulation
of the nasal mucosa, a long-latency response is seen
at 350 msec with the source near SII (Huttunen et
al. 1986), clearly posterior to the source activated by
Fig. 4. Magnetic fields at the upper and lower ends of the right dental stimulation.
central sulcus after median nerve stimulation at the wrist. The
interStimulus interval was 200-220 msec, passband 0.05-2000 Hz, (5) Premovement activity
and the sampling frequency 8 kHz. The traces are averages of
In monkey motor cortex, preparation for a voluntary
about 1000 responses. The first cortical deflection at 19 msec is
movement is associated with neural activity several
specified, the following deflection of opposite polarity peaks at 30
msec. Modified from Tiihonen et al. (1989a). hundred milliseconds before the movement. In hu
mans, slow EEG shifts precede voluntary movements.
(Huttunen et al. 1987). The response wave forms and It is also possible to record magnetic shifts resem
amplitudes were similar independently whether the bling in moφhology the electric 'readiness' poten
stimulus was standard or deviant, indicating that there tials. Fig. 5 shows that magnetic shifts preceding self-
is strong interaction between the afferent input from paced plantar flexions of the right foot start even 1
both nerves. sec before muscular activity (Hari et al. 1983a). The
The somatosensory cortex also seems to have an idle recording, made along the line connecting the ampli
rhythm comparable to the alpha activity of the visual tude extrema, shows polarity reversal in the middle,
cortex. This rhythm consists of about 10 Hz and 21.5 over the motor representation area of the ankle. Simi
Hz activity with a source area close to the source larly, MEG shifts preceding finger extensions reverse
of N20m for median nerve stimulation (Tiihonen et in polarity between the upper and lower ends of the
al. 1989b). The high-frequency rhythm resembles the rolandic fissure suggesting a source in the hand rep
electric mu rhythm in reactivity: it is blocked by resentation area.
clenching the fist, but not by opening the eyes. That
the mu rhythm seems to be mainly generated at the SI
hand area may be explained by the fact that the hand Auditory system
(especially the thumb) occupies a relatively large area
in the somatosensory homunculus, in accordance with (I) General
its importance to human behaviour. Due to the anatomical location of the auditory cortex,
the electric activity is best recorded in the midline
(3) Responses from SI I of the scalp. It is thus very difficult to differentiate
It is also possible to detect MEG responses from the between responses of each hemisphere, unless source
peaks at 19 msec with an equivalent source deep
within the sylvian fissure, probably at the primary
auditory cortex (Scherg et al. 1989). The activity in
the supratemporal cortex continues for a few hundred
O.SpT
milliseconds, with slightly varying source areas.
(2) Steady-state responses
When the interstimulus interval is shortened below
about 200 msec, 'steady-state responses' are formed.
If the system under study is non-linear, steady-state
and transient responses give complementary informa
tion. The best known steady-state response is the 40
Hz response, first described by Galambos et al. (1981)
in the electric recordings. This potential was largest
in amplitude for stimulus rates of 40 Hz. The mag
netic 40 Hz response has been detected to trains of
clicks and to continuous presentation of clicks and
noise bursts (Mäkelä and Hari 1987; Hari et al. 1989b;
Tiihonen et al. 1989c). The field patterns indicate a
10 "^^^^^ ^ source at the supratemporal auditory cortex, 20-35
mm beneath the scalp. This source explains the major
part of the electric potential on the scalp suggesting
that the electric response achieves its major contribu
tion from cortical currents.
Two explanations can be presented for the ampli
tude enhancement around 40 Hz (see Fig. 6). First,
Fig. 5. Magnetic fields preceding self-paced plantar flexions of the
right foot. The recordings were made along a line connecting the
field extrema of the slow shift. The vertical bars on the right hand
side of the curves indicate the average standards errors of the mean
for each curve. The schematic figure shows a simple current dipole
model for the measured field. Adapted from Hari et al. (1983a).
The vertical lines indicate the onset of the movement.
modelling is used (Scherg 1990). The special advan
tage of MEG in the study of the auditory system is that
,¡1
activity of both hemispheres can be detected selec 40.1 50 fT
tively. Neuromagnetic studies of the auditory cortices in
1 1
have demonstrated in humans some functional fea 0 20 40 60 0 25 50 75 100
tures, earlier observed only in animals, and have also Repetition rate (Hz) Time (nis)
given information about new functional principles. Fig. 6. Left: mean (± S.E.M.; 10 subjects) amplitudes of the steady-
Further, recordings of both electrically evoked poten state responses to clicks as a function of stimulus repetition rate.
Right: responses of 1 subject to clicks presented at 10.1, 20.1, and
tials and magnetic fields under identical conditions
40.1 Hz. The recordings are from the posterior field extremum over
have been important in identifying neural sources of
the right hemisphere. The passband is 0.05-250 Hz, and 1500-1800
auditory evoked responses (for a recent review, see responses were averaged for each curve. The dotted lines illustrate
Hari 1990). 'synthetic responses' calculated from the 10.1 Hz responses by
multiplying the repetition rate by 2 and 4. The vertical line at 40
When stimuli are presented at slow rates, typically
msec illustrates the 'apparent latency' of the steady-state response
below 3 Hz, 'transient responses' are elicited. The
deduced from the phase/repetition rate dependence. From Hari et
earliest transient magnetic auditory response to a click
al. (1989b).
