Neural Ctl. of Space Coding, Action Prodn. [Prog. in Brain Res. Vol 142] by C. Prablanc, et. al.,

296 Pages·2003·36.206 MB·English

List of Contributors
A. Bergeron, Montreal Neurological Institute. McGill University, 3801 University Street.
Montreal, QC H3A 2B4, Canada
J. Blouin, UMR 6152 Mouvement et Perception, CNRS and Universite de la Mediterranee.
Campus Scientifique de Luminy, F-13288 Marseille, Cedex 9. France
D. Boisson. Hopital Neurologique Pierre Wertheimer. 59 Boulevard Pinel, 69003 Lyon.
France
G. Bottini, Dipartimento di Psicologia, Universita degli Studi di Pavia, Pavia, Italy
C. Bourdin, UMR 6152 Mouvement et Perception, CNRS and Universitt de la Mediter-
ranee, Campus Scientitique de Luminy, F- I3288 Marseille, Cedex 9, France
W.Y. Choi, Montreal Neurological Institute. McGill University. 3801 University Street.
Montreal, QC H3A 2B4, Canada
J.D. Crawford, York Centre for Vision Research, York University, 4700 Keele Street,
Toronto, ON M3J IP3, Canada
M. Desmurget. Espace et Action, INSERM Unite 534, 16 Avenue Doyen Lepine, 69676
Bron. France
H.C. Dijkerman, Psychological Laboratory, Helmholtz Research Institute, University of
Utrecht, Heidelberglaan 2, 3584 CS Utrecht, The Netherlands
K.C. Engel. Department of Neuroscience, 6-145 Jackson Hall, 321 Church Street S.E..
Minneapolis, MN 55455-0250, USA
A. Fame. Dipartimento di Psicologia, Universita di Bologna, Viale Berti Pichat 5 , 40127
Bologna, Italy
N.J. Gandhi, Division of Neuroscience, Baylor College of Medicine, I Baylor Plaza,
Houston, TX 77030, USA
G. Gauthier, UMR 6152 Mouvement et Perception, CNRS and Universite de la Mediter-
ranee, Campus Scientifique de Luminy, F- 13288 Marseille, Cedex 9, France
B. Gaymard, INSERM 289 and Service d’Explorations Fonctionnelles du Systeme
Nerveux, Hopital Salpetritre. Paris, France
L. Goffart, Espace et Action. INSERM Unite 534, 16 Avenue Doyen LCpine, 69500 Bron,
France
S.T. Grafton. Center for Cognitive Neuroscience. and the Department of Psychological and
Brain Sciences, Dartmouth College, HB 6 I62 Moore Hall. Hanover, NH 03755, USA
H. GrCa, Espace et Action, INSERM Unite 534, 16 Avenue Doyen L&pine, 69676 Bron.
France
A. Guillaume, UMR Mouvement et Perception, Universite de la Mediterranee, CP 910,
163 Avenue de Luminy. 13288 Marseille, France
D. Guitton, Montreal Neurological Institute, McGill University, 380 I University Street,
Montreal, QC H3A 2B4. Canada
K.-P. Hoffmann, Allgemeine Zoologie und Neurobiologie. Ruhr-Universitlt Bochum, D-
44780 Bochum, Germany
G.W. Humphreys, Behavioural Brain Sciences Centre. School of Psychology, University of
Birmingham. Birmingham, B I5 2TT, UK
VI
H. Imamizu, ATR Human Information Science Laboratories, 2-2-2, Hikaridai, Seika-cho,
Soraku-gun, Kyoto 6 19-0288, Japan
S.H. Johnson. Center for Cognitive Neuroscience, and the Department of Psychological and
Brain Sciences, Dartmouth College, HB 6162 Moore Hall, Hanover, NH 03755, USA
M. Kawato, ATR Human Information Science Laboratories, 2-2-2, Hikaridai, Seika-cho,
Soraku-gun, Kyoto 6 19-0288. Japan
G. Kerkhoff, EKN - Clinical Neuropsychology Research Group, Department Neuropsy-
chology, Hospital Bogenhausen, Dachauerstrasse 164, D-80992 Munich. Germany
E.M. Klier. York Centre for Vision Research, York University, 4700 Keele Street, Toronto,
ON M3J IP3. Canada
T. Kuroda. JST/ERATO Kawato Dynamic Brain Project. 2-2-2, Hikaridai, Seika-cho,
Soraku-gun, Kyoto 6 19-0288, Japan
W. Lindner. Allgemeine Zoologie und Neurobiologie. Ruhr-Universitst Bochum, D-44780
Bochum. Germany
L. Liinenburger, Paraplegic Center of the University Hospital Balgrist, CH-8008 Ziirich.
Switzerland
J.C. Martinez-Trujillo. York Centre for Vision Research. York University, 4700 Keele
Street, Toronto, ON M3J IP3. Canada
S. Matsuo, Montreal Neurological Institute, McGill University, 3801 University Street,
Montreal. QC H3A 2B4, Canada
C. Maurer. Neurozentrum, Neurological University Clinic. Breisacher Strasse 64, 79106
Freiburg, Germany
R.D. McIntosh. Cognitive Neuroscience Research Unit, Wolfson Research Institute, Uni-
versity of Durham. Queen’s Campus. University Boulevard, Stockton-on-Tees TS 17
6BH, UK
W.P. Medendorp, York Centre for Vision Research. York University. 4700 Keele Street,
Toronto, ON M3J IP3, Canada
T. Mergner. Neurozentrum. Neurological University Clinic, Breisacher Strasse 64, 79106
Freiburg. Germany
A.D. Milner, Cognitive Neuroscience Research Unit, Wolfson Research Institute. Univer-
sity of Durham. Queen’s Campus, University Boulevard. Stockton-on-Tees TS 17 6BH.
UK
S. Miyauchi. Communications Research Laboratory. 588-2, Iwaoka, Iwaoka-cho, Nishi-ku,
Kobe. Hyogo 65 l-2492, Japan
R.M. Miiri. Eye Movement Research Laboratory and Department of Neurology, Inselspital,
Bern, Switzerland
E. Nakano, ATR Human Information Science Laboratories, 2-2-2, Hikaridai, Seika-cho,
Soraku-gun, Kyoto 6 19-0288, Japan
D. Pklisson, Espace et Action, INSERM UnitC 534. 16 Avenue Doyen LCpine, 69500 Bron,
France
R.J. Peterka, Neurological Sciences Institute, Oregon Health and Science University. 505
NW 185th Avenue, Beaverton, OR 97006, USA
C. Pierro-Deseilligny, Service de Neurologie 1 (AP-HP), HBpital de la SalpEtri&, 46 Bd.
de l’H8pita1, 7567 1, Cedex 13, Paris, France
L. Pisella. Espace et Action. INSERM UnitC 534, 16 Avenue LCpine, 69676 Bron. France
C.J. Ploner. Klinik fiir Neurologie, Charitt, Berlin, Germany
C. Prablanc, Espace et Action. INSERM UnitC 534, 16 Avenue Doyen LCpine. 69676 Bran.
France
vii
S. Rivaud-Pechoux, Service de Neurologie 1 (AP-HP), Hopital de la Salpetriere, 46 Bd. de
l’HBpita1, 75671, Cedex 13, Paris, France
G. Rode, Service de Reeducation Neurologique, Hopital Henry Gabrielle, Hospices Civils
de Lyon, Lyon and Universite Claude Bernard, Route de Vourles, BP 57, F-69565 St
Genis-lava], France
Y. Rossetti, Espace et Action, Institut National de la Sante et de la Recherche Medicale,
Unite 534, I6 Avenue Lepine, Case 13, 69676 Bron, France
F. Sares, UMR 6152 Mouvement et Perception, CNRS and Universite de la Mediterranee.
Campus Scientihque de Luminy, F- 13288 Marseille, Cedex 9, France
M.A. Smith, York Centre for Vision Research, York University, 4700 Keele Street, Toronto,
ON M3J IP3, Canada
J.F. Soechting, Department of Neuroscience, 6-145 Jackson Hall, 321 Church Street S.E..
Minneapolis, MN 55455-0250, USA
D.L. Sparks, Division of Neuroscience, Baylor College of Medicine, 1 Baylor Plaza.
Houston, TX 77030, USA
R. Sterzi, Divisione Neurologica, Ospedale S. Anna, Como, Italy
M. Takagi, Divisions of Ophthalmology and Visual Science, Niigata University, Graduate
School of Medical and Dental Sciences, and CREST, Japan Science and Technology,
Niigata, 95 I-85 10, Japan
R. Tamargo, Department of Neurosurgery, The Johns Hopkins University School of
Medicine, Baltimore, MD 2 1287, USA
G. Vallar, Dipartimento di Psicologia, and Laboratorio di Neuroimmagini Cognitive e
Cliniche, Universita degli Studi di Milano-Bicocca, Edihcio U6 Piazza dell’Ateneo,
Nuovo 1, 20126, Milan, Italy
J.-L. Vercher, UMR 6152 Mouvement et Perception, CNRS and Universite de la Mediter-
ranee, Campus Scientihque de Luminy, F- 13288 Marseille, Cedex 9. France
T. Yoshioka, ATR Human Information Science Laboratories. 2-2-2, Hikaridai, Seika-cho,
Soraku-gun, Kyoto 619-0288, Japan
D.S. Zee, Departments of Neurology and Ophthalmology, The Johns Hopkins Hospital,
Path 2-210, Baltimore, MD 21287, USA
IX
Preface
The commonplace action of pointing or reaching and grasping the simplest object involves
a complex series of neural processing, including object localization and identification,
decision, and the sensorimotor transformations leading to the planning and control of
action. The approach of such a problem has been initially divided into two main fields:
perception and motor control.
Although visual perceptual integration and oculomotor control are commonly consid-
ered as hardly dissociable, the action per se has been considered as deriving from sensory
input and very little the other way around. This book presents some new lines of research
showing the sharp and fast reciprocal influences between the two systems (beyond the
debate between gibsonian and motor theories of perception).
Another evolution of concepts has gone from the antagonist views of brain activity
between neophrenology and widely distributed networks to an intermediate view integrat-
ing both specialized functional areas having multi-modal inputs and outputs and tightly
interconnected with other areas. A simple example is that of the visual and posterior
parietal structures, devoted to space perception, which integrate motor signals, whereas
the limb premotor structures in turn integrate visual and oculomotor signals. The same
intermingling occurs also within the brainstem: for instance whereas the superior colliculus
was considered as a structure devoted only to eye and head movements. recent researches
have shown that it includes hand movement related neurons.
In the same way the oversimplificative dichotomic association of conscious perception
and action/cortical activity, versus unconscious perception and action/subcortical activity,
has been strongly modulated.
More than fifteen years ago, in the same series of Progress in Brain Research, Freund,
Btittner, Cohen and Noth compiled the main communications made in a symposium on
the differences and similarities between the oculomotor and skeletal-motor systems. This
book highlighted the main characteristics of those systems, including large differences in
inertia and in degrees of freedom. At that time the concept of efference copy formalizing
quantitatively the notion of corollary discharge, although very popular in the field of eye
movements research, seemed inappropriate for the control of the upper limb and posture.
This conceptual gap between the two fields has been partially overcome. The approach of
animal behavior, as knowledge has become sharper, has led to concepts of multiple sources
of influence and gone to the notion of cooperative networks. with functions scarcely
reflected by single neuronal activity, but more often subserved by populations of neurons
which give a new insight in the correlation between the average activity of a population
and a behavioral variable. The neural basis of these networks has become possible through
investigations of human brain activity, approached first by brain mapping evoked potentials
and then by neuroimaging methods including PET and fMR1. In addition, the development
of MEG associated with spatio-temporal EEG maps has allowed to follow the fast temporal
evolution of cortical activity. Modeling sensory-motor adaptation and learning by neural
networks compatible with known neurophysiological processes and especially those of the
cerebellum has created a new fertilizing field. These theoretical advances allow tighter
interactions between experimental and modeling approaches, which could be as fruitful as
,
the metaphoric approach of control theory has been for the oculomotor neurophysiologists
during more than twenty years. The field of neuropsychology, derived from the observation
of specific dysfunctions in brain damaged patients, has been totally renewed by the
association of sharp methodological approaches and neuroimaging allowing to observe the
substitution processes that patients developed and the residual functions. Transient lesions
achieved by transcranial magnetic stimulation have provided complementary information.
Clinical neuropsychology has evolved by integrating in its field the knowledge derived
from neuroanatomical, electrophysiological and psychophysical data, and has led to the
development of more efficient rehabilitation tools.
If we have now a better understanding of the way the eye position signals modulate
the visual response of neurons within cortical structures such as the parietal cortex, the
premotor cortex, and in the subcortical brainstem and cerebellar circuitries where both
arm movements and eye and head movements are encoded, we have not yet the key to
the complex sensorimotor transformations for the control of the over-redundant degrees of
freedom of the upper arm. However, some solutions are currently formalized by artificial
neural networks making use of basic physiological principles.
In the field of visuomotor coordination, both the neuroanatomical pathways of fast feed-
forward links between spatial vision and motor behavior and those of slower pathways.
going through the temporal cortex for identification and frontal cortex for decision, have
been revealed by the neuropsychological description of rare clinical cases. The discovered
neuropsychological dissociations have allowed a better understanding of the link between
perception and action.
The association of motor psychophysical techniques together with neuroimaging or
transcranial stimulation of neural structures has also made feasible paradigms allowing
the separation between planning and control phases. They have also revealed the powerful
plasticity of the brain reorganization and their high dependence upon the active adaptation
to sensorimotor conflicts. This adaptation has led to the surprising recovery of upper
cognitive dysfunctions, suggesting that abstraction keeps tight links with sensorimotor
processing. This hypothesis will stimulate new lines of research on the biological substrate
of abstract levels of thinking and on their analogy with spatial representations.
The present book tries to link the new concepts and discoveries in the field of
sensorimotor coordination. It puts together the main contributions of participants of an
international symposium held in Lyon in 2001 and entitled “Neural Control of Space
Coding and Action Production.” The book emphasizes the reciprocal relationship between
perception and action, and the essential role of active sensorimotor organization or
reorganization in building up perceptual and motor representations of the self and of the
external world.
C. Prablanc
D. Pelisson
Y. Rossetti
(Editors)
Acknowledgements
We greatly acknowledge the following institutions for the financial support of the sym-
posium from which this book is issued : Institut National de la Sante et de la Recherche
Medicale (INSERM), Universite Claude Bernard, Centre National de la Recherche Sci-
entifique (CNRS), Institut FCdhatif des Neurosciences de Lyon (IFNL), SociCtC des
Neurosciences, Pole Rhone-Alpes des Sciences Cognitives, Conseil General du RhBne and
Region RhGne-Alpes. We are also indebted to the following companies for their dona-
tions : Optique Peter, Ipsen, Synapsis, SMI-Gmbh, Credit Mutuel Enseignants, Essilor.
UCB-Pharma SA, John Benjamins, Jansen-Cilag.
We gratefully acknowledge the active contribution of the members of the INSERM
Research Unit 534 Espace et Action to the organisation of the symposium, and especially
the contribution of Mrs Soulier for the administrative part, and thank Mr Borsch and Mr
Prince for the illustrations. We also thank the reviewers for their helpful criticisms and for
their contribution to the quality of the book.
CHAPTER 1
Cortical control of ocular saccades in humans:
a model for motricity
C. Pierrot-Deseilligny I,*, R.M. Mb-i *, C.J. Ploner 3, B. Gaymard ‘A and
S. Rivaud-Pkhoux ’
Abstract: Our knowledge of the cortical control of saccadic eye movements (saccades) in humans has recently progressed
mainly thanks to lesion and transcranial magnetic stimulation (TMS) studies, but also to functional imaging. It is now
well-known that the frontal eye field is involved in the triggering of intentional saccades. the parietal eye field in that of
reflexive saccades, the supplementary eye field (SEF) in the initiation of motor programs comprising saccades, the pre-SEF
in learning of these programs, and the dorsolateral prefrontal cortex (DLPFC) in saccade inhibition, prediction and spatial
working memory. Saccades may also be used as a convenient tnodel of motricity to study general cognitive processes
preparing movements. such as attention, spatial memory and motivation, Visuo-spatial attention appears to be controlled by
a bilateral parieto-frontal network comprising different parts of the posterior parietal cortex and the frontal areas involved
in saccade control, suggesting that visual attentional shifts and saccades are closely linked. Recently, our understanding of
the cortical control of spatial memory has noticeably progressed by using the simple visuo-oculomotor tnodel represented
by the memory-guided saccade paradigm, in which a single saccade is made to the retnembered position of a unique visual
item presented a while before. TMS studies have determined that, after a brief stage of spatial integration in the posterior
parietal cortex (inferior to 300 ms), short-term spatial metnory (i.e. up to I S-20 5) is controlled by the DLPFC. Behavioral
and lesion studies have shown that medium-term spatial metnory (between IS-20 s and a few minutes) is specifically
controlled by the parahippocampal cortex, before long-term metnorization (i.e. after a few minutes) in the hippocatnpal
formation. Lastly, it has been shown that the posterior part of the anterior cingulate cortex. called the cingulate eye field.
is involved in motivation and the preparation of a11 intentional saccades, but not in reflexive saccades. These different
but complementary study methods used in humans have thus contributed to a better understanding of both eye movement
physiology and general cognitive processes preparing motricity as whole.
Introduction vestibulo-ocular reflex) stabilize images on the retina
for vision, whereas rapid eye movements (i.e. oc-
Eye movements serve vision and are either rapid ular saccades) allow vision to change quickly the
or slow. Slow eye movements (ocular pursuit and images which have to be seen. There are different
types of saccades. Saccades may be reflexive. exter-
nally triggered by the sudden appearance of a visual
* Corresponding author. C. Pierrot-Deseilligny, Service
de Neurologie 1, Hopital de la Salpetriere. 47 Bd de target (reflexive visually guided saccade) (Fig. IA)
I’HBpital, 7.5651 Paris cedex 13. France. Tel.: [phone]. or intentional, internally triggered towards a target
I X2X: Fax: [phone]: either already present (intentional visually guided
E-mail: [email protected] saccade), not yet present (predictive saccade) or no
Peripheral visual target
Extinguishing
1 STIMULI )
4.
Central fixation point f r Visually guided saccade
( SACCADE [
Error (misdirected saccade)
1 ANTISACCADE 1
M
‘t
:
: \ L
-:
L Correct antisaccade
4 b
A
Gap
Latency
Movement
Peripheral flashed -;
L
target
4
Go signal
riGGLq
- _ - - - r-L:
/c
Corrective saccade
Central fixation point 1
c
-Memory-guided saccade
50 ms Delay
LZcy
longer visible (memory-guided saccade) (Fig. IB). should be interpreted with caution. Finally, all these
Antisaccades, made in the opposite direction to a methods provide complementary information in the
suddenly appearing visual target. are also intentional study of any human cerebral function, including the
saccades (Fig. IA). Lastly. there are spontaneous control of different types of saccades.
saccades, made for example at rest in darkness. and Saccades may be studied per se to improve our
quick phases of nystagmus, which are also saccades. knowledge of eye movement physiology. However.
Saccades are generated in the brainstem reticular saccades may also be used as a convenient model of
formations. but are prepared and triggered by the motricity to understand complex neuropsychological
cerebral cortex, except for the quick phases of nys- processes such as attention, spatial integration, spa-
tagmus. which are entirely controlled in the brain- tial memory, prediction and motivation. Therefore,
stem. Between the cortical areas and the brainstem, after a brief review of our current knowledge of
a number of subcortical structures (basal ganglia and the cortical areas triggering or inhibiting saccades in
superior colliculus) are also involved in the control humans, i.e. the movement taken here as a model.
of saccades (see PClisson et al., 2003, this volume), this chapter will focus on the study of the main neu-
but this large field falls outside the scope of this ropsychological processes preparing this movement
chapter. In humans. several methods may be used to as well as motricity in general.
study the control of saccades at the cortical level.
Lesion studies are required to determine which corti- Movement
cal areas are crucial to perform a saccade paradigm.
However, lesion studies cannot tell at what spe- In a sensory-motor act, i.e. a movement responding
us
cific time in the execution of this paradigm each to a sensory stimulus, there are different stages of
area plays a significant role. Transcranial magnetic preparation and execution of the movement. At the
stimulation (TMS), recently used in research to study cortical level, the movement is either triggered, the
different cerebral functions. can help to answer such triggering marking the end of the preparation phase
questions. This technique. which inhibits or inacti- and the beginning of the execution phase (Fig. 2: 4),
\‘ates the stimulated areas for a few milliseconds, or inhibited.
i.e. with the same effect as a brief functional le-
sion, has relatively good temporal resolution, but
poor spatial resolution. Conversely, functional imag-
ing, i.e. PET scan and functional magnetic resonance Experimental studies have shown that three cerebral
imaging (WRI), has the best spatial resolution but areas are capable of triggering saccades (Pierrot-De-
relatively poor temporal resolution and at times false seilligny et al., 1995b; Leigh and ‘Zee, 1999): the
positive or negative activity. Functional imaging is frontal eye field (FEF), the supplementary eye field
therefore mainly useful to determine the precise lo- (SEF) and the parietal eye field (PEF). In humans.
cations of the ocular motor areas in humans, and functional imaging suggests that the FEE SEF and
other types of results obtained using this method PEF are involved in the control of all saccade types.
-
Fig. I. (A) Main haccade paradigms used. Retlexive visually guided baccade and antiaaccade paradigms. In the saccade paradigm. the
subject. fixating a central fixation point. has to make a reHexive visually guided saccade as soon as the peripheral visual target occurs.
Latency is a reflection of the triggering mechanism of this reflexive saccade. Note that a gap is used. i.e. the central point is extinguished
200 ms before the appearance of the vijual target. in order to facilitate the disengagement of fixation. In the antiaaccade paradigm. the
subject is instructed to make a haccade in the opposite direction to the visual target. A reflexive misdirected saccade to the target i\
an error- and the percentage of errors is a reflection of inhibition mechanisms controlling saccades. Latency of correct anti\accade\ i\
a Ireflection of the triggering mechanisms of intentional saccades. (B) Memory-guided jaccade paradigm. A peripheral visual target is
Hnshed while the subject is fixating a central lixation point. After a delay (memorization). the central point is switched-off (‘go <igal’)
and the \uh.ject then ha\ to make a saccade to the remembered position of the Hash. Accuracy of this memory-guided saccade (or of the
final eye position if there arc several \accades) i\ a reHection of spatial memory. Latency is a reflection of the triggering mechanism\ of
intentional \accade\. 1.. left: M. midline; R. right.