Eye Movements from Physiology to Cognition. Selected/Edited Proceedings of the Third European Conference on Eye Movements, Dourdan, France, September 1985

640 Pages·1987·17.666 MB·English

by  J.K. O'Regan and A. Lévy-Schoen (Eds.)

EYE MOVEMENTS
From Physiology to Cognition
Selected/Edited Proceedings of the
Third European Conference on Eye Movements
Dourdan, France, September 1985
Edited by:
J.K. O'REGAN
and
A. LEVY - SCHOEN
Groupe Regard
Laboratoire de Psychologie Expérimentale
CNRS, Université René Descartes, EPHE, EHESS
Paris, France
1987
NORTH-HOLLAND
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© Elsevier Science Publishers Β .V., 1987
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Cover design: ® by Vera Molnar, 1987
Library of Congress Cataloging-in-Publication Data
European Conference on Eye Movements (3rd : 1985 :
Dourdan, Franc e)
Eye movements.
Bibliography: p.
Includes index.
1. Eye--Movements—Congresses. 2. Cognition—
Congresses. 3. Neuropsychology—Congresses.
I. 0fRegan, J. Κ. II. Levy-Schoen, A. III. Title.
QP477.5.E9 1985 612\846 86-19785
ISBN 0-444-70113-3
PRINTED IN THE NETHERLANDS
ν
PREFACE
This book contains edited versions of the majority of the papers and posters
presented at the Third European Conference on Eye Movements, held at Dourdan,
France, from 24 to 27 September, 1985.
The study of eye movements is of course a research field in its own right. But
eye movements have an additional particularity, which is that they can be used as a
tool to reveal covert perceptual and cognitive processes. This explains why workers
with many different research interests, ranging from the fundamental to the applied,
are concerned with eye movements. The conference's purpose was to allow these
workers to exchange viewpoints.
In attracting participants from a wide range of disciplines, we were continuing
in the tradition of the two previous European Conferences on Eye Movements, held in
Bern in 1981 and in Nottingham in 1983. The number of participants at these confer-
ences has increased rapidly since the first conference, rising from 100 through 150,
and reaching 250 at the present conference, with 20 countries being represented.
The conference was organised into symposia spanning eye movement research from
the neurophysiological to the cognitive and applied levels. Among these, the sym-
posium on Saccade Programming was the largest at the conference. One of the reasons
for this was undoubtedly the excellent organisation by John Findlay and Zoi Kapoula.
A further reason lies in the increasing success of classical biocybernetic models
describing the mechanical properties of eye saccades, as studied behaviourally, in
explaining and motivating neurophysiologal research into the saccadic system. Tes-
tifying to this, many of the papers presented at the Saccade Programming Symposium
concerned behavioural evidence pertinent to study of the neurophysiologically known
pulse generation system. Also relevant to biocybernetic modelling of eye movements
were a number of papers concerning the question of how eye position is represented
in the visual system. This determines how the eye saccade will adapt to a change in
target position, and also how movement perception will depend on eye movements.
Another centre of interest at the Programming Symposium concerned the cognitive
factors involved in saccade programming. These factors are essential in determining
which among several targets should be aimed at, and also in controlling the way a
smooth pursuit movement will follow a predictable target.
Adaptability is a fundamental property of biological systems, as these must at
the same time be sufficiently stable in their functioning to guarantee fast and
efficient responses to surrounding sollicitations, but also sufficiently flexible to
adjust to changing constraints and new demands for survival. A number of identi-
fiable subsystems take part in eye movements: the saccadic system, the smooth
pursuit system, and the various vestibular and optokinetic reflexes. Changes in
oculomotor behaviour can occur through adaptation within a given subsystem or by
different modes of interaction between subsystems. This latter type of adaptation
is important in man, for whom cognitive factors play a role. In the Symposium on
Adaptation in the Oculomotor System, a first session concerned adaptation (induced
by experimental manipulations or by pathology) within the saccadic system, either
with reference to cybernetic models, or to physiology. A second session contained a
few papers on the smooth pursuit system, but mainly was concerned with interactions
between subsystems, particularly eye-head coordination. As was the case for the
symposium on Saccade Programming, the Adaptation Symposium showed the usefulness of
a dialogue between biocybernetic models and physiology or pathology.
vi Preface
The symposium on Scanning was divided into papers attempting to model parame-
ters of ocular exploration, and papers describing scanning behaviour in cognitive
tasks and reading. Our idea in this symposium was to encourage participants to
bridge the gap between theory and observation. While biocybernetic models study the
saccade triggered by an isolated target, when considering the sequence of saccades
that the eye makes in exploring a complex scene, it becomes necessary to take
account of global scanning strategies (for example, in reading, from left to right,
line by line). In addition a process of selection of targets among non-targets must
intervene; further, pre-processing of information in non-central vision will take
place. These factors were considered in some of the theoretical papers, although
these were limited to relatively simple situations, such as search for a letter in a
string of letters, or scanning a sequence of dots. The more descriptive papers
considered more complex situations, for example scanning of stationary or moving
images, reading, or eye movements during problem solving or aesthetic judgements.
In order to progress, research on the scanning of visual scenes now needs a
theory of how humans recognize such scenes. This problem is less acute in the study
of reading: here the objects to be recognized are describable in terms of well-
defined units (letters, words...). Further, well-developed linguistic theories
describing how these units combine (lexical structure, syntax, semantics) give us a
description of the objects being looked at. Finally an abundant literature in
experimental psychology is concerned with letter and word perception, and psycho-
linguistics has for many years been concerned with lexical access and sentence
comprehension. Reading is thus a sort of microcosm of visual perception in which
the study of eye scanning may be more profitable than in the wider, less well
understood domain of visual scenes in general. At the present conference, a special
topic within reading research, namely Lexicons and Languages, was chosen as a point
of interest. The first session was aimed at the problem of differences between
languages, with particular reference to languages written in non-european alphabets
such as Japanese and Arabic. A thorough review of the main writing systems is
provided at the beginning of the section as a background to the eye movement stu-
dies. A second, more general session was concerned with the influence of typo-
graphy, task demands, and ambiguity on sentence processing as measured by eye move-
ments.
The symposium on The Usefulness of Eye Movements in Ergonomics and Applied
Studies attracted fewer papers than we had hoped. There were papers on automobile
dashboard design, improving performance in sport, of doctors in radiological diag-
nosis, of postal and bank workers. It appears that eye movements, at present, give
little more information about performance than can be obtained by verbal question-
ing. Again, as was the case for Scanning, the problem is a lack of a satisfactory
description of the tasks being studied and of the actions that the subjects must
undertake to accomplish them. Without these, eye movement data are too complex to
interpret.
In the symposium on Measurement Techniques it was apparent that current re-
search generally concerns, not new techniques, but ways of improving the reliability
of existing ones. In particular, the real time use of microcomputers to calibrate
and control measurements allows increased accuracy and ease of use. A number of
not-too-expensive commercial systems were demonstrated at the conference.
In conclusion, it is interesting to compare the contents of the present confer-
ence with that of its predecessors in Europe and the United States. First, we noted
a decrease in the number of submitted papers on applied topics such as ergonomics
and médecine, as well as in the fields of visual development of the child and of
pathology. (It is of course difficult to know whether this corresponds to morose-
ness in these fields, or to our having insufficently publicized the conference in
these fields). Second, we noted an increasing interest in interdisciplinary studies
that unite biocybernetic models with neurophysiology and that take account of cogni-
tive factors.
Finally, it is clear that eye movement research remains an expanding domain.
Preface vii
Acknowledgement s
The conference was supported financially by the Centre National de Recherche
Scientifique, Electricité de France (Club Lumière), Essilor, Union Nationale des
Syndicats dfOpticiens de France, and Société d'Optique Physiologique. We would
particularly like to thank the symposium organisers: John Findlay, Zoi Kapoula,
Gabriel Gauthier, Alain Berthoz, Bernard Pavard, Gilles Roman, James Richardson, and
Michel Neboit, who helped us put together the topics, encouraged contributions in
each of the domains, selected among the potential papers, and finally, proposed
changes and clarifications in the final manuscripts. The success of the conference
was to a great extent due to this arduous work. We would also like to thank Rudolf
Groner and Alastair Gale, who, having organised the previous two conferences, gave
us precious advice. The following people also gave scientific advice: D. Heller, C.
Menz, J. Leplat, and C. Bonnet. Finally, the conference would not have been possib-
le without the patient secretarial work of Marie-Denise Philomète and the excellent
assistance of Jacqueline Guerre. Finally, very special thanks are due to Barbara
Steinkeller, who was the organisational mainstay before, during, and after the
conference, and who also helped us with the preparation of the manuscript.
J.K. 0»Regan
A. Lévy-Schoen
Paris, May 1986
EYE MOVEMENTS: From Physiology to Cognition
J.K. O'Regan and A. Lévy-Schoen (editors)
© Elsevier Science Publishers B.V. (North-Holland), 1987 3
SYMPOSIUM INTRODUCTION : THE MODELLING OF
SACCADE PROGRAMMING
John M. Findlay*
Zoi Kapoula**
* Department of Psychology, University of Durham, South Road,
DURHAM DH1 3LE, England.
**Laboratoire de Psychologie Experimentale, 28 rue Serpente, PARIS.
The previous European Conference on Eye Movements contained a session entitled
Properties of the Saccadic Eye Movement System (Gale and Johnson, 1984). This
demonstrated that the current capacities for accurate recording of saccadic eye
movements and automated analysis of such records have opened up many options for
scientific study. The symposium at Dourdan shows that this approach continues
to be productive. Indeed the number of papers in the saccade programming
symposium was so large that individual mention of all papers in this introduction
is regrettably not feasible. Also study of saccadic eye movements forms the
basis of much work reported in the Scanning and the Adaptation symposis.
The saccadic eye movement system has attracted the attention of workers in
several different disciplines and this can only be welcome in an era of
increasing fractionation and compartmentalization of knowledge. Contributions
to the symposium come from engineers, physicists, physiologists and
psychologists, and it is fitting that several contributors explicitly
acknowledge the influence of D.A. Robinson. Robinson, as a physiologist with
a background in systems engineering has pioneered the careful harmonization of
engineering concepts with physiological findings. In consequence the modelling
of the saccadic system that appears in the following pages is much more
constrained by the realities of brain function than any comparable modelling in
the past. Thus in general, rather than resulting in totally new insights, much
work is concerned with fleshing out details and redressing the unfortunate
overemphasis on horizontal saccades in earlier studies.
What is the physiological basis on which saccadic modelling now stands? We know,
through the work on single unit recordings in animals (see e.g. Fuchs, Kaneko and
Scudder, 1985), that certain cells in the brainstem are normally active but switch
off for each and every saccade - the omnipauser cells. We know in turn that when
these cells switch off, burst cells are released from inhibition, or at least a
selection of burst cells since these, in contrast to the omnipauser cells,
selectively code the spatial properties of the saccadic movement. Above all we
know, following the work of Robinson (1975, 1981), how the burst cells can
direct the appropriate firing in the motoneurons to move the eye and hold it in
position. Thus the basic pulse generation system can be regarded as well
established, although one of the most significant developments in recent years
has been the demonstration by Fischer's group of different categories of
saccades based on measures of latency distributions. These presumably reflect
different points in time at which the pulse generator may be activated.
Several papers address the issue of whether there might be more than one pulse
generator, notably those by van Gisbergen, van Opstal and Roebroek, and the
impressive study on the pigeon by Bloch, Lemeignan and Martinoya. Properties
of the pulse generator also form the basis of the paper by Inchingolo,
Spanio and Bianchi, and the posters by Galley, by Kapoula, Robinson and Hain,
and by Bour, de Veth and Huygen.
Another idea introduced by Robinson was that the control of burst cells to move
the eye to the target position was achieved by a local feedback loop using
4 J.M. Findlay and Ζ. Kapoula
instantaneous eye position information. Several of the papers are concerned
with the details of how this might be implemented and the general idea of a
spatiotopic framework for saccade planning is discussed below in connection with
predictive eye movements. Van Gisbergen et al provide further confirmation, in
a very striking way, that saccades trajectories are modifiable in a target-seeking
manner. Viviani and Velay carry out a psychophysical study which parallels the
informative demonstration by Mays and Sparks (1980) that saccade control uses a
spatiotopic signal, and the paper by Ling relates to the same issue. Roll and
Roll introduce the technique of muscle vibration to discover properties of the
extraocular muscle system. The partial stabilization technique of
Barabanschikov shows that a bizarre form of interference with voluntary eye
movement can be created when the relationship between the direction of movement
of the eye and contingent direction of retinal motion is changed. However, it is
interesting that small changes in this relationship pass unnoticed.
Moving upwards from the brainstem circuitry that generates the movement itself,
psychophysical studies in the posters by Ästen and Gielen and by van der Wildt,
Flipse, Rodenburg and Keemink examine the properties of the visual system in
relation to eye movements. The poster by Accardo, Inchingolo and Pensiero
enriches our knowledge of the relation between latency and size of the movement
which is often thought to be due to visual processing.
Amongst psychologists, saccadic eye movements are usually seen as a means rather
than an end and interest focuses on their role in perception and cognition. In
the area of perception particularly, the elegant work of oculomotor modellers and
experimenters, along with other work in neurobiology, has currently to face
criticisms from a movement, associated with the writings of J.J. Gibson (1966,
1979), which queries the relevance of laboratory based studies for understanding
perception in real world environments. We believe that this attack is largely
unjustified and that work in eye movements has been more sensitive than in some
other areas to the biological nature of the system under study, for example in
the recent emphasis on adaptive properties of oculomotor control.
Nevertheless it is necessary to be vigilant. It is easy to forget that eye
movements did not evolve to scan display screens. Certain things are
immediately evident when consideration is given to 'real world' eye movements.
The three dimensional nature of visual space is paramount and this has the
consequence that the normal visual input to the saccadic system is different in
two respects from that usually considered by systems modellers. Firstly, sharply
focused, small targets are unlikely to occur frequently. Secondly, targets at
a different depth from the original fixation plane will show disparity; that is
the retinal error signal in the two eyes will differ. When this is borne in mind,
it is not too surprising that the saccadic system shows the spatial integration
of the visual input found in the global effect (Findlay, 1982; Ottes, van
Gisbergen and Eggermont, 1984).
Gibson's ambition to explain perceptual systems with no reference to cognitive
process sometimes drove him to absurd lengths when he discussed eye movements.
His claim (Gibson 1966, p.260) that shifts of fixation can be attributed to
"interesting structures in the array and interesting bits of structure" answers
very little. Saccadic eye movements provide an unrivalled opportunity for
psychologists to investigate the microstructure of cognitive activity (or
whatever name is given to the process which allows what is 'interesting' to
change from moment to moment). Much of the material on cognitive control of
saccades is to be found in other symposia but two papers (Coëffé and Menz and
Groner) examine the tradeoff between sensory and cognitive factors in the
programming of saccades to newly appearing complex targets. Both confirm the
interaction that occurs between the two influences on the spatial properties of
the saccades supporting the view that this is a fruitful research strategy
(Findlay, 1985).
Symposium introduction 5
Arguably the simplest evidence of cognitive activity comes when anticipatory
saccades are made to a predictable target movement. Ron, Droulez and Vieville
demonstrate prediction in the saccades to acquire a moving target, thus
extending the debate about the saccadic system's ability to 'take into account'
target motion. It is worth noting that a recent study shows that monkeys also
are capable of such a predictive ability (Newsome, Wurtz, Dursteler and Mikami,
1985). A pressing need seems to be to decide whether such predictive abilities,
which seem attributable to low levels ('predictive ability in the saccadic
system'), are really different from predictive abilities at higher levels. The
demonstration by Zambarbieri, Schmid and Ventre is important in this context in
showing that similar patterns of predictive saccadic movements emerge when the
stimulus is auditory rather than visual. The concept of a general spatial
framework for motor programming is very appealing. Skavenski and Hansen (1978)
suggested some time ago that the same information might be used for the control
of eye movements and for limb movements. The elegant results of Pelisson,
Goodale and Prablanc showing readjustment of manual pointing on the basis of
target error following a saccade evidently fit well into this framework, as
also does the paper by de Bie, van den Brink and van Sonderen. The posters by
Lecas and Vitton and by Fischer and Rogal also concern eye-hand interactions.
These ideas have a significance away beyond the narrow specialisation which
might appear indicated by the title of the symposium.
J. M. Findlay and Ζ. Kapoula
6
REFERENCES
Findlay, J.M., Global processing for saccadic eye movements, Vision Research,
22 (1982) 1033-1045.
Findlay, J.M., Saccadic eye movements and visual cognition, L'Année
Psychologique, 85 (1985) 101-136.
Fuchs, Α.F., Kaneko, C.R.S. and Scudder, CA., Brainstem control of saccadic
eye movements, Annual Review of Neuroscience, 8 (1985) 307-337.
Gale, A.G., and Johnson, F.W., Theoretical and Applied Aspects in Eye Movement
Research (North-Holland, Amsterdam, 1984).
Gibson, J.J., The senses considered as perceptual systems (Boston, Houghton-
Mifflin, 1966).
Gibson, J.J., The ecological approach to visual perception (Boston, Houghton-
Mifflin, 1979).
Mays, L.E. and Sparks, D.L., Saccades are spatially, not retinotopically, coded,
Science, 208 (1980) 1163-1165.
Newsome, W.T., Wurtz, R.H., Dursteier, M.R. and Mikami, Α., Deficits in visual
motion processing following ibotenic lesions of the middle temporal visual area
of the macaque monkey, J. Neuroscience, 5 (1985) 825-840.
Ottes, F., van Gisbergen, J.A. and Eggermont, J.J., Metrics of saccade responses
to visual double stimuli : two different modes, Vision Research, 24 (1984)
1169-1179.
Robinson, D.A., Oculomotor control signals, in Bach-y-Rita, P. and Lennestrand, G.
(eds.), Basic Mechanisms of Ocular Motility and their Clinical Applications
(Oxford, Pergamon, 1975).
Robinson, D.A., Control of eye movements, in Brooks, V.B. (ed.), Handbook of
Physiology, Section 1 : The Nervous System. Volume 2 : Motor Control, Part 2,
(Bethesda, American Physiological Society).
Skavenski, A.A. and Hansen, R.M., Role of eye position information in visual
space perception, in Sanders, J.W., Fisher, D.F. and Monty, R.A. (eds.),
Eye Movements and the Higher Psychological Functions (Hillsdale, Lawrence
Erlbaum, 1978).
EYE MOVEMENTS: From Physiology to Cognition
J.K. Ο'Regan and A. Lévy-Schoen (editors)
© Elsevier Science Publishers B.V. (North-Holland), 1987 7
DYNAMICS OF SACCADIC TRACKING RESPONSES: EFFECTS OF TASK COMPLEXITY
A.C. Smit, J.A.M. van Gisbergen* and A.R. Cools
Depts. of Pharmacology and Medical Physics and Biophysics*
University of Nijmegen, P.O. Box 9101,
6500 HB Nijmegen, The Netherlands
The influence of task complexity on saccade dynamics was
explored using three experimental paradigms: visual
target, remembered target, and anti-saccade task. Main
sequences were established for all three types of
saccades, for two subjects. We have found that (1)
anti-saccades and saccades to remembered targets have
strongly reduced peak velocities, (2) these saccades
typically have very skewed velocity profiles, and (3) the
reconstructed neural control signals, held responsible
for the generation of these saccades, are quite abnormal.
INTRODUCTION
Saccadic responses to visual targets are characterized by fixed relationships
among amplitude, duration and peak velocity, the so-called main sequence
(Bahill, Clark and Stark, 1975; Baloh, Stills, Kunley and Honrubia, 1975). In
the human, saccades made to remembered targets (Becker and Fuchs, 1969), or to
auditory targets in darkness (Zambarbieri, Schmid, Magenes and Prablanc, 1982)
are known to be somewhat slower. In the monkey a similar result has been
obtained for saccades to remembered targets (Hikosaka and Wurtz, 1985a).
Furthermore, Hallett and Adams (1979) have noticed 'anomalous' velocity
profiles in saccades away from a visual cue stimulus (antisaccades). Taken
together, these findings indicate that the task and the stimulus conditions
seem to influence saccade dynamics. This may imply the involvement of different
supranuclear systems in the generation of these saccades. There is indeed some
preliminary evidence that remembered target saccades and antisaccades are
generated by a neural subsystem which is different from that responsible for
saccades to a visual stimulus (Hikosaka and Wurtz, 1985b; Guitton, Buchtel and
Douglas, 1985).
We have further explored the influence of task complexity on the dynamics of
saccadic responses, by using three different experimental paradigms: visual
target, remembered target and antisaccade task.
We found that main sequence plots are insufficient to characterize the abnor-
mally shaped velocity profiles which we have observed. As will be demonstrated,
there appears to be a strong relationship between the skewness of the velocity
profile and saccade duration.
Finally, we have tried to reconstruct the neural control signals involved in
the generation of these saccades, using a deconvolution method described by Van
Opstal, Van Gisbergen and Eggermont (1985). The results show that the amplitude
and the shape of the pulse in the reconstructed neural control signal for re-
membered target saccades and antisaccades is very abnormal.