The Brain and Regulation

of Eye Movement
The Brain and Regulation
of Eye Movement

A. R. Shakhnovich
N. N. Burdenko Moscow Institute of Neurosurgery
Academy of Medical Sciences of the USSR

Translated from Russian by

Basil Haigh

With a Foreword by
Lorrin A. Riggs
Brown University

PLENUM PRESS· NEW YORK AND LONDON

 Library of Congress Cataloging in Publication Data
Shakhnovich, A R
The brain and regulation of eye movement.
Revised translation of Mozg i reguliatsiia Dvizhenii glaz.
Bibliography: p.
Includes index.
1. Eye-Movements-Regulation. 2. Brain. I. Title. [DNLM: 1. Eye movements.
2. Visual cortex-Physiology. WW400 S527m]
QP477.5.S5213 612'.846 77·2209

ISBN 978-1-4684-6966-0 ISBN 978-1-4684-6964-6 (eBook)

001 10.1007/978-1-4684-6964-6

Aleksandr Romanovich Shakhnovich. Doctor of Medical Sciences, is a clinical

neuropathologist and is currently director of the research group in experimental
neurology at the N. N. Burdenko Moscow Institute of Neurosurgery, Academy of
Medical Sciences of the USSR. He is at present engaged chiefly on the study of
the neurophysiological mechanisms of human psychological activity, the problem
of unconscious states, and the pathology of the cerebral circulation.

The original Russian text, published by Meditsina in Moscow in 1974, has been
corrected by the author for the present edition. This translation is published
under an agreement with the Copyright Agency of the USSR (V AAP).

M03r 11 PErYJI5ILll151 .ll.Bl1)1(EHl1F1 rJIA3

AAeKcaHap POMaHo8u~ LUaxHo8u~

MOZG I REGUL YATSIY A DVIZHENII GLAZ

Aleksandr Romanovich Shakhnovich

© 1977 Plenum Press, New York

Softcover reprint of the hardcover 1st edition 1977
A Division of Plenum Publishing Corporation
227 West 17th Street, New York, N.Y. 10011
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, mechanical, photocopying, microfllming,
recording, or otherwise, without written permission from the Publisher
 Foreword

Dr. Shakhnovich brought out the original Russian edition of this work in 1974.
Fully half of that book was concerned with his own studies of eye movements.
These included observations on patients with neuromuscular disorders that
produced unique oculomotor deficits. Other anomalies of eye motility resulted
from local changes in cerebral and cerebellar blood flow and the effects of
surgical intervention for aneurisms and brain tumors. Supplementary experi-
ments included the probing of single units in the motor and visual brain areas of
rabbits. Still other studies were done on normal human eye movements with the
aid of the Yarbus "cap" attachment to the cornea of the eye.
A major aim of the original book was to show that eye movements provide
a relatively simple illustration of "goal-directed behavior." This traditional
Russian theme, developed by Sechenov, Pavlov, and Bemshtein, was put forth as
a unifying concept to explain the author's findings. Consideration was also given
to Western ideas ana problems that dominated the research of the 1950's and
1960's. Among these, as summarized by Dr. Shakhnovich, were perceptual
constancy, corollary discharge, saccadic suppression, and the effects of image
stabilization.
The present English translation includes not only the 1975 contents but
also 30 additional figures and numerous additions to the text and bibliographic
references. The intent here is obviously to update and revise the Original work in
order to prepare it specifically for Western readers. The present work can
therefore be credited with presenting experimental studies and points of view
not previously available in English for students of vision and eye movements.
While recognizing these valuable aspects of Dr. Shakhnovich's work, the
reader should not make the mistake of viewing this monograph as a guide to the
present state of knowledge on the control of eye movements. The new material
that the author has added brings the reporting of his own and related research up
v
vi FOREWORD

to date, but does not involve a change in the basic point of view. Recent Western
work, in particular, the exciting new American experiments involving single unit
recording and stimulation in the alert, responding monkey and the bioengineer-
ing approach that permits concise formulations and explanations of results, is
dealt with rather perfunctorily. Admittedly, no one person could be expected to
cover all aspects of eye movement research, and the present author has quite
naturally emphasized the neurological and ideological features for which his own
background has prepared him.
Regrettably, there is still an enormous cultural barrier between Russian
and Western treatments of physiological problems. Certain features of this book
may therefore appear strange to Western eyes. For example, some eye movement
records are published without amplitude scales. In the single unit studies there is
often insufficient specification of the location of the microelectrode. There is no
indication of the manner in which Dr. Shakhnovich has arrived at a very
different frequency spectrum from that previously reported for tremor motions
of the human eye, and there is no explanation for his insistence that tremor is
important visually to prevent the disappearance of objects of regard. It is
difficult to get any unifying grasp of the significance of the many surgical cases
of changes in blood flow, even though these are unique and provocative
observations.
By presenting a comprehensive review of Russian work, Dr. Shakhnovich
contributes to the lifting of the barrier that has prevented an international effort
to achieve understanding of the regulation of eye movements. For this he
deserves credit; this English translation goes farther in that direction than did the
original Russian monograph. Let us hope that still further progress along these
lines will soon be made from both sides of the barrier.
Lorrin A. Riggs
Professor of Psychology
Brown University
 Preface

The behavior of the living organism in the course of its active integration with
the outside world is one of the most complex and ideal forms of homeostasis.
The sense organs, and above all the organ of vision, with its central
connections, play an essential role in the organization of the goal-directed
behavior of man and animals.
The accessory apparatus of the organ of vision, the eye muscles, are
controlled by a hierarchy of innervation mechanisms located at different levels
of the nervous system. This broad representation of the innervation mechanisms
of the eye muscles in the nervous system is the reason for the occurrence of a
great variety of disturbances of eye movements in patients with local brain
lesions.
Because of improvements in electrophysiological and biophysical methods,
it is now possible to undertake a more refined analysis of the mechanisms of
control of eye movements. The high accuracy of recording of these movements
and their correlation with single-unit activity at different levels of the nervous
system have been instrumental in the obtaining of much new evidence.
The study of the physicochemical mechanisms of memory, thought, and
behavior is an interesting problem in modern neurology. The system controlling
the eye movements is one of the simplest models of goal-directed behavior, and
one of the most convenient to investigate. The remarkable ability of the brain to
plan for the future is nowhere more clearly revealed in behavioral responses than
in the system controlling eye movements.
The use of eye movements to study the mechanisms of formation of
"plans of behavior" was the basic task of the writer of this book. At the same
time, an attempt was made to discover the special features distinguishing the
character of function of neuron groups at different levels of innervation during
eye movements.
vii
 Contents

Chapter I. The Structural and Functional Organization of the Innervation

Mechanisms of the Eye Muscles
Peripheral Innervation of the Eye Muscles
Supranuclear Innervation Mechanisms of the Eye Muscles 3
Afferent Regulation of the Tonus of the Eye Muscles 16

Chapter II. Fixation Movements of the Eyes 23

The Role of Fixation Movements of the Eyes in Visual Perception 23
Microtremor of the Eyes as an Indicator of Combined Activity of
Motor Units of the Ocular Muscles . . . . . . . . . . . . . 25
Mechanisms Controlling Fixation Micromovements of the Eyes 45
Plasticity of the System for Stabilization of Fixation . . . . . . 64

Chapter III. Tracking Movements of the Eyes . . . . . 67

Visual Perception of Moving Images . . . . . . . . 67
Mechanisms of Extrapolation in the Control of Tracking Movements of
the Eyes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 69
Electrical Activity of the Ocular Muscles During Tracking Movements
of the Eyes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72

Chapter IV. Saccadic Eye Movements 79

Saccadic Eye Movements and Visual Functions 79
Mechanisms Controlling Saccadic Eye Movements 81
Electrical Activity of the Ocular Muscles During Saccadic Eye Movements 92
ix
x CONTENTS

Chapter V. Convergent Eye Movements . . . . . . . . . . . . . . . 97

Convergent Eye Movements and Stereoscopic Vision . . . . . . . 97
Eye Movements and Reactions of the Pupils During Convergence 98
Interaction Among Innervation Mechanisms of the Various Eye Muscles
During Convergence . . . . . . . . . . . . . . . . . . . . . . . . . 100

Chapter VI. Eye Movements and Higher Cortical Functions 109

Eye Movements and Cortical Unit Activity . . . . . . . 109
Eye Movements and Local Cerebral Blood Flow . . . . 114
Eye Movements and the "Constancy" of Visual Perception 141

Conclusion 163

References 171

Index 185
 CHAPTER I

The Structural and Functional

Organization of the Innervation
Mechanisms of the Eye
Muscles

The innervation mechanisms of the eye muscles have a multilevel organiz~tion

and numerous connections with the visual and other afferent systems. Most
information on the innervation of the eye muscles has been obtained as a result
of clinical observations and experiments involving destruction or stimulation of
different parts of the brain.

Peripheral Innervation of the Eye Muscles

The eye muscles receive their efferent innervation from the 3rd, 4th, and
6th pairs of cranial nerves, as well as from sympathetic fibers running from the
superior cervical sympathetic ganglion.
The external ocular muscles are composed of separate fibers that in man
vary in diameter from 10 to 50 J.UIl. The thinnest fibers are found at the
periphery of the muscle, where they are about one-quarter as thick as the fibers
in the center of the muscle (Voss, 1957). The thin muscle fibers are rich in
sarcoplasm and are of the "red" type, whereas the thick fibers contain less
sarcoplasm and are ofthe "white" type.
The functional elements of the eye muscles are motor units. Each motor
unit consists of a motoneuron in the nucleus of a cranial nerve, a nerve fiber or
axon running from the motoneuron, and a group of muscle fibers innervated by
1
2 CHAPI'ER ONE

this axon. The system of the single motor unit of the eye muscles includes from
2 to 4 muscle fibers (in skeletal muscle, there are about 50-125 muscle fibers
for every nerve fiber).
Continuous rhythmic electrical discharges, with a frequency considerably
higher than in skeletal muscles, arise in the motor units of the eye muscles. In
cats and dogs, the frequency of these discharges in the motor units of the eye
muscles may reach 160/sec (Reid, 1949); in man, they may reach 200/sec (Bjork
and Kugelberg, 1953). The unit activity of the motoneuron of the eye muscles is
characterized not only by a very high frequency, but also by instability
(Tokizane and ShimaZu, 1964), the reason for which is evidently the absence of
recurrent collaterals and of postsynaptic inhibition through Renshaw cells
(Sasaki, 1967). Among the factors participating in the stabilization of the firing
rate of motoneurons of the eye muscles, the role of posthyperpolarization,
fusimotor control, and cortical influences must be taken into consideration
(Tokizane and Shimazu, 1964; Kernell, 1968).
Nerve endings in muscle fibers differ in their histological structure (Wolter,
1955). In thick muscle fibers, there are characteristically long, branching nerve
endings with an end plate. These endings characteristically have thin, un-
myelinated nerve fibers, forming an arch near the end plate. Thick muscle fibers
have unmyelinated nerve endings forming a network in the sarcoplasm. No end
plates are found in the thin muscle fibers, but only unmyelinated nerve endings.
Destruction of the ciliary ganglion leads to partial degeneration of the extra-
ocular muscles, but stimulation of the ciliary ganglion leads to contraction of
these muscles (Armaly, 1959).
The cranial nerves, as they run to the eye muscles, consist of nerve fibers
of different thicknesses, but most are thick (11-17 Jim) or thin (2-6 JIm)
(Donaldson, 1960). The thick fibers evidently innervate the extrafusual muscle
fibers, whereas the thin nerve fibers run to the intrafusal fibers in the muscle
spindles; i.e., they belong to the group of r-efferent fibers.
The cells from which nerve fibers run to the muscles of the eyeballs and
lids form the nuclei of the 3rd, 4th, 6th, and 7th cranial nerves. The nuclei of
the oculomotor nerves have the most complex structure of all. Opinions differ
regarding the functional organization of these nuclei. By the use of a stereotactic
method, Szentagothai {1942), in cats and dogs, and Bender and Weinstein
(1943), in monkeys, stimulated different parts of the nucleus of the 3rd cranial
nerve electrically. These workers found that groups of cells connected with the
individual ipsilateral eye muscles are arranged in the following order in the
dorsoventral direction: m. sphincter pupillae, m. rectus inferior, m. ciliaris, m.
obliquus inferior, m. rectus medialis, m. rectus superior, and m. levator
palpebrae. Warwick (1953), however, in a study of chromatolysis of the nerve
cells of monkeys after division of nerve fibers running to the various eye
muscles, found that m. rectus superior is connected with cells located in the
INNERVATION MECHANISMS OF THE EYE MUSCLE 3

nucleus of the contralateral oculomotor nerve. The innervation of m. levator

palpebrae on both sides arises entirely from a single unpaired nucleus located in
the midline of the caudal part of the nuclei of the oculomotor nerves. According
to Warwick (1953), Perlia's nucleus is very poorly developed in the chimpanzee
and in man. It has efferent connections only with m. rectus superior and m.
obliquus inferior. There is thus no reason to suppose that this nucleus
participates in the mechanism of convergence of the eyes.
The conflicting information on the functional organization of the nuclei of
the 3rd cranial nerve can evidently be attributed to the inadequate number of
investigations and the imperfections of the methods used, making further
research in this direction well worthwhile (Tarlov, 1971). The structural and
functional organization of the nucleus of the oculomotor nerve in man, however,
is the least-studied problem of all. The most detailed information on this
question is given in the paper by Putsillo (1970), which is based on three
combined clinical and anatomic observations. In these cases, the cause of the
paresis and paralysis of the ocular muscles was either compression of the
oculomotor nerves, leading to retrograde degeneration of the nerve cells, or a
disturbance of the blood supply, with hemorrhages and ischemic injury to the
nerve cells. In continuous series of 20-J.lIll sections, measurements were made on
every 20th section. In this way, the number of intact and degenerating cells in
the principal nucleus of the oculomotor nerve was determined. These investiga-
tions showed that the muscle raising the upper lid is innervated by cells in the
caudal portion of the oculomotor nucleus, m. rectus inferior is innervated by
cells at the junction between the caudal and middle third of the nucleus, and m.
rectus medialis is innervated by cells in the oral part of the nucleus. Fibers in the
root of the principal nucleus of the oculomotor nerves originating in the oral
part of the nucleus do not cross to the other side. There is no complete
decussation of fibers arising in the caudal and middle parts of the nucleus. No
more than 26% of fibers decussate in the caudal part.

Supranuclear Innervation Mechanisms of the Eye Muscles

The regulatory mechanisms of the eye muscles are organized at many
different levels. Unlike the nuclei of the cranial nerves (the 3rd, 4th, and 6th
pairs), the supranuclear mechanisms control coordinated movements of both
eyes, not single muscles of one eye. The anatomical delineation of structural
formations participating in the control of horizontal and vertical fixation, the
act of convergence, and the pupillary reflexes is quite distinct in the brainstem.
The existence of these supranuclear brainstem control mechanisms is familiar to
clinicians: in lesions of the brainstem, vertical movements and convergence are
disturbed, whereas in lesions of the pons, horizontal movements are disturbed.
There are indications that the nuclei of the abducens nerve participate in
4 CHAPTER ONE

the control of horizontal movement of the fixation axis (Gagel, 1941). The cell
composition of these nuclei is not sufficiently well developed, however, to
produce complex combined movements of both eyes (Marburg, 1911). De-
generation of the nuclei of the 6th nerve is not accompanied by degeneration of
the nuclei of the 3rd nerve, and it does not lead to a disturbance of movement of
the other eye (Siemerling, 1888). In the opinion of Crosby (1953), horizontal
movement of the fixation axis is associated with the nucleus paraabducens. This
nucleus contains small associative cells of the reticular formation that lie in the
immediate vicinity of and among cells of the nucleus of the abducens nerve. The
shortest processes of these cells terminate in synapses near cells of the nucleus of
the abducens nerve, whereas their long processes cross the midline of the
brainstem and end in synapses on cells of the nucleus of the contralateral
oculomotor nerve. These fibers run in the posterior longitudinal bundle, which
also has extensive connections with the vestibular nuclei and the cervical
segments of the spinal cord, exerting vestibular and cervicotonic effects on the
oculomotor system. Carpenter and MacMasters (1963), after dividing various
parts of the posterior longitudinal bundle in monkeys, studied ascending
degeneration of its fibers and compared their findings with the oculomotor
disturbances. They concluded from their investigations that partial decussation
of the ascending fibers of the posterior longitudinal bundle occurs O••lY at the
level of the nuclei of the abducens nerves.
The posterior longitudinal bundle is one of the oldest tracts of the CNS,
and one of the first to become myelinated during embryogenesis. The physio-
logical role of the posterior longitudinal bundle is to coordinate the combined
activity of the various ocular muscles, and also to correlate eye movements with
movements of the head and trunk. It is therefore difficult to imagine that the
posterior longitudinal bundle would also participate in the regulation of
horizontal fixation.
The attempt to link the control of horizontal fixation with the vestibular
nuclei also has little foundation. Spiegel (1933) found that after destruction of
the vestibular nuclei, horizontal eye movements arising in response to stimula-
tion of the cortical optomotor areas are absent. These findings by themselves,
however, are insufficient to prove a role of the vestibular nuclei in the control of
horizontal fixation.
Any form of pathology in the sensory system can considerably modify the
character of motor responses evoked by cortical stimulation. For example, limb
movements in response to cortical stimulation can be eliminated by sectioning the
vestibular nerve (Kempinsky and Ward, 1950). Attempts to explain the mechan-
ism of horizontal fixation by the function of one particular localized cell group
(nucleus of the abducens nerve or vestibular nucleus, or the nucleus para-
abducens) thus rest on an insecure basis.
Sounder views are held by Bender and Shanzer (1964), who deny the
INNERVATION MECHANISMS OF THE EYE MUSCLE s
existence of any specialized centers for the control of horizontal ftxation in the
brainstem. These workers observed horizontal movements of the eyes in
monkeys in response to stimulation of a wide area in the middle part of the
tegmentum of the brainstem, corresponding to the position of the reticular
formation. These eye movements are one of the ftrst components of the
complex behavioral arousal reaction, which is reflected in the EEG (Magoun,
1954). Stimulation of the reticular formation below the level of the nuclei of the
3rd nerve gives rise to movement ofthe eyes toward the side of stimulation, but
stimulation of parts of the brainstem rostrally to the nuclei of the 3rd nerve
gives rise to movements toward the opposite side. These fmdings indicate
opposite effects of the oral and caudal regions of the brainstem on horizontal
ftxation. The same results are obtained by experimental application of strych-
nine to different parts of the brainstem (Hyde, 1959a,b). If a small area of the
superior colliculus in the anesthetized cat is stimulated by strychnine, the
eyeballs respond to light by rotating toward the opposite side, whereas during
stimulation of the medial areas of the medullary reticular formation, the eyes
respond to light by turning toward the same side. During simultaneous
stimulation of the medullary reticular formation and the superior colliculus,
three types of responses can be observed: (1) the eyes remain in the midposition;
(2) the eyes make oscillatory movements between the two. extreme positions;
(3) the eyes turn toward one side. These fmdings suggest that the reticular
formation of the medial areas of the medulla and the superior colliculus on the
same side act antagonistically toward each other. Horizontal eye movements
arising in response to stimulation of one superior colliculus are effected with the
aid of the medial areas of the reticular formation in the contralateral tegmentum
rhombencephali. Local destruction of these areas of the reticular formation on
one side makes turning of the eyes to this side in response to stimulation of the
contralateral superior colliculus impossible. At the same time, in a lesion in the
same situation (medial areas of the reticular formation of the tegmentum
rhombencephali), horizontal eye movements toward the side of the focus can be
evoked by stimulation of the contralateral occipital lobe. These movements are
absent, however, in the case of local destruction of the medulla slightly orally
and laterally to that in the case described above.
These observations conftrm the absence of any strictly localized "center"
for horizontal ftxation in the brainstem. Different parts of the brainstem
participate in the mechanism of different types of horizontal eye movement.
According to Hyde (1964), there is no single localized area in the brainstem of
the cat destruction of which would abolish all types of horizontal eye
movements. Hyde (1964) made motion pictures of the movements of the
eyeballs during stimulation of a speciftc site in the brainstem and found that the
eyeballs pointed in the same ftxed direction regardless of their original position.
This movement of the ftxation axis in a deftnite direction is observed only
6 CHAPTER ONE

in waking animals (encephale isaie preparation). In anesthetized animals, the

eyeballs assume the same mid position in response to stimulation of different
sites in the reticular formation (Bender, 1955). It can be concluded from a
comparison of the results obtained by Bender and by Hyde that anesthesia
blocks some part of the complex integrative mechanism that is responsible for a
change in the direction of fIxation. During anesthesia, movements of the eyeballs
become less highly differentiated, and in response to stimulation of different
areas of the reticular formation, the eyeballs move to the same midposition.
Saccadic eye movements arise in monkeys in response to stimulation of
the paramedian zones of the reticular formation of the pons (Cohen, 1971;
Cohen and Henn, 1972a,b; Cohen and Kornatsuzaki, 1972). In contrast,
according to the observations of Westheimer and Blair (1973a), electrical
stimulation of certain areas of the brainstem (pretectal area, the pons ventral to
the medial longitudinal bundle close to the midline) leads to inhibition of
saccadic eye movements. In the opinion of these workers, this inhibition is
brought about by interaction between the stimulating pulses and impulses
circulating in certain neuronal orbits, which cause the appearance of saccadic eye
movements. The experiments of Westheimer and Blair suggest that these
neuronal orbits are located in the brainstem in the region of the pretectal area
and the ventromedial areas of the pons.
It is interesting to note that in these experiments, electrical stimulation
had a selective action on saccadic eye movements, and did not affect fIxation,
tracking, or convergent movements. These results indicate that different types of
eye movements have different representations in the brainstem. Further evidence
in support of differential representation of different types of eye movements in
the brainstem is given by the results of neuronographic studies. Sparks and Sides
(1974) found a varied relationship between unit activity in the reticular
formation of the brainstem in monkeys and their eye movements. In some
neurons, a burst of spikes appeared during saccadic eye movements (usually
10-15 msec before the beginning of the saccades). Other neurons were charac-
terized by reduced activity during saccades. In addition, neurons with a fIring
pattern that depended on the position of the eyes and varied during smooth
tracking movements were found. Neurons with a fIring pattern that depended on
both smooth and saccadic eye movements were found close to the nucleus of the
abducens nerve. It is considered that this region is the site of convergence of
tonic and phasic influences on the motoneurons of the ocular muscles.
Paramedian neurons of the brainstem reticular formation are the generator of
rapid eye movements. Neurons connected with the function of attention,
suggesting that they may be concerned with the choice of the visual target, have
been found in the same region. In the investigations of Keller (1974), different
types of neurons were also found when the unit activity was recorded in the
medial areas of the pontine reticular formation: neurons that gave bursts of
INNERVA'DON MECHANISMS OF mE EYE MUSCLE 7

activity during saccadic eye movements, neurons the activity of which was
inhibited during saccadic movements, and tonic neurons the activity of which
depended on the position of the axis of the eye during fixation. According to
Cohen and Henn (1 972a,b ), changes in activity of neurons of the reticular
formation situated close to the oculomotor neurons precede the appearance of
the saccade by 12-20 msec. Similar changes in unit activity appeared before
saccades, and also before the fast phase of vestibular and optokinetic nystagmus.
As a result of electrophysiological investigations in cats (Highstein et al., 1974),
it was found that neurons of the pontine reticular formation are connected
monosynaptically with the motoneurons of the oculomotor nerve.
In contrast to this wide zone of localization of the mechanism of
horizontal fixation, the mechanism controlling the direction of vertical eye
movements in the midbrain is localized. The reason for this difference in the
extent of representation of the mechanisms of horizontal and vertical fixation in
the brainstem is evidently the different functional roles of horizontal and
vertical eye movements in the visual perception of space. Horizontal eye
movements are exceptionally important for orientation in surrounding space, for
fusion, for stereoscopic vision, and so on. Vertical eye movements playa much
less important role in the behavioral responses of the organism.
Paralysis of vertical movement of the eyes is a major clinical sign of a
lesion of the midbrain. Paralysis of upward and downward movements of the
eyes can be observed separately, evidence of the anatomic separation of the
corresponding mechanisms. Experiments with electrical stimulation of the
superior colliculi of animals give results indicating the existence of separate
mechanisms for upward and downward eye movements. Stimulation of super-
ficial areas of the superior colliculi gives rise to upward movements of the eyes,
but shifting the electrodes toward the gray matter of the aqueduct of Sylvius
causes the electrical stimulation to evoke a downward movement of the eyes
(Spiegel and Scala, 1937). Among the various formations of the superior colliculi
that participate in the regulation of vertical fixation, the nuclei of Cajal and
Darkshevich have a particularly important role (Szentagothai, 1950a).
Interaction of a complex nature between the systems controlling vertical
and horizontal fixation has been found by the study of eye movements during
the transition from sleep to wakefulness. Arduini et al. (l974a,b), in experi-
ments on cats (encephale isole) in darkness, recorded the eye movements during
sleep and wakefulness. Sleep was characterized by slow (on the average, less than
1° /sec) and high-amplitude (2_5°) movement without any precise orientation
(although the vertical components predominated). During wakefulness, on the
other hand, the eye movements were characterized by rapidity (3-15° /sec) and
low amplitude (less than 1°), with predominance of the horizontal component.
Some particularly important results were obtained in a study of correlation
between eye movements and neurons of the superior colliculus. During the slow
8 CHAPTER ONE

phase of sleep, when the rapidity of the eye movements was less than 1.5° /sec,
unit activity did not correlate with the eye movements. In the intermediate state
between sleep and waking, when the rapidity of the eye movements reached
3-20° /sec, but fixation was not precisely oriented, bursts of unit activity
appeared in response to a change in any direction. These bursts preceded the eye
movement by a few to a hundred milliseconds. In the waking state, when the
direction of the eye movements was more precise and predominantly horizontal,
changes in unit activity became selective in relation to their direction (strength-
ened in one direction and inhibited in the other). According to Robinson
(1972), electrical stimulation of an area of the superior colliculi in waking
monkeys evoked saccadic eye movements. The saccades were independent of the
preceding position of the eyes, the parameters of the stimulus, and the depth of
insertion of the electrode into the colliculus. As the site of stimulation moved
caudally, the amplitude of the saccades increased. Neuronographic studies have
shown that the superior colliculi are connected with eye movements, but not
with head movements, nor are they related to the integration of eye and head
movements (Robinson and Jarvis, 1974). An important role in this integration is
evidently played by the nucleus prepositus hypoglossi. In the experiments of
Baker and Berthoz (1975) on anesthetized, immobilized cats, many neurons of
the nucleus prepositus were shown to respond by short-latency (less than
2 msec) EPSPs and IPSPs to stimulation of the vestibular nerves (ipsilateral
inhibition and contralateral excitation), and also to stimulation of the cerebel-
lum and nuclei connected with oculomotor function. During stimulation of all
these structures, antidromic responses were also recorded in the nucleus
prepositus. Bilateral connections of the nucleus prepositus with the vestibular
system and oculomotor complex revealed by these experiments suggest that this
nucleus is concerned with the organization of the dependence of eye movements
on the position of the head.
The supranuclear mechanism of convergence is located in the midbrain.
Paralysis of convergence arises in lesions of the midbrain. There are indications
that the unpaired Perlia's nucleus, which is located between the nuclei of the
oculomotor nerve, participates in the control of the act of convergence. This
nucleus develops in phylogeny Simultaneously with the appearance of a function
of convergence; however, no reliable proof of the connection between this
nucleus and the mechanism of convergence has yet been obtained. According to
the observations of Spiegel et al. (1964), Forel's field participates in the control
of convergence. If this field is stimulated during stereotactic operations for
parkiIisonism, two types of eye movements arise: (1) a monocular effect of
adduction of the ipsilateral eye (sometimes combined with its movement upward
or downward); (2) a binocular effect - convergent eye movements, sometimes
with a vertical component (upward or downward).
Higher levels of mechanisms for the control of eye movements are located
INNERVADON MECHANISMS OF THE EYE MUSCLE 9

in the basal ganglia, simulation of which causes the eyes to turn to the side
(Rioch and Brenner, 1938). The most detailed investigation of the eye move-
ments during stimulation of the basal ganglia and white matter of the cerebral
hemispheres in monkeys was undertaken by Wagman (1964), who showed that
eye movements to the opposite side arise during stimulation of the thalamus.
Eye movements also arise during stimulation of the white matter in the region of
the internal capsule and corpus callosum. Evidence of the role of the basal
ganglia in the control of eye movements is also given by clinical observation and
the results of stereotactic operations. For example, in patients with parkin-
sonism and with a lesion of the basal ganglia, oculogyric crises and limitation of
upward movement of the eyes are observed. Bipolar stimulation of the
inferomedial part of the medial nucleus of the thalamus during stereotactic
operations evokes horizontal nystagmus directed toward the side of stimulation
(Hassler, 1957, 1959).
According to Schlag et al., (1974), neurons of the intralaminar region of
the thalamus in cats have a firing pattern that correlates with saccades. Most
commonly, a burst of spikes precedes the saccade. The duration of the saccades
depends on the duration of the burst of spike activity. In the nonspecific nuclei
of the cat thalamus, changes in unit activity preceded the appearance of a
saccade by 50-150 msec; these changes in unit activity could arise in darkness
(Schlag et al., 1973). According to Kirkham and Kamin (1974), saccadic eye
movements are grossly disturbed in patients with Wilson's disease. These
disturbances are evidently due to damage to the descending frontobulbar system
controlling saccadic eye movements. Pathology of the nucleus caudatus in
Wilson's disease may also play a role in disturbances of descending polysynaptic
connections.
Mechanisms of regulation of eye movements are also located in the
cerebral cortex: destruction of certain areas in the frontal and occipital lobes
may lead to rotation of the eyes to the side of the focus, stimulation of these
same areas, to rotation of the eyes to the opposite side. Rasmussen and Penfield
(1947) observed eye movements toward the opposite side when they stimulated
the precentral gyrus in the area between the motor representation of the thumb
and the upper part of the face, as well as adjacent zones of the frontal gyri.
There are extensive regions of the cortex stimulation of which elicits eye
movements. lilly (1958) found that movements arise in response to stimulation
of 34% of the surface area of the cerebral cortex, an area exceeded only by the
regions that on stimulation evoke movement of the upper limb (37%). The
extensive representation of mechanisms controlling eye movements in the
cerebral cortex is not surprising, considering the important role of these
movements in the diverse behavioral responses of man and animals: eye
movements are one of the first manifestations of orienting and defensive
reflexes, and they participate in the arousal reaction and in the establishment of
10 CHAPrERONE

posture. It is therefore not surprising that during stimulation of the cortex, eye
movements are usually accompanied by rotation of the head, and if the stimulus
is strong enough, by rotation of the whole trunk. If the animal's head is held in a
fixed position, however, isolated movement of the eyes can be produced. The
character of the eye movements depends largely on the intensity of stimulation
and the degree of anesthesia.
Stimulation of each part of the cortex is characterized by eye movements
in a specific direction. In the occipital optomotor area, there is a definite
connection between the part of the visual field projected into that area of the
cortex and the direction of the eye movements evoked by stimulation of that
area. For example, the lower parts of the visual field are represented in the
superior lip of the calcarine fissure. Stimulation of this cortical area evokes
movement of the eyes downward and to the opposite side. The vertical
component of the eye movements during stimulation of areas 18 and 19 differs
in direction. The threshold of electrical stimulation of area 17 to evoke
movement of the eyes is much lower than the threshold of area 18, even though
motor cells giving rise to descending fibers to the brainstem mechanisms of
fixation are located in both areas (Walker and Weaver, 1940). During stimulation
of the occipital lobe, however, deviation of the eyes to the opposite side does
not always occur. Sometimes the eyes move toward the side of stimulation
(Penfield and Rasmussen, 1950). This bilateral representation of the mechanisms
of eye movement in the occipital lobe may playa role in the compensation of
paresis of fixation in patients with unilateral lesions of the occipital lobe.
An area of the cortex located in the posterior part of the second frontal
gyrus (area 8) also participates in the regulation of eye movements. Stimulation
of this area causes the eyes to turn to the opposite side and the palpebral fissure
to dilate (Foerster, 1924; T. Brown and Graham, 1927). The frontal optomotor
area apparently consists of two branches, at an angle to each other. These two
branches of the frontal optomotor area are not functionally synonymous. If the
lateral rectus muscle of the right eye and the medial rectus muscle of the left eye
are divided, the eyes will turn to the left because of the tonus of the antagonist.
Sherrington (1893) showed that stimulation of the left frontal optomotor area
in such an animal leads to rotation of the eyes to the right as far as the midline,
by lowering the tonus of the antagonist. According to Crosby (1953), however,
this return of the eyes to the midposition takes place in response to stimulation
only of the lower part of the frontal optomotor area. The two parts of the
frontal optomotor area (superior and inferior) thus differ in their effect on
reciprocal relationships of the eye muscles. The superior portion excites the
ocular agonist muscles; the inferior inhibits the antagonist muscles. Impulses
from both parts of the frontal optomotor area evidently run along different
pathways. After destruction of the occipital lobe, deviation of the eyes to the
opposite side can be evoked by stimulation only of the superior parts of the
INNERVATION MECHANISMS OF TIlE EYE MUSCLE 11

frontal optomotor area. These experiments show that the inhibitory effect of
the inferior part of the frontal optomotor area on the eye muscles takes place
through the participat!on of the ipsilateral occipital optomotor area, and they
indicate the exceptionally complex character of the supranuclear influences on
reciprocal relationships of the eye muscles. Bilateral stimulation of the frontal
optomotor areas can produce vertical movement of the eyes if the parts of the
optomotor areas stimulated in this case are those the isolated stimulation of
which causes the eyes to tum to the opposite side and upward.
The topographical arrangement of the frontal optomotor area in man and
the monkey is different, evidently because of the development of the speech
area in man in the posterior areas of the inferior frontal gyrus. Cytoarchitectoni-
cally, area 8 differs considerably from the motor area (area 6), which is situated
posteriorly to it, in having an inner layer of granules, and it differs from the
association area (area 9), which is located anteriorly to it and contains granular
cells, by the less well developed outer and inner layers of granules (Bailey and
Bonin, 1951). In response to stimulation of area 6, the head rotates to the
opposite side.
Eye movements produced by stimulation of the occipital optomotor area
have a longer latent period, and they are slower and less regular than those
produced by stimulation of frontal mechanisms (T. Brown and Graham, 1927).
If electrical stimulation of equal intensity is applied simultaneously to the region
of the frontal optomotor area on one side and the occipital optomotor area on
the other, the eyes will tum to the side opposite the frontal optomotor area.
These experiments indicate that the frontal optomotor area has a more
important role in the regulation of eye movements (Berger, 1901). The frontal
optomotor areas in each hemisphere are not connected, for stimulation of one
has no appreciable effect on the excitability of the corresponding area on the
opposite side.
The occipital optomotor areas evidently have an inhibitory action on each
other. Application of cocaine to one increases the excitability of the occipital
optomotor area on the opposite side, whereas stimulation lowers it (Oaes,
1939). Commissural fibers connecting the two occipital optomotor areas run in
the posterior parts of the corpus callosum (Cords, 1926).
On the basis of his clinical investigations, Daroff (1970) concluded that
the frontal optomotor area controls horizontal saccadic eye movements to the
opposite side. At the same time, the occipital optomotor area on the same side
participates in the control of tracking movements of the eyes: in lesions of the
posterior parts of the hemispheres, tracking movements of the eyes are disturbed
on the side ofthe focus.
The cortical mechanisms of fixation are connected with the subcortical
system of efferent fibers. The medial corticotectal tract from the occipital
optomotor area runs toward the corpora quadrigemina. Nerve fibers forming this
12 CHAPTER ONE

tract begin in ganglion cells of the 4th cortical layer and single cells of the 6th
layer (Clark, 1942). These fibers are thinner, and they are covered with a myelin
sheath later during embryogenesis, than the fibers of the optic radiation
(Flechsig, 1920). This tract divides into two sets of fibers - occipital and
preoccipital, corresponding to cortical areas 18 and 19, from which they
originate. The two sets of fibers of the medial corticotectal tract are parallel to
the optic radiation, but situated medially to it, and they run into the posterior
limb of the internal capsule. Fibers running from the superior part of area 19
and the inferior part of area 18 terminate in the oral and medial part of the
superior colliculi. Fibers from the inferior part of area 19 and superior part of
area 18 run toward the lateral and caudal part of the superior colliculi (Clark,
1942; Crosby and Henderson, 1948). Descending fibers from the occipital opto-
motor area run not only to the superior colliculi, but also to the nuclei of
Darkshevich and to the interstitial and oculomotor nuclei (Mettler, 1964).
Unfortunately, Mettler's investigations do not answer the question whether
descending fibers terminate on the motoneurons of the eye muscles in the
nucleus of the oculomotor nerve or on interneurons located in the same nucleus.
Descending fibers running from the occipital optomotor area also terminate in
the thalamus and pons (Muskens, 1937; Polyak, 1941; Sunderland, 1940).
Efferent fibers from the frontal optomotor area run in the anterior limb of
the internal capsule and terminate in the thalamus and mesencephalon (Crosby
et al., 1952) and the pons (Hirasawa and Kato, 1935). Brucher (1966) found
that the frontobulbar pathways of the oculomotor system run in the anterior
limb of the internal capsule, cross the ventrolateral surface of the thalamus
through the zona incerta and Forel's field, and reach the pontine paramedian
reticular formation. Descending fibers running from the frontal optomotor area
thus terminate in the same parts of the brainstem as fibers from the occipital
optomotor area. The functional role of these two descending pathways is
evidently different, however, for after division of the brainstem above the nuclei
of the abducens nerve, horizontal eye movements can be evoked only by
stimulation of the occipital optomotor area, not by stimulation of the frontal
optomotor area (Claes, 1939). Destruction of the corpora quadrigemina prevents
horizontal eye movements evoked by stimulation of the occipital optomotor
area, whereas the corresponding eye movements produced by stimulation of the
frontal optomotor area remain intact (Scala and Spiegel, 1938). The superior
colliculi receive impulses chiefly from the occipital optomotor areas, and the
mechanisms of horizontal fixation in the pons receive impulses chiefly from the
frontal optomotor areas.
The necessity for combined function of the optomotor areas of the right
and left hemispheres is manifested particularly clearly when vertical eye
movements are studied. Pasik et al. (1967) studied vertical optokinetic nystag-
mus in monkeys to discover the role of interhemispheric connections in the
INNERVATION MECHANISMS OF THE EYE MUSCLE 13

control of vertical eye movements. Division of one optic tract or transection of

the chiasma combined with covering one eye had no appreciable effect on
vertical optokinetic nystagmus. At the same time, division of the corpus
callosum and hippocampal commissure reduced the frequency of optokinetic
nystagmus, and changed its direction from strictly vertical to oblique (toward
the side of the "deafferented" hemisphere). Additional division of the anterior,
posterior, habenula, and intercollicular commissures, and also of the massa
intermedia, caused almost total suppression of optokinetic nystagmus in the
upward direction, and greatly weakened it downward. These findings indicate
the need for functional connection between the two hemispheres for vertical eye
movements. Disturbance of vertical optokinetic nystagmus after division of the
subcortical commissures, even in the case of binocular stimulation of chiasma to-
mized animals, is evidence that this division affects the oculomotor "output"
more than the optic "input" of optokinetic nystagmus.
Special attention must be paid to the role of the cerebellum in the control
of eye movements. The effect of the cerebellum on the eye muscles is not so
cleady manifested as its effect on the muscles of the limbs and trunk. The
cerebellum may have a direct influence on eye movements, and may also modify
vestibulooculomotor reflexes, depending on anatomic connections between the
cerebellum and the vestibular nuclei (Dow, 1936, 1938). Despite the existence
of such connections, the unit activity of motoneurons of the ocular muscles is
unchanged after removal of the cerebellum (Westheimer and Blair, 1973b).
The role of the cerebellar cortex in the regulation of eye movement has
been demonstrated by numerous experiments involving electrical stimulation,
starting with those of Hitzig (1874). Among the most recent investigations in this
direction, those of Ron and Robinson (1973) merit particular attention; these
workers found a defmite pattern of somatotopic representation of eye move-
ments ill the cerebellar cortex (crura I and II, lobulus simplex, flocculus).
Evidence of the role of the cerebellar cortex in the regulation of eye movements
is also given by the results of studies of unit activity. Neurons increasing their
rate of discharge and the appearance of spike activity during sleep with fast eye
movements, but without synchronous connection with the eye movements, have
been found in the cerebellar cortex of cats (Haday et ai., 1974). Neurons of
another type (Purkinje cells) had spike activity that was synchronous with fast
eye movements. In the waking state, the activity of one-third of neurons changes
to correspond to the fast eye movement. The flocculus of the cerebellar cortex
plays a special role in visual influences on vestibulooculomotor reflexes.
Destruction of the flocculus depresses or completely abolishes visual inhibition
of vestibulooculomotor reflexes in rabbits (Ito et ai., 1974) and monkeys
(Takemori and Cohen, 1974). Experiments involving electrical stimulation of the
flocculus and semicircular canals in rabbits showed that the vestibulooculomotor
reflexes arising during stimulation of each semicircular canal are dependent to
14 CHAPTER ONE

different degrees on the cerebellum (Ito et ai., 1973). By recording the unit
activity of the Purkinje cells in the flocculus in waking monkeys, it was shown
that this activity depends on vestibular stimulation when the monkey actively
inhibits the vestibulooculomotor reflexes, but does not so depend when the
monkey performs normal compensatory mo~ments of the eyes in darkness.
These findings also support the hypothesis that the flocculus participates in
visual suppression of vestibulooculomotor reflexes (Usberger and Fuchs, 1974).
A lesion of the cerebellar cortex leads to dysmetria (usually hypometria) of the
fast saccadic eye movements (Komhuber. 1971). Instead of a large saccade,
several small saccades appear; on the basis of this finding, it was postulated that
the programming of the fast ballistic eye movements was disturbed. In unilateral
injuries to the cerebellum, the dysmetria is ipsilateraL The cerebellar cortex
evidently participates in determining the temporal parameters of saccadIC eye
movements. Not only saccades, but also other movements programmed before-
hand, are disturbed in lesions ~f the cerebellar cortex. They include speech,
writing. piano-playing, and so on.
An interesting hypothesis on the mechanisms of regulation of the spatio-
temporal characteristics of eye movements by special "holding lines" in the
cerebellar cortex has been put forward by Kornhuber (l973). According to this
hypotheSiS, axons of the granule cells of the stratum granulosum of the
cerebellar cortex form parallel fibers that make contact with the Purkinje cells
and that differ in length and diameter and, consequently, in conduction velocity.
The conduction time during which the motor potential spreads along the parallel
flbers depends on the length and conduction velocity, with the result that the
Purkinje cells are excited one after another. Ifaxons of a number of Purkinje
cells converge on one neuron of the cerebellar cortex (or vestibular nucleus), the
unit activity of that neuron will continue throughout the period of spread of the
motor potential along the parallel fibers formed by axons of the granule cells. In
metabolic disturbances, the long parallel fibers are the first to undergo atrophy,
and for that reason, the large saccadic movements of the eyes are the first to
disappear. The cerebral cortex is connected with the granule cells of the stratum
granulosum of the cerebellar cortex for movements of the upper limb through
the nuclei of the pons, and for saccadic eye movements, through the corpora
quadrigemioa. Neurons the activity of which anticipates saccades of a certain
amplitude and direction, but is unconnected with saccades of greater or lesser
amplitude, have been found in the deep layers of the corpora quadrigemioa
(Wurtz, 1969). These neurons, which evidently conduct information from the
cerebral cortex, do not themselves participate in the organization of spatio-
temporal relations, for their bursts do not correspond in duration to the saccadic
movements of the eyes.
The cerebellar cortex behaves as a "clock" determining the time required
for fast, previously programmed movements, the temporal characteristics of
INNERVATION MECHANISMS OF THE EYE MUSCLE IS

which must have been predetermined (Kornhuber, 1973). Such a clock is

essential not only for the preliminary programming of every simple movement,
but also for its successful performance. The rapid interchange of fast movements
takes place during piano-playing, speech, and so on. All these movements are
disturbed in lesions of the cerebellum. Disturbance of the programming of fast
movements leads to dysmetria and to inability to begin succeeding simple
movements after the end of a preceding movement, as is the case in adiadocho-
kinesis, one of the main symptoms of a lesion of the cerebellar cortex. The
Purkinje cells, which are the only output for the cerebellar cortex, inhibit
neurons of the cerebellar and vestibular nuclei monosynaptically (Ito and
Yoshida, 1964). This phenomenon is evidently linked with the fact that before a
movement can begin, the stabilizing function of the phylogenetically oldest part
of the cerebellar nuclei must be inhibited. The function of regulating fast
movements has been taken over by the archicerebellar cortex, which has begun
to inhibit the function of position stabilization and to program fast movements.
The function of stabiliZing the position of the eyes is evidently performed by the
n. emboliformis, n. globosus, n. dentatus, and n. interpositus: coagulation of n.
interpositus and the medial part of n. dentatus leads to ipsilateral paralysis of
fixation in man (Nashold et al., 1969). According to Kornhuber (1973), the
cerebellar cortex is concerned mainly with the programming of fast saccadic eye
movements, and the cerebellar nuclei with the stabilization of fixation.
The data of Kornhuber (1971) on the disturbance of saccadic eye
movements in lesions of the cerebellar cortex do not agree with the results of
work by Westheimer and Blair (1974). In these authors' experiments, the
removal of one cerebellar hemisphere in monkeys did not cause any disturbance
of saccadic eye movements. At the same time, steady fixation of an object
located on the side of the lesion became impossible, tracking an object moving
from the midline toward the side of the lesion was disturbed, the eye drifted
constantly toward the side opposite the lesion, especially in darkness, and
asymmetry of vestibular effects appeared. This syndrome was permanent in
adult monkeys and transient in young monkeys, which, even after complete
cerebellectomy, were able within a very short time to maintain fixation
eccentrically and to perform smooth tracking movements. In these workers'
opinion, after unilateral cerebellectomy, the drifting of the eyes toward the
opposite side depends on disturbance of the balance between bilateral influences
of the vestibular nuclei on the oculomotor system. Predominance of activity of
one of these nuclei leads to deviation of the eyes to the opposite side (Cogan,
1956), with the appearance of nystagmus, the fast phase of which is directed
ipsilaterally. Under normal conditions, each cerebellar hemisphere inhibits the
vestibular nucleus on its own side (Fukuda et al., 1972). Removal of one
cerebellar hemisphere abolishes this inhibition, and the tone of the ipsilateral
vestibular nucleus begins to predominate. Deviation of the eyes to the opposite
16 CHAPTER ONE

side then appears. In young monkeys, this effect diminishes during the week
after the operation, and has completely disappeared by the end of the second
week. Next follows a period of hypercompensation - drifting of the eyes in
darkness toward the side of the removed cerebellar hemisphere. A similar
situation is known to arise after destruction of the labyrinths (Bechterew, 1883).

Mferent Regulation of the Tonus of the Eye Muscles

A. Proprioceptors

The problem of the proprioceptors of the eye muscles and their role in the
regulation of eye movements as well as in the perception of space and in
stereoscopic vision has not yet been finally solved.
In ordinary laboratory animals, such as rabbits, cats, and dogs, there are no
muscle spindles in the eye muscles (Cilimbaris, 1910; S. Cooper and Daniel,
1949; S. Cooper and Fillenz, 1955). At the same time, the eye muscles of these
animals are equipped with sensory endings, impulses from which reach the
brainstem (Fillenz, 1955) and may inhibit responses in the reticular formation to
vestibular stimulation (Gernandt, 1968). Muscle spindles have been found in the
eye muscles of goats, monkeys, and man (S. Cooper et aI., 1951, 1954, 1955;
Greene and Jampel, 1966; Daniel, 1946; S. Cooper and Daniel, 1949; Merrillees
et aI., 1950; Voss, 1957). The eye muscles of goats contain many muscle
spindles (up to 120 in the inferior oblique; S. Cooper et aZ., 1951). In contrast,
each of the ocular muscles of the macaque contains not more than 6 muscle
spindles (Greene and Jampel, 1966). Each of the human ocular muscles contains
about 50 muscle spindles (Merrillees et aZ., 1950). The inferior rectus muscle has
the largest number of spindles, evidently in connection with the continuous
visual control exerted over actions performed by the hands. Muscle spindles in
the human eye muscles are distributed in the distal and proximal ends of the
muscle, never in the belly, where spindles are found in the limb muscles (S.
Cooper and Daniel, 1949).
if impulses are recorded in the afferent fiber from a muscle spindle, and
electrical stimulation is simultaneously applied to the motor nerve to the same
muscle, the same phenomena are observed as during the study of skeletal
muscles. During contraction of an ocular muscle, the firing rate in the afferent
fibers running from the muscle spindle decreases, whereas during relaxation of
the muscle, it increases. If, however, after isolation of the thin 'Y-efferent fibers,
only these fibers are stimulated, the firing rate in the afferent fibers running
from the muscle spindle increases sharply. The firing rate in afferent fibers from
tendon receptors increases during contraction of the muscle and decreases during
its relaxation.
INNERVATION MECHANISMS OF THE EYE MUSCLE 17

Mferent fibers from receptors of the ocular muscles run chiefly into the
trigeminal nerve. Some afferent fibers, however, join motor nerves (the 3rd, 4th,
and 6th pairs), and some leave these nerves in the region of the cavernous sinus
and join the trigeminal nerve (Stibbe, 1929). Manni et aZ. (1968), in investiga-
tions on pigs and sheep, found neurons in the Gasserian ganglion to which
afferent fibers run from muscle spindles in the extrinsic ocular muscles. In
investigations on cats, however, no responses to stretching the extrinsic ocular
muscles could be found in the same ganglion. Stretching the eye muscles of pigs
and sheep led to the appearance of responses in the sensory root of the
trigeminal nerve, running into the brainstem, whereas no such responses were
found in the oculomotor nerve. Division of the first (supraorbital) branch of the
trigeminal nerve abolished responses in the Gasserian ganglion to stretching of
the eye muscles. These workers concluded from their experiments that the
Gasserian ganglion contains neurons that give offaxons that run into the
brainstem. These same neurons are connected by fibers with the proprioceptors
of the eye muscles that run in the first (supraorbital) branch of the trigeminal
nerve. Afferent fibers running from the eye muscles terminate in the principal
sensory and mesencephalic nuclei, and also in the descending track of the
trigeminal nerve. During stretching of the eye muscles, electrical responses with a
short latent period (1-3 msec) are observed in these nuclei. Secondary neurons
and neurons of a higher order, connected with the proprioceptors of the eye
muscles, have been found in the deep layers of the superior colliculi, the
posterior commissure, and the superior cerebellar peduncle. Responses with a
longer latent period (20-200 msec) arise in these parts of the brainstem to
stretching of the eye muscles in goats (S. Cooper et aZ., 1951; Manni et aZ.,
1971). The problem of the connection between the motoneurons of the eye
muscles and the proprioceptors of the same muscles has not been finally solved.
According to Whitteridge (196O), in the decerebrate goat, stretching the superior
oblique muscle either has no appreciable effect on the motor units of the same
muscle or leads to a decrease in the discharge frequency by about 10%. The
discharge frequency in the same motor unit, however, is appreciably increased
during rotation of the animal's head. It can be concluded from these experi-
ments that there are no stretch reflexes in the ocular muscles of the goat. In
contrast, Matyushkin (1962) found stretch reflexes in the eye muscles of the
rabbit. The different results obtained by Whitteridge and Matyushkin evidently
depend on differences in the experimental conditions (anesthesia of the animal).
According to Breinin (1962), if the eyeball is removed and the eye muscles are
allowed to contract, the reciprocal bursts of spikes in them disappear. These
fmdings suggest that stretch reflexes are necessary for the normal operation of
the eye muscles. These reflexes are evidently important for the organization of
the reciprocal relationships among the eye muscles, which, in tum, also depend
on complex supranuclear influences (Crosby, 1953).
18 CHAPTER ONE

The functional role of proprioceptors can be studied not only by recording

the electrical activity of motor units, but also by assessing their effect on the
integral movement. Local anesthesia of the eye muscles has no effect on
vestibular nystagmus (Rademaker, 1955). Information from the eye muscles
does not reach consciousness. If, after instillation of decicaine, the eye is moved
with forceps, the subiect is unaware of the position of the eyes. If the eyeball is
Kept ill complete darkness, the subject does not know whether his attempt to
change the direction of fixation is successful or not (Brindley and Merton,
1960). The results of the psychophysiological investigations of Brindley and
Merton agree with electrophysiological data obtained by Keller and Robinson
(1971), who studied the unit activity in the nuclei of the abducens nerve in
unanesthetized monkeys. By use of a contact lens, the eyeball of the monkey
was rotated through 8-25". The lateral rectus muscle of the eye was shortened
or stretched by 1.3-4.1 mm in this process. During these investigations, no
changes occurred in the unit activity in the nucleus of the abducens nerve.
Stretching and shortening of the muscle likewise caused no change in the
number of active motoneurons. The bursts of spikes during saccadic eye
movements did not change their character if the eye was held with the contact
lens. These workers concluded from their observations that stretch reflexes are
absent in the extrinsic ocular muscles of monkeys.
Thus, despite the undisputed existence of a rich system of receptors in the
eye muscles, its functional role has not been finally elucidated.

B. The Visual System

Connections between the motor apparatus of the eyes and the visual
pathways occur at different levels of the nervous system - in the region of the
superior colliculus and in the occipital cortex. Visual fibers in the region of the
superior colliculus terminate chiefly in the stratum opticum, and partially in the
stratum griseum superficiale. The outer layer of the superior colliculus contains
cells with axons that run perpendicularly, cross the stratum opticum, and
terminate in synapses near cells located in the stratum griseum profundum.
These cells are large, and they give rise to the colliculooculomotor and
tectospinal tract. The projection of the visual field on the superior colliculus is
quite definite in character (Apter, 1945). The upper part of the visual field is
represented close to the midline of the superior colliculus, the lower part more
laterally. The horizontal meridian of the retina is represented in the superior
colliculus by a line running from front to back and a little medially. The fovea
centralis of the retina, which has greater representation than the other parts of
the retina, is represented in the superior areas of the superior colliculus.
Two-way connections between the visual and oculomotor mechanisms are
also found at the cortical level, where they are of a distinctive "mirror
INNERVATION MECHANISMS OF THE EYE MUSCLE 19

character." The superior sections of area 17 are connected by associative fibers

with the inferior section!; of area 19 (T. Brown et al .• 1922; Crosby and
Henderson, 1948; Thompson et al., 1950).
Interaction between visual and oculomotor mechanisms at the geniculate
body level likewise cannot be ruled out. Only 5% of neurons in the monkey
lateral geniculate body show changes in activity after the beginning of saccadic
eye movements (Buttner and Fuchs, 1973). In the nucleus pregeniculatus, 39 of
55 neurons showed correlation with saccades; changes in activity occurred
approximately 80 msec after the beginning of a saccade in darkness.

C. The Vestibular System

Connections between the vestibular and oculomotor systems are very
complex. Klosovskii (1934) transected fibers running from the vestibular to the
oculomotor nuclei. These investigations showed that crossed fibers run from the
triangular nuclei to the oculomotor nuclei, and that these connections partici-
pate in the formation of horizontal nystagmus. Uncrossed fibers from
Bekhterev's nuclei to the nuclei of the oculomotor nerves play a role in the
formation of vertical nystagmus. According to Lorente de No (1933), poly-
synaptic connections via the reticular formation of the brainstem play the
principal role in the transmission of influences from the vestibular to the
oculomotor system, and the system of the medial longitudinal bundle is much
less important.
Szentagothai (1952) showed that each semicircular canal is connected with
two eye muscles. For example, the left lateral canal excites the left medial rectus
and the right lateral rectus muscles. This connection is effected by three
neurons, with the participation of the system of the medial longitudinal hundle
Additional polysynaptic connections between this same canal and other eye
muscles are present, and are effected through the reticular formation of the
brainstem.
Axons of the second vestibular neuron, running in the system of the
medial longitudinal bundle, terminate on motoneurons of the ocular muscles in
large synapses. Each presynaptic fiber can form a contact with one or more
motoneurons. Many small synapses, in which presynaptic fibers running from
the reticular formation of the brainstem and the nucleus of Cajal terminate, are
present on these same motoneurons. Because of these small synapses, the same
motoneuron can form contacts with many presynaptic fibers.
Experiments with section of the oculomotor nerve and of the medial
longitudinal bundle have shown that the functional roles of the large and small
synapses on the motoneurons of the ocular muscles are different (Szentagothai,
1964). The large synapses are responsible for the "inflexible" connections of the
oculomotor system with the vestibular system through a three-neuron reflex arc.
20 CHAPTER ONE

These "inflexible" connections are responsible for the precise character of

changes in the state of the oculomotor system during stimulation of the
labyrinth. The small synapses are responsible for "plastic" polysynaptic connec-
tions of the oculomotor system with various afferent systems through the
reticular formation of the brainstem. There is every reason to suppose that these
"plastic" connections account for the wide range of functional tuning that is
possible in the control of the oculomotor apparatus. The action of the vestibular
system on the oculomotor apparatus may be not only excitatory, but also
inhibitory. The nucleus of Darkshevich is an intermediate link in the trans-
mission of inhibitory influences. Stimulation of this nucleus can lead to a
decrease in contraction of the eye muscles produced by stimulation of the
vestibular apparatus (Szentagothai and Shab, 1956).
According to Krej~ova (1971), stimulation of one semicircular canal gives
rise to eye movements in a plane parallel to the plane of the canal, regardless of
the position of the eyes in the orbit. Static tilting of the head activates the
otolith apparatus, as a result of which compensatory rotation of the eyes takes
place.
Primary synapses ofaxons running from the semicircular canals are located
in a part of the vestibular nuclear complex that differs from the site of synapses
ofaxons arising from the utriculosaccular apparatus.
In the investigations of Meyer et al. (1973), rotation of the chair to which
a rabbit was fixed through a few degrees led to asymmetrical changes in the unit
activity of motoneurons of the ocular muscles. Vestibular influences evidently
are instrumental in the production of this asymmetry.
In the experiments of Baker and Berthoz (1974) on cats, the membrane
potential of motoneurons of the oblique muscles of the eye and also of
vestibular neurons was recorded extracellularly and intracellularly. Vestibular
nystagmus was produced by transecting the left vestibular nerves. During the slow
phase of nystagmus, depolarization of the motoneuron membrane gradually
increased, and this increase was followed by rapid hyperpolarization. Simulta-
neous recording of vestibular neurons shows that their activity can lead to
membrane depolarization during both the fast and the slow phases of nystagmus.
These workers conclude from their fmdings that the medial longitudinal bundle,
which contains axons of vestibular neurons, is an important supranuclear
structure with a role in the formation of vestibular nystagmus. The frequency of
the nystagmus evidently does not depend on direct interaction between the
bilateral vestibular nuclei, but is determined by the activity of reticular neurons
sensitive to bilateral vestibular effects. One cannot rule out, however, the
possibility that the frequency of nystagmus also depends on specific vesti-
bulovestibular and vestibulooculomotor connections. In the experiments of
Shinoda and Yoshida (1974) on decerebrate, unanesthetized cats, the dynamic
characteristics of various structures of the vestibulooculomotor system (neurons
INNERV AnON MECHANISMS OF THE EYE MUSCLE 21

of the vestibular nuclei, motoneurons of the abducens nerve, axons of the

abducens nerve, the eye itself) were compared. During vestibular stimulation,
there appeared in the oculomotor system short-latency responses that could have
been due only to direct connections between it and the vestibular system. These
direct connections are based on a three-neuron reflex arc (Szentagothai, 1950b).
The middle component of this three-neuron reflex arc is a secondary vestibular
neuron, the axon of which enters the medial longitudinal bundle. In response to
stimulation of vestibular afferent fibers, however, spikes appeared in only half of
the motoneurons of the abducens nerve. During repeated stimulation of
vestibular afferents, more widespread discharges appeared in the motoneurons of
the abducens nerve, and these discharges persisted after injury to the direct
connections of the vestibular system and of the abducens nerve. The discharges
were characterized by a longer latent period and by recruiting, and they were
evidently caused by the spread of impulses along polysynaptic reverberating
networks of collaterals of the bulbopontine reticular formation.
Special analysis of the effect of electrical stimulation of the ampullary
receptor of the horizontal semicircular canal on the various components of
vestibular nystagmus in rabbits, undertaken by Levashov (1965), revealed an
optimal frequency of stimulation at which the velocity of the fast phase of
nystagmus was maximal. At the same time, the velocity of the slow phase of
nystagmus increased with an increase in the frequency of stimulation. Levashov
concluded from these findings that both components of nystagmus are depen-
dent on the vestibular apparatus, but the character of the relations.b!p is
anatomically and functionally different in the two cases.
The tonus of the eye muscles is thus the result of complex interaction
among widely different effects on the motoneurons of those muscles. Effects of
the motor apparatus of the eye of this sort can evidently be exerted by the
proprioceptors of the eye muscles and also by the visual and vestibular systems
(the reticular formation of the brainstem, and supranuclear formation).
 CHAPTER II

Fixation Movements of
the Eyes

Constant micro movements of the eye (physiological micronystagmus) can be

found in any healthy person who is looking at a stationary point. The use of
special methods has revealed the extremely complex organization of these
movements and their important role in visual perception.

The Role of Fixation Movements of the Eyes in Visual Perception

During fixation on a stationary point, three types of micromovements of

the eyes occur: tremor, drift, and saccades.
Tremor is small, frequent movements of the eye. The mean amplitude of
tremor, as measured by different workers, varies: Adler and F1iegelman (1939),
l' of arc; Riggs and Ratliff (1951),17.7" of arc; Higgins and Stultz (1953),1.2'
of arc; Ditchbum and Ginsborg (1953), 10-30" of arc; and Yarbus (1965),
20-40" of arc. The frequency of tremor, according to measurements by the
same workers, also varies widely: Adler and Fliegelman (1934), 50-100 Hz;
Riggs and Ratliff (1951),30-70 Hz; Higgins and Stultz (1953), 50 Hz; Ditch-
bum and Ginsborg (1953), 30-80 Hz; Ditchbum (1963), a continuous spectrum
of frequencies up to 150 Hz; and Yarbus (1965), 70-90 Hz.
The discharge frequency in the motor units and also in motoneurons of
the ocular muscles is approximately the same as the frequency of tremor of the
eye (Keller and Robinson, 1971). On the basis of this finding, it has been
suggested that tremor of the eye is incomplete smooth tetanus due to periodic
activity of the motor units (Bjork and Kugelberg, 1953). This hypothesis is
supported by the very high fusion frequency of single contractions of the eye
23
24 CHAPTER TWO

muscles in tetanus: even during stimulation of the oculomotor nerve at very high
frequency (350-400 pulses/sec), the eye muscles respond by single contractions
(I. Cooper and Eccles, 1930; Bach-y-Rita and Ito, 1966).
Drift is a slow, smooth movement of the eye interrupted by micro-
saccades. Most workers conclude that the mean amplitude of drift is 5-6' of arc
(Dodge, 1900; Riggs and Ratliff, 1951; Ditchbum and Ginsborg, 1953, and
others). The duration of drift, according to Ditchbum and Ginsborg (1953),
varies from 30 to 5000 msec. According to Ditchbum and Ginsborg (1953),
during drift, the two eyes move synchronously in the vertical plane, but
horizontally they may move in mutually opposite directions.
Saccades are rapid eye movements lasting 10-20 msec and with a mean
amplitude of 5-6' of arc (Ditchbum and Ginsborg, 1953; Nachmias, 1959;
Krauskopf et al., 1960). The maximum difference in time between the
appearance of sacca des in the right and left eyes does not exceed 10 msec
(Krauskopf et af., 1960).
Physiological micronystagmus is essential for visual perception, because it
maintains constant displacement of the image on the retina, and thus ensures
that different receptor elements are stimulated in tum. Electrophysiological
investigations have shown that an impulse appears in a single fiber of the optic
nerve only as an on-off effect to light (Granit, 1957). Movement of the eyes
produces a constant change in the intensity of illumination of the photo-
receptors and prevents adaptation of parts of the retina on which the image is
projected. During the creation of a stabilized image on the retina (by means of a
microprojector or mirror fixed to the eye), all visible differences in the visual
field disappear after 1-3 sec (Riggs et al., 1953; Ditchbum, 1955; Yarbus,
1965). To study the role of different types of micromovements of the eye in
disadaptation, Ditchbum et al. (1959) created a stabilized retinal image and then
caused this image to move with the characteristics of tremor, drift, or sacca des.
They found that saccades restore the image of an object once it has disappeared,
but do not retain it for a sufficiently long time. Drift produces only a slight
degree of retinal disadaptation, whereas tremor restores an image that has
disappeared, provided that summation of the whole of its frequency spectrum
takes place; low-frequency components of tremor play the major role in this
process. According to Riggs et af. (1953), vision can be improved by increasing
movement of the image of the retina, by comparison with movements of the
image taking place during ordinary fixation. An increase in the amplitude and
rate of displacement of the image on the retina to twice their values in ordinary
fixation movements was brought about by means of a special optical system
consisting of prisms and mirrors. The use of this optical system enabled the
subjects to distinguish much thinner lines than under ordinary conditions. The
abolition of micromovements of the image on the retina thus leads to the
impairment of vision, whereas increasing these movements can improve visual
acuity.
FIXATION MOVEMENTS OF THE EYES 2S

Mia-otremor of the Eyes as an Indicator of Combined Activity of Motor Units

of the Ocular Muscles

The high fusion frequency of single contractions of the eye muscles into
tetanic contraction is the cause of tremor of the eyes, the mean frequency of
which is approximately the same as the mean firing rate of single motor units.
Correlation between tremor and the firing pattern of the motor units of the eye
muscles is determined by several factors, the most important of which are the
relationship between strength and duration of isometric muscular contraction
(Fel'dman, 1964) and the state of the eyeballs and eye muscles as "mechanical
fIlters," possessing definite viscosity and elasticity (Thomas, 1969).
Wide prospects for the investigation of micro tremor of both eyes have
been opened up by the use of the electronic method developed by Thomas,
which is based on the controlling of fine eye movements with the aid of a
piezocrystal. Small saccadic eye movements are transmitted to this crystal
through a small piece of soft rubber that touches the eyeball after anesthesia of
the conjunctiva. Because of the characteristics of its electronic design, Thomas's
method enables the velocity of the tremor of the eyes, which is related to
changes in its amplitude, to be recorded (Thomas, 1965, 1967, 1969; Bengi and
Thomas, 1968). By anesthetizing the conjunctiva with decicaine and immobil-
izing the upper and lower limbs with strips of adhesive tape, several workers have
succeeded in using the electronic method under clinical conditions (A. R.
Shakhnovich and Thomas, 1974; A. R. Shakhnovich et al., 1975).
Tremor in healthy subjects was found to have certain special features
characteristic of both eyes and maintained during prolonged recording. The
dominant frequency of tremor was about 100 Hz. Distinctive changes in tremor
occurred periodically in the form of "bursts" - waves of high amplitude and
close to sinusoidal in shape (Figs. 1-3). The frequency of the waves during a
"burst" was virtually constant in the same subject, but in different subjects, it
varied over a narrow range (85-108 Hz). The histogram of interspike intervals
has a maximum at about 70 msec. No precise correlation could be found
between the "bursts" of tremor of the two eyes. One cannot rule out the
possibility that "bursts" of tremor are important for disadaptation in the retina.
In the periods between "bursts," the tremor was irregular and reached a very
high frequency (up to 200 Hz), evidently as a result of certain features of the
method used (the absence of inertia of the contact lens and of the Yarbus cap).
Under pathological conditions, changes were observed in the microtremor;
these changes differed in character and severity. Changes in the character of the
tremor were observed during recording. Often, a considerable difference was
found in the character of the tremor of the two eyes (Figs. 4 and 5). "Bursts" of
tremor, with a frequency of about 100 Hz under normal conditions, were often
absent. "Pathological bursts" of high-amplitude tremor, with a much lower
frequency than normal (40-60 Hz), sometimes appeared. These "pathological
 26 CHAPTERlWO

(.)
Q)
II>

*'....>- 3 -
·in
c: ---
Q)
'"0
2 ~_r----

>
."!::
:c
'"0
.c 1
...
Q..

~-
50 100 150 250
Frequency of tremor, Hz

Figure 1. Microtremor of the eyes under normal conditions. Top: Tremorograms of the right
(d) and left (s) eye. Bottom: Distribution of frequencies of microtremor of the right eye
(solid line) and left eye (dashed line) as a function of the frequency of tremor. To calculate
the probability density, the percentage occurrence of a particular frequency in a given
frequency interval was divided by the length of that interval (in oscillations per second).

bursts" of tremor occurred irregularly (Fig. 6). Long waves of very low
frequency (about 30 Hz), and near-sinusoidal in shape, also sometimes appeared
on the tremorogram under pathological conditions.
Comparatively slow oscillations of the base line (8-12 Hz) also appeared
under patholOgical conditions against the background of the high-frequency
tremor. Slow oscillations of this type could occur in one or both eyes (see Figs.
2 and 3). These oscillations could appear and disappear in the course of a short
period of time. The considerable changes in the frequency of tremor in disease
can reasonably be subdivided into the following frequency bands: K-rhythm,
>120 Hz; L-rhythm, 80-120 Hz; M-rhythm, 60-80 Hz; N-rhythm, 40-60 Hz;
O-rhythm, <40 Hz.
Microtremor of the eyes is a sensitive indicator of the functional state of
the brainstem. It is therefore interesting to compare changes in microtremor of
the eyes with the degree of disturbance of consciousness. The degree was
FIXATION MOVEMENTS OF THE EYES 27

100 msec

Figure 2. Tremor of the eyes under normal and pathological conditions. The top curve of
each pair represents the right, the bottom curve, the left eye. Top pair: Tremor of eyes
under normal conditions. "Bursts" of tremor can be seen. Middle and bottom pairs:
Different parts of a record of ocular tremor in a patient with bulbar encephalitis. No
"bursts" of tremor are present. Slow waves (approximately 11 Hz) appear periodically, lust
in one eye (middle), then in both eyes (bottom).

100 msec

Figure 3. Tremor of the eyes under normal and pathological conditions. The top curve of
each represents the right eye, the bottom curve, the left eye. Top pair: Ocular tremor under
normal conditions. "Bursts" of tremor can be seen on the records. Bottom pair: Ocular
tremor of a patient with a tumor of the left cerebellopontine angle, affecting the brainstem.
The frequency of tremor is much lower than normal In addition, slow oscillations of the
base line of the tremorogram (8-11 Hz) can be seen.
28 CHAPTER lWO

100 msec

Figure 4. Tremor of the eyes in a patient with bulbar encephalitis. There is a considerable
difference between the frequencies of tremor of the right (top) and left (bottom) eyes.

--v
I I
100 msec

- J_ _' -_ _ _ _ _ _ _ _ _ _ _ _ _ _ _~_----------------~-------------------

Figure S. Tremor of the eyes in a patient after hemorrhage from ruptured aneurysm of the
basilar artery. The top curve of each pair represents the left eye, the bottom curve, the right
eye. Top pair: Tremor of eyes 7 days before patient's death. Patient unconscious, response
to nociceptive stimulation present only on the face. Tremorograms show absence of typical
"bursts." Frequency of tremor differs in right and left eyes. Monocular appearance of
saccades - only in the right eye (the appearance of the curve during the saccade is
determined by the frequency characteristics of the amplifier). Middle pair: Recorded 5 days
before patient's death. Patient in a state of stupor. Frequency of tremor sharply reduced.
Both binocular and monocular saccades can be seen. Bottom pair: Recorded 4 days before
patient's death. Patient unconscious, response to nociceptive stimulation only of the left
half of the body. Frequency of tremor higher than on the previous day, but lower than
when first tested.
FIXATION MOVEMENTS OF THE EYES 29

100 msec

-----------------~~~-----------~----------~-----~
Figure 6. Tremor of the eyes in a patient after hemorrhage following rupture of an
aneurysm of the supraclinoid part of the right internal carotid artery. The top curve of each
pair represents the left eye, the bottom curve, the right eye. Top pair: Records of tremor 4
days before patient's death. Patient unconscious and did not respond to nociceptive
stimulation. Cerebral blood flow normal. Frequency of tremor lower in left eye than in
right. Middle pair: Records obtained 2 days before patient's death. Patient unconscious,
responded to nociceptive stimulation by decerebrate rigidity. No blood flow in cerebral
cortex. "Pathological bursts" of low-frequency, high-amplitude tremor in left eye. Boitom
pair: Records obtained 14 hr before patient's death. Unconscious. Responded to nociceptive
stimulation by decerebrate rigidity. Frequency of tremor lower than on previous days;
number of "pathological bursts" of tremor increased.

assessed by the use of a combined classification (Fig. 7), based on clinical and
electroencephalographic criteria. The most characteristic types of disturbances
of micro tremor of the eyes associated with different levels of unconsciousness
are illustrated in Fig. 8. Statistical analysis of microtremor of the eyes in 60
patients with intracranial hemorrhages of different genesis (head injuries, rupture
of aneurysms of the cerebral vessels) showed a decrease in the dominant
frequency of tremor as the depth of unconsciousness increases (Fig. 9). Particu-
larly clear correlation is observed between degree of disturbance of unconscious-
ness and the decrease in the frequency of tremor during bursts.
Investigations of microtremor of the eyes during deepening of uncon-
sciousness and also during recovery from unconsciousness are particularly
interesting. Following are observations on the dynamics of ocular microtremor
in a patient recovering from a state of deep unconsciousness:
30 CHAPTER TWO

Clinical features Electroencephalographic features

Muscular tone, Vital tunc- Pupillary :: ~ Carrying Answer- 8 a fJ Response to af-

6
motor response tion (respira- and blink- ~ -i out sim-
... g pie in- '-2 3-6 7-12 13-24 ~i~~t(!::~r
to pain ti:~~:;al ~7::: i l structio stimuli)

I
Somno- Initial
lence depression
Coordinated
movement

Stupor

III Uncoordinated
movement or
Coma decerebrate
rigidity
N
Decerebrate
Deep rigidity or
coma atony

o - Response present eJ - No response

Figure 7. Combined classification of degree of unconsciousness based on clinical and

electroencephalographic features.

After an operation for clipping an aneurysm of the anterior communi-

cating artery, this patient's circulation was disturbed in the territory of the
anterior cerebral artery, and he developed left-sided hemiplegia. His condition
remained grave for a long time, and he gradually began to improve only several
months later. His state was particularly serious during the first month after the
operation. It was impossible to communicate with the patient, he did not answer
questions, and he did not carry out simple instructions. He was fed through a
tube and had no control over his sphincters. His pupils were constricted and did
not react to light. The blinking reflexes were also absent. Nevertheless, his
breathing was spontaneous, and his blood pressure remained at the normal level.
This state was unstable, and it varied from the appearance of elements of
consciousness (opening the eyes in response to instruction) to total absence of
any response to nociceptive stimulation.
Considerable fluctuations were observed in the character of the ocular
microtremor as recorded on different days. For example, on the 13th day after
the operation (Fig. 10), the dominant rhythm of tremor corresponded to higher
frequencies than on the 17th day (Fig. 11). On the 20th day after the operation
(Fig. 12), the distribution of ocular microtremor became bimodal, and its
dispersion increased.
During recovery from unconsciousness, changes in the ocular microtremor
were found at long intervals of time. The results of an investigation on a patient
who had undergone an operation for the removal of a chronic subdural
hematoma of the right parietal region will serve as an example. During the
month after the operation, the patient was in a deeply comatose state with
FIXATION MOVEMENTS OF THE EYES 31

disturbance of his vital functions. Later, he gradually recovered from uncon-

sciousness, with successive changes between states of akinetic mutism and an
apathetic syndrome. Not until 2 months after the operation did the patient
begin to carry out simple instructions, and it was later still before he could
answer simple questions. Tests on the patient 4 years later showed no gross
mental disturbance. He merely showed some unconcern and was insufficiently
critical of his own state. Bilateral briskness of the tendon reflexes was combined
with slight disturbances of static posture. The EEG showed general cerebral
changes of an irritative character and evidence of involvement of the midline
brain structures. Investigation of the ocular microtremor showed a definite
decrease in the dominant rhythm to about half the normal level (Fig. 13).
The disturbances of the ocular microtremor increased in the patients who
eventually died. Tests carried out on a patient after rupture of an aneurysm of

II

III

100 msec

IV

Figure 8. Ocular tremor in patients with different stages of unconsciousness: (0) lucid
consciousness; (I-IV) various stages of unconsciousness. The top curve of each pair
represents the right eye, the bottom curve, the left eye.
32 CHAPTER lWO

DOMINANT RHYTHM FREQUENCY DURING

% % BURSTS
80 80
60
o 40 40
20 20

80 80
60 60
40 40
20 20

80 80
60 60
II 40 40
20 20

80 80
60 60
III 40 40
20

80 80
60 60
IV 40
20

0 3 0 2 0, N M L K 0 3 O 2 0, N M L K Hz
c c('0) c c c c
~ ('0) c c
~
~ CO ~ or ~ ~
... "'"
C'I
~ 6 "'6('0)" 6 6 ~ ~ 6 6 c
6 A ~ ~ ~
A
C'I
"'" 10 CO "'" 10

Figure 9. Relationship between dominant rhythm of ocular micro tremor (left) and
frequency of tremor during bursts (right) and degree of unconsciousness (Roman numerals).

° ,°
The contributions of individual frequencies are plotted against the frequency of tremor,
using the author's accepted classification of rhythms (K, L, M, N, 1 2 , and 03).
 d

100 msec

...u
01)
3
~

....>-
'in
,...- """-
c 2
01)
>--
">
.~
:c.., 1 r-I="=
f--
.0 ~
...0
a... 1 .......
50 100 150 167
Frequency of tremor, Hz
Figure 10. Ocular tremor in a patient on the 13th day after operation for clipping
aneurysms of anterior communicating artery. Legend as in Fig. 1.

100 msec

50 100 125 150

Frequency of tremor, Hz
Figure 11. Ocular tremor in the same patient as in Fig. 10, on the 17th day after operation.
Legend as in Fig. 1.
34 CHAYfERlWO

s
100ll1sec

~3
en

-- r-

.c 1
- -
-
III
.c
e
Il..
f--
~- f--- ~-----.,
~--
I I
50 100 150 167
Frequency of tremor, Hz

Figure 12. Ocular tremor in the same patient as in Fig. 10, on the 20th day after operation.
Legend as in Fig. 1.

the anterior communicating artery will serve as an example. This patient was in a
stuporous state. He did not answer questions, but could carry out simple
instructions. Swallowing was normal, the pupillary and blinking reflexes were
preserved, and there were no disturbances of the vital function. A histogram of
the ocular rnicrotremor (Fig. 14) showed a bimodal distribution and a decrease
in the frequency of the dominant rhythm of the tremor. An operation to remove
a subdural hematoma of the left frontoparietotemporal region was performed 3
days after this investigation. The patient's condition improved a little. He was
able to answer simple questions, although he remained drowsy and soon became
tired. While he was in this state, 3 days after the operation, the rnicrotremor of
the eyes was tested (Fig. 15). On the tremorograms, it was difficult to detect a
dominant rhythm, but the dispersion was increased, chiefly on account of high
frequencies - up to 250 oscillations/sec. Later, the patient's condition
worsened, and communication with him became impossible. At 5 days before
death, the pupillary and blinking reflexes were absent, but the response to
nociceptive stimulation still remained. Disturbances of breathing appeared. A
clearly defmed dominant rhythm with about half the normal frequency
appeared on the tremorogram (Fig. 16).
FIXATION MOVEMENTS OF THE EYES 3S

Another example of a gradual increase in the disturbance of ocular

micro tremor, in a patient with a saccular aneurysm of the supraclinoid part of
the right carotid artery after repeated subarachnoid hemorrhages, is illustrated in
Figs. 17 and 18. This patient became unconscious 4 days before death.
Nociceptive stimulation of the trunk and limbs, however, led to the appearance
of uncoordinated movements. The right pupil was wider than the left; it did not
respond to light, and the response of the left pupil was sluggish. Blinking reflexes
were reduced, muscle tone was increased and extensor in type, and bilateral
pyramidal signs were present. The tremorogram showed bursts of slow waves,
appearing synchronously in both eyes (Fig. 17). The histogram showed a
bimodal distribution of the frequencies of microtremor and an increase in their
dispersion. On the day of this patient's death, she became completely uncon-
scious. General muscular hypotonia was accompanied by absence of all tendon
reflexes and of response to nociceptive stimulation. Pupillary and blinking
reflexes were absent. Disturbances of breathing appeared. The tremorogram of
the patient's left eye on the day of death showed high-amplitude oscillations of
very low frequency, 10-20 per second (Fig. 18). This asymmetrical appearance
of bursts of slow oscillations of one eye was rarely observed. More frequently,
bursts of slow waves were synchronized in the two eyes. They were usually
sinusoidal in shape, and they were repeated after relatively stable time intervals.
The results of an investigation of a patient with a severe head injury will

s
100 msec
u
Q)

~
'"
3
....>-
·en
c:
Q) 2
"0
>
.~
:cca r-
..0 i::::..=..:::J
...
0
Il..
~---~
I
50 100 150 167
Frequency of tremor, Hz
Figure 13. Tremorograms of a patient 4 years after operation to remove a chronic subdural
hematoma of the right parietal region. The dominant rhythm of ocular micro tremor is
decreased. Legend as in Fig. 1.
36 CHAPrER1WO

serve as another example. This patient was completely unconscious. Motor

responses, in the form of grimaces, appeared to nociceptive stimulation in the
region of the face only. The pupillary and blinking reflexes were absent. Tendon
and periosteal reflexes were also absent. Muscle tone was increased and extensor
in type. Respiration was spontaneous. During recording of the ocular micro-
tremor of this patient (Fig. 19), bursts of synchronous oscillations of both eyes,
sinusoidal in shape, were discovered. These bursts of microtremor, about
100 msec in duration, were repeated periodically after fairly stable time intervals
(600-700 msec). They appeared simultaneously with bursts on tremorograms of
the arms and correlated with heart contractions recorded on ballistocardiograms.
The bursts are seen clearly only in atonic coma. The relationship between
the amplitUde of these bursts and the amplitude of background tremor can be
used to measure muscle tonus. Besides these sinusoidal bursts of tremor, bursts
of irregular, high-amplitude oscillations were observed in comatose patients.
These bursts of tremor usually appeared simultaneously in both eyes, lasted
200-300 msec, and were repeated at intervals of 1-4 sec. An example of such a

Figure 14. Ocular tremor in a patient with aneurysm of the anterior communicating artery,
3 days before operation for the removal of a subdural hematoma of the left frontoparieto-
temporal region. Legend as in Fig. 1.
 d

s
100 msec
u
• I

Q)
en
3
'*>-
:!::
en
c:
Q)
"C
2
>
,,=
:c ,--
.--- ----
'"0 1
.c
....
Q..
~ ....
-
--
-------i. -d
50 100 150 250
Frequency of tremor, Hz
Figure 15. Ocular tremor in the same patient as in Fig. 14, 3 days after operation for the
removal of a subdural hematoma. Legend as in Fig, 1.

I
100 msec
,.
u
Q)
en
-
'*....>-
3

---
'Vi
c:
"C
Q)
2
>
,,= ~.
:c
'"0
.c 1
--
....
r-- ~ I
-l -----~
Q..
-I
I
50 100 150 167
Frequency of tremor, Hz

Figure 16. Ocular tremor in the same patient as in Fig. 14, on the 13th day after operation
(5 days before death). Legend as in Fig. l.
 d

(,)
II)
en
'#. 3
>.
.....
'iii .--
c: 2
II)
"0
>
~
:.c 1 -------
----
~ -
IU
.c
0.... f-
0.. --l'fl-.r- -~
50 100 150 250
Frequency of tremor, Hz
Figure 17. Ocular tremor in a patient with a saccular aneurysm of the supraclinoid portion
of the right carotid art~ry, showing her condition after the third subdural hemorrhage, 4
days before death. Legend as in Fig. 1.

(,)
II)
en
'#.
3
>.
.....
'iii
c:
"0
II)
2
>
.1:
:.c
IU 1
.c
....
0
0..

Frequency of tremor, Hz

Figure 18. Ocular tremor in the same patient as in Fig. 17, on the day of death. Legend as in
Fig. I.
FIXATION MOVEMENTS OF THE EYES 39

100 msec

Figure 19. Ocular tremor in a patient with severe head injury after removal of a subdural
hematoma of the right frontoparietotemporal region. The patient's condition was extremely
grave. Deep coma (stage IV).

burst of high-amplitude, irregular oscillations of the eyes, in a patient at stage III

of unconsciousness, can be seen in Fig. 8.
Bursts of microtremor not only arise spontaneously, but can also be
provoked by various factors. An example of this provocation of microtremor can
be seen in the results of test on a patient with bulbar encephalitis. The patient's
condition was extremely grave, and he was unconscious. The patient did not
answer questions, and could not carry out instructions. The right eye responded
to photic stimulation by turning inward. The pupillary responses to light and the
blinking reflexes were preserved. Of the tendon reflexes, only the patellar could
be evoked, and these were sharply increased. Muscle tone in the limbs was
increased and extensor in type. Tonic spasms appeared periodically in the limbs,
and a state of decerebrate rigidity developed, accompanied by an increased rate
of respiration. These states developed spontaneously, and they could also be
provoked by any external stimulus. During tonic spasms in the limbs, the ocular
tremorogram showed bursts of slow, high-amplitude oscillations of very low
frequency: 16-18 per second (Fig. 20).
As a rule, the appearance of these slow, high-amplitude oscillations was a
40 CHAPTERlWO

100 msec

Figure 20. Ocular tremor of the right eye in a patient with bulbar encephalitis in a comatose
state (stage III), at rest (top) and during tonic spasms in the limbs evoked by nociceptive
stimulation (bottom).

bad prognostic sign. Analysis of the writer's own material shows that the
appearance of bursts of low-frequency ocular tremor «33-35 oscillations/
second) as a rule presaged death. The discovery of this critical level of
disturbances of ocular microtremor may be of great practical importance. Poor
prognostic signs that may be found in a patient in a comatose state include
changes in the EEG (the appearance of a generalized theta-rhythm or isoelectric
line), the stop-contrast phenomenon on cerebral angiograms, a reduction in the
volume velocity of the cerebral blood flow below 25 ml/IOO g tissue per min, a
reduction in the rate of oxygen consumption by the brain below 1.0 mi/IOO g
tissue per min, a reduction in the arterio-venous oxygen difference below
2 vol.%, and an increase in the lactate concentration in the CSF above
40 mg/IOO ml. Analysis of the writer's clinical material (60 patients with
intracranial hemorrhages caused by head injuries and rupture of aneurysms of
the cerebral vessels) shows that all these poor prognostic signs appear not more
than 4 or 5 days before death. At the same time, critical disturbance of
ocular microtremor (the appearance of bursts with a frequency of less than
33-35 oscillations/sec) appeared much sooner in these patients, 2-3 weeks
before death (Fig. 21). These fmdings suggest that in the combined investigation
of comatose patients, changes in the ocular microtremor are one of the most
important prognostic signs.
Disturbances of ocular microtremor are observed not only in patients with
lesions actually in the brainstem, but also in patients with toxic manifestations
of infectious hepatitis. Even though consciousness was lucid and the manifes-
tations of hepatitis were confined to slight jaundice of the sclera, the tremoro-
gram of both eyes showed sufficiently clear changes (Fig. 22). As the jaundice
increased and insomnia and loss of appetite appeared, the disturbances of ocular
tremor increased (Fig. 23). Changes in ocular micro tremor were particularly
clear in patients with infectious hepatitis in whom consciousness was disturbed.
 FIXATION MOVEMENTS OF THE EYES 41

Frequency of tremor
durin9 burst, Hz

L 00

.. • ..•• -. .. ..
~-~,---~-,--~------------------

··• - ·• •
•
•
•
•
•
• •
•
0
0 1 2 3 4 5 6 7 8 9 10 t 1 12 13 14 15 16 1718 19 20 21
Days before death

Figure 21. Appearance of a critical level of disturbance of ocular microtremor in relation to

the number of days before death that bursts of ocular tremor of a given frequency appeared.

s
100 msec
u
Q)

'"
*- 3
>-
.....
.iii
c: r-
Q)
\j
2 r-
I--f---
>
.'::! - '---
:c 1
CtI
.c 1=
...0
0..
.~

50 100 150 250

Frequency of tremor, Hz
Figure 22. Ocular tremor in a patient with infectious hepatitis. Clinical picture of slight
jaundice of the sclera. Consciousness lucid. Legend as in Fig. 1.
42 CHAPTER1WO

s
100 msec

-
.0 1
~
o...
a...
H I
50 100 150
Frequency of tremor, Hz

Figure 23. Ocular tremor in the same patient as in Fig. 22. Clinical picture showed increased
severity of jaundice, insomnia, and loss of appetite. Consciousness lucid. Legend as in Fig. 1.

The results of tests on a patient with infectious hepatitis in a stuporous state will
serve as an example. The frequency of the dominant rhythm of tremor in this
patient was considerably less than normal (Fig. 24).
Comparison of the results of investigation of the ocular micro tremor in
health and disease enables suggestions to be made regarding the functional
organization of the motoneuron pool of the ocular muscles. The mechanisms of
appearance of ocular tremor under normal conditions can be explained as
follows: The activity of the various motor units of the ocular muscles has a mean
frequency of about 100Hz. The duration of a single contraction of an ocular
muscle does not exceed 10 msec. The dominant frequency of ocular tremor is
therefore about 100 Hz, in agreement with views expressed by Fel'dman (1964)
on the basis of model experiments.
To explain the shape of the ocular tremor curve in health and disease,
views regarding the combined activity of a small number of motor units may be
useful (A. R. Shakhnovich et ai., 1975). In accordance with this simplified
model (Fig. 25), every nervous impulse evokes a short contraction of the muscle
FIXATION MOVEMENTS OF THE EYES 43

fibers it supplies. The contractions produced by the activity of four motor units
are represented in Fig. 25A. These units function independently, and have
different frequencies (ranging from 90 to 110 Hz), but each unit functions
strictly periodically. The single curve of combined contraction of four muscle
bundles is shown below the four separate curves. It is close to sinusoidal in
shape. The contractions arising as a result of the activity of another four motor
units are represented in Fig. 258. In this case, the units function independently
and each has the same average frequency, as in Fig. 25A, but some irregularity in
the function of each unit can be seen (deviation of about 10%). Again, the single
curve of combined contraction of four muscle bundles is shown below. It is
similar to the tremorogram of the healthy subject. Part of the record is irregular,
this part being followed by a short sinusoidal burst, and another irregular part. It
is interesting to note that when the four units function independently but
regularly, at the same mean frequency, the single curve of combined contraction

c.J
CI)
en
4 r
*-
.'=>-
en
3
c:
CI)

".'=> 2
~
r--
:c<0
1 t-
-
.0
...
0
c..
1--

---Fl---t.:.= l
50 100 150 167
Frequency of tremor, Hz

Figure 24. Ocular tremor in a patient with infectious hepatitis in a stuporous state of
consciousness (stage II). Legend as in Fig. 1.
44 CHAPTER lWO

~ ~
~ ~
~ ~
~ ~

A ~ B ~

~ ~
~ ~
~ ~
~ ~
C ~ 0
~
Figure 25. Model views of the dependence of ocular microtremor on regularity and
frequency of motor unit activity (see the text): (A) motor units act independently, strictly
periodically, and with different frequencies; (B) motor units act independently, irregularly
(deviations about 10%), and with different mean frequencies (with the same mean
frequency of each unit as in A); (C) motor units act independently and irregularly, but with
the same mean frequency; (D) motor units act independently with identical mean frequency
of each unit, but with increase in degree of irregularity (to 50%).

differs from those in Figs. 25A and B, and bursts are absent (Fig. 25C). These
results are not basically altered if three, four, five or more motor units are
examined. It can accordingly be concluded that the normal tremorogram is
determined by the activity of motor units that function independently, with
some degree of irregularity, and with a slight but significant difference in their
mean frequencies, distributed around 100 Hz. The motor units of the right and
left eyes evidently work independently, so that the bursts of tremor of the two
eyes are not interconnected.
Motor units that function independently and at about equal average
frequencies, but with great irregularity in the activity of each unit (deviation of
about 50%), are examined in Fig. 25D. The single curve of combined contraction
of four muscle bundles is shown below. Note that it is a low·frequency, irregular
curve, resembling the tremorogram of a patient in deep unconsciousness. It can
accordingly be postulated that stabilization of the frequency of motor neurons
of the ocular muscles is disturbed if the changes in consciousness are increased in
degree.
The model views represented in Fig. 25 give a very simplified interpret·
ation of the dependence of the ocular tremorogram on the activity of motor
units of the ocular muscles. Nevertheless, these views can prove useful in the
attempt to discover how ocular rnicrotremor depends on the functional state of
the motoneuron pool of the ocular muscles.
FIXATION MOVEMENTS OF THE EYES 4S

The appearance in disease of an ocular tremor with a lower dominant

frequency (30-60 Hz) than normal can be explained by an increase in
fluctuations of the interspike interval of the motor units, although their mean
discharge frequency remains unchar.ged (Fel'dman, 1964). Fel'dman's model
views, however, provide an additional explanation for the decrease in frequency
of tremor through a change in the firing rate of the motor units (an increase or a
decrease).
The appearance of fluctuations of the base line of the tremorogram with a
low frequency (8-12 Hz), and also the appearance of "pathological bursts" of
high-amplitude, low-frequency tremor (40-60 Hz), can be explained by the
synchronous activity of the motor units in connection with a disturbance of the
functioning of their de synchronization mechanisms. Disturbances of function of
the desynchronization mechanisms, and also of mechanisms of stabilization of
the interspike intervals of motor units, were manifested particularly clearly after
decortication (following cessation of the blood flow in the cerebral cortex; see
Fig. 6). Mention has also been made of the important role of cortical influences
in the stabilization of interspike intervals of motor units (Tokizane and Shimazu,
1964).
In the explanation of the mechanism of the low-frequency waves of the
tremorogram (8-12 Hz, i.e., the same frequency as the a-rhythm of the EEG), it
is important to remember the possibility of influences of the thalamic "pace-
maker" on the oculomotor system (Andersen and Eccles, 1962).
It can be seen from the foregoing discussion that recording the ocular
tremor provides extensive opportunities for an integrative definition of the
functional state of the motoneuron pool of the eye muscles.

Mechanisms Controlling Fixation Micromovements of the Eyes

Stable fixation of gaze depends largely on mechanisms of interaction

between saccades and drift of the eye during fixation. In the opinion of most
workers, drift is uncontrollable, and is the result of instability of the eye,
whereas saccades perform a corrective role, ensuring stable fixation (Ratliff and
Riggs, 1950; Ditchbum, 1955; Comsweet, 1956; Glezer, 1959; Boyce, 1967).
Comsweet (1956) came to this conclusion after having shown that the velocity
of drift is independent both of the character of movement of the image of the
stimulus across the retina and of its disappearance. The velocity of drift is
unchanged when the image is stabilized on the retina, and also during fixation on
an imaginary point in darkness.
In Comsweet's opinion, the basic stimulus for saccade development is not
impulses from proprioceptors of the ocular muscles, but displacement of the
image on the retina. With an increase in displacement of the eye from the
mid position, the probability of saccades increases and reaches unity if the
46 CHAPTERlWO

displacement amounts to 6' of angle. The direction of the saccades is aimed at

abolishing this displacement, and their amplitude increases with an increase in
the degree of deviation of the eye from the midposition. The frequency of
saccades decreases if the image is stabilized on the retina. The corrective role of
saccades relative to drift is also postulated by Boyce (1967), who showed that
saccades are opposite to drift, and their amplitude is such that they compensate
for displacement of the eye caused by drift. The same conclusion was reached by
Nachmias (1959), who showed that saccades are opposite in direction to drift
during fixation. In Nachmias's opinion, not every drift is compensated com-
pletely by a subsequent saccade, and it is possible to speak only of correction of
the average. The area of the ellipses of scatter, calculated for the beginnings of
saccades, is greater than that for the ends of the saccades; this finding is also
evidence for the corrective role of saccades with respect to drift. As a supporter
of the hypothesis of the correction of drift by saccades, Nachmias pointed out
some of its limitations: the latent period of the saccade is not less than 0.1 sec,
and for that reason, the part of the drift corresponding to the last 100 msec
before the saccade cannot be compensated.
Nachmias carried out his investigations on only two subjects. Moreover,
the contact lens technique he used is susceptible to error on account of slipping
of the lens on the eyeball.
The writer investigated the orientation of fixation micromovements of the
eyes in a larger series of cases than in Nachmias's experiments, and also with the
use of the Yarbus cap, which is free from the drawbacks of the contact lens that
have already been mentioned (A. R. Shakhnovich, 1965a, c, 1966; A. R.
Shakhnovich et ai., 1966; Proskuryakova and Shakhnovich, 1968). Ten subjects
20-36 years old with normal eyesight were examined. A Yarbus cap, covering
the pupil, was secured to the eye. Fixation was carried out with the other eye. A
cross-shaped beam of light, reflected from a mirror secured to the cap, was
aimed at the slit of a photokymograph, 180 mm long and 0.5 mm wide. One line
of the cross was perpendicular to the slit of the photokymograph, and the other
was at an angle of 45° to it (Fig. 26). Displacement of the eye caused
displacement of the cross of light along the slit of the photokymograph, and this
displacement was reflected in the corresponding record. The coordinates of the
center of the cross were determined as follows: OK (horizontal) is the distance
from the vertical line of the cross to the edge of the photographic fIlm; Oa = ab
(vertical) is the distance between the two lines of the cross. The trajectory of
displacement of the visual axis was determined relative to these coordinates. The
eye movements were recorded with a sensitivity of 6' of arc (the fixation point
measured l' of arc).
Areas of the trajectories of displacement of the visual axis in the course of
10 sec and in four subjects, in the writer's opinion, characterize the micromove-
ments of the eyes of healthy human subjects with sufficient completeness
FIXATION MOVEMENTS OF THE EYES 47

o
o
o
D
D
D
n
D
D
D
D
D
o

2'L
D
D
D
D

~==~==~========~go
o
o
o
o
o
0.04 sec
"k-----Iij K

... p ,
o
o
o
..... ---J"""
Figure 26. Micromovements of the eyes during fIxation recorded by an optical method (see
the text). Left: Diagram of projection of a cross of light on the slit of a photokymograph.
Right: Specimen record.

(Fig. 27). The character of the micro movements did not differ significantly in
the other six subjects.
Saccades consist of two, or sometimes three, components. In some cases,
the first and second components of the saccade are in mutually opposite
directions (e.g., the saccade dermed by points 40-42 in the record of subject
L.A., Fig. 27). The second component of the saccade is most frequently at an
acute angle to the first (e.g., the saccade defined by points 25-27 in the record
of subject L.A., Fig. 27). In cases when the angle between the first and second
components of the saccade is greater, and almost a right angle, a third
component of the saccade usually appears, and is directed toward the trajectory
vector of the first component (e.g., the saccade defined by points 49-52 in the
record of subject L.A.; Fig. 27).
The breaking up of saccades into separate components can be regarded as
due to errors of recording (slipping of the cap, the action of forces of inertia,
and so on). The variability of the angle between the individual components of
saccades, however, as well as the variability of their relative amplitudes, make
this hypothesis improbable. Under these conditions, the existence of several
components of saccades can be explained by the character of the function of the
central regulatory mechanisms. One cannot rule out the possibility that this
complex structure of saccades is one of the retina.
Some information on interaction between drift and saccades can be
 N.B

.; l~
~~.9 ,,-
t: 16
37"", :.~~~z

J.J

J'L JI

1li

44<
Jf}

Figure 27. Micromovements of the eyes during fixation on a stationary point (see the text). Trajectories of displacement of visual axis during 10 sec in
subjects L.A., N.B., I.S., and Y.M. Changes in direction of saccades (straight lines) are shown. Changes in direction of drift (wavy lines) are not shown.
Numbers denote successive positions of gaze.
FIXATION MOVEMENTS OF THE EYES 49

obtained by examination of the region in which the points of the beginnings and
ends of saccades are located (Fig. 28). Usually, the points of the beginnings and
ends of saccades are located in the same region, and there is no displacement of
one group of points relative to the other (Fig. 28, subjects N.B. and L.A.). It
cannot be concluded from the data that saccades compensate for eye movement
caused by drift from a certain midposition. Only in one subject (V.M.) were
these two regions displaced relative to one another. In this case, it is possible to
speak of the orientation of the saccades in one definite direction, so that the
presence of a corrective relationship between drift and saccades can be
postulated.
To study this corrective role of saccades relative to drift, a statistical
analysis was made of the resultant vectors of saccades and drifts (lengths of the
lines connecting the points of beginning and end of these movements). A
continuous record containing 250 saccades of three subjects (with the corre-
sponding drifts in each case) and 150 saccades and drifts for one subject (V.M.)
was subjected to statistical analysis. These portions of the record corresponded
to continuous fixation for a period of 2.5-3 min. The amplitude of the saccades
varied within wide limits - from 1 to 50' (Fig. 29), but the saccades most
frequently found in different subjects differed in amplitude (7-14' of arc in
L.A., 5-11' in N.B., 7-14' in l.s., and 15-24' in V.M.). The amplitude of drift
varied from 0 to 40' of arc and varied within wide limits in different subjects
(1-6' of arc in L.A., 2-7' in L.A., 2-7' in N.B., 3-9' in I.S., and 16-25' in
V.M.).

L.A. N.B.
•
o
• 0 o.
o • 0 0

• 0
• • 0

I.s. V.M.

• • 0
0
•• 0

•
0 ••

• • • • •• • 0 0 0 00

• • • o oo 00

•••• ••••
0
00
•
0
o • 0
0 0 0
0
0 0
•
Figure 28. Orientation of saccadic eye movements during fIXation (tests on the same
subjects as in Fig. 27). Solid circles show the beginnings of saccades, open circles their ends.
 20 20

'#. 15 15 IS ~

?ic 10 10
Q)
~
C"
~
'Po
Q) 5
>
.~
2.5
.!!!
Q) L
a: 3040500 10 20 30 40 o 30 40
o 10 o 10

Amplitude of saccades, min

25

* :~, 20H , 20
>-
(.)
c
~ 15~ ISH 15 r I 15
C"
Q)
...
'Po

~ 10J \ IO~ 10H \ 10

.~

co
Qj

~5~ s
2.5 2's~ 2~U 2,5 g
0 10 20 0 10 20 0 10 20 0 10 20 30 ~O

Amplitude of drifts, min

~
Figure 29. Unidimensional distributions of amplitudes of resultant vectors of saccades (top) and drifts (bottom) in subjects L.A., N.B., I.S.,.and
~
Y.M. The relative frequency is the ratio between the number of points within a given interval and the total number of points.
FIXATION MOVEMENTS OF THE EYES SI

Comparison of the distribution of amplitude of the drifts and saccades in

the different subjects showed different relationships between them. The ampli-
tudes of the saccades were greater than the amplitudes of the drifts in the first
three subjects. In subject V.M., however, the curves of distribution of amplitudes
of the saccades and drifts almost completely coincided. The amplitudes of the
saccades and drifts were greater in this case than in the other subjects.
The reason for this difference in the relationship between the amplitudes
of drifts and saccades was investigated by analysis of the directions of these
movements (Fig. 30). In subject L.A., the saccades were relatively clearly
oriented in two opposite directions. In subject N.B., the orientation of the
saccades was less regular in character, but the predominant orientation within a
wide range was in three directions. In subject I.S., the orientation of the saccades
was less regular still, but within a narrower range than in N.B. In subject V.M.,
the saccades were relatively clearly oriented, but in one direction.
Drift was also clearly oriented in this subject V.M., but in the opposite
direction of the saccades. In subject L.A., in whom the saccades were oriented in
two opposite directions, drift was irregular. In subjects N.B. and I.S., drift also
was not strictly regular, but nevertheless it was most frequently in directions
opposite to the saccades. Relationships between the orientation of the saccades
and that drifts thus differ: from complete absence of any connection between
their orientation, on the one hand, to definite orientation in two mutually
opposite directions, on the other.
To judge whether saccades can correct displacement of the eye caused by
drift, it is useful to examine the distribution of directions of drifts and saccades,
allowing for their amplitudes, or the distribution of amplitudes allowing for
directions (Fig. 31). Such an analysis can show whether a corrective relationship
exists between drifts and saccades. In subject L.A., however, any such connec-
tion was completely absent. In subject V.M., the saccades completely compen-
sated for displacement of the eye through drift. In subjects N.B. and I.S., there
was partial compensation of drift by saccades.
The corrective relationship between drifts and saccades also affects the
temporal characteristics of these movements. In the writer's investigation, the
duration of drift varied from 30 msec to 8 sec (Fig. 32). The drift in different
subjects differed in duration. In subject L.A., with no corrective relationship
between drift and saccade, the duration of drift usually varied from 3 to 1000
msec, whereas the other drifts each lasted 5, 6, and 8 sec. The most common
durations of drift in subject L.A. were smaller in value than in the other subjects
(N.B., I.S., V.M.), in whom a corrective relationship existed between drifts and
saccades. The velocities of drift varied from 0 to 48' of arc/sec. The most
common velocities of drift found in subject L.A. were the smallest (2-6' /sec).
whereas in subject V.M., they were the largest (13-25'/sec).
These investigations show that in a given subject, there is a definite
 III
N

20
>R. l.A. loS. N.B. 351 II V.M.
"> 15 1S lSr

100 150 JOO 250 300 35010 50 90 SO 100 150 200 250 JOO 35010 50 50 100 150 200 250 JOO J5010 50 50110170230
Angle, deg
20 40

15 ~~ ~
I

70 f- ./ \ 20
>-
*'O~IO
%! g 5 5
.- QJ 5f.. J " 10
~ ~ 2.5 2.5, J , , " , '" , '" J' "=, J' '" J I IIII J I III

.... 100 150 200 250 JOO J5010 SO 100 50 100 150 - - 700 ISO 700 250 300 J5070 50 230 310

Angle, deg
Figure 30. Unidimensional distributions of spatial orientation (directions of resultant vectors) of saccades (top) and drifts (bottom) in subjects
L.A., 1.5., N.B., and Y.M. ~
~
FIXATION MOVEMENTS OF THE EYES S3

relationship among the different characteristics of the eye movement. For

example, in subject L.A., slow speeds of drift corresponded to small amplitudes,
a mainly short duration, and irregularity of direction of drift, and also to the
absence of a mutual relationship of correction between drift and saccades. Strict
orientation of drift accompanied by an increase in its velocity, amplitude, and
duration, and by the presence of clear correlation between drifts and saccades,
were observed in subject Y.M.
Analysis of the experimental material suggests that there are different
types of fixation, in which different relationships between drifts and saccades
are observed. In some subjects, there is no form of correlation between drift and
saccades (e.g., in subject L.A., Fig. 31). In such cases, the drift has no definite
orientation, and the duration of individual drifts and their velocity are very
small. The amplitUde of individual drifts is several times smaller than the
amplitude of the saccades, and this is one sign of absence of correlation between
them. The saccades in these subjects have a clear spatial orientation and are
aimed in two mutually opposite directions, so that each compensates for
displacement of the eye caused by the other. Under these conditions, the points
corresponding to the beginnings and ends of the saccades lie in the same region.
Correlation is observed in these cases between the saccades in different
directions, and there is no correlation between saccades and drifts. The absence
of correlation between drifts and saccades does not rule out the possibility of
correction of displacements of the eye due to drift. st. Cyr and Fender (1969)
consider that correction of displacements of the eye during fixation is carried
out by drift as well as by saccades. In their opinion, drift is particularly
important for correcting eye displacements caused by convergence and diverg-
ence.
Organization of fixation micromovements of the eye of a fundamentally
different character was observed in subjects in whom close correlation was found
between drifts and saccades. The saccades in these subjects were in a direction
opposite to drift; the mean amplitudes of the saccades and drifts were almost
exactly the same. The amplitude of the saccades in these subjects was greater
than in the others, and not only the amplitude but also the duration and velocity
of the drifts were increased.
Besides these two fundamentally different types of organization of
fixation movements of the eyes, with clear correlation between drifts and
saccades or with complete absence of such correlation, an intermediate type of
organization of the micromovements of the eye is observed in some subjects. In
these subjects, some saccades are aimed in two mutually opposite directions, so
that one compensates for displacements of the eye caused by the other, whereas
the other saccades compensate for displacements of the eye by drift.
Different types of organization of fixation micromovements of the eyes
are thus observed in different subjects, and they are determined mainly by the
54 CHAPTER TWO

N.B.

t80· f---t----!-;t-"E:O ~=-~;:;-t-;=-IJ80' O·

800

Figure 31. Spatial orientation of micro movements of the eye. Each coordinate grid shows
the distribution of amplitudes of saccades (unshaded area) and drifts (shaded area) by
direction in subjects L.A., N.B., I.S., and V.M. in polar coordinates. The amplitude p is
plotted in minutes of angle. In the construction of the graphs, the amplitudes of all drifts
FIXATION MOVEMENTS OF THE EYES ss

(saccades) were added together in the interval ¢ < () < 100. To the right of the coordinate
grids are shown the regions of displacement of the optic axis during fixation in the same
subjects, with the maximum diameter shown in minutes of angle.
 30
~
25

20

15
L.A. 1.5.

> JO
CIl t.l
> c
. - CIl
~IO~
~ S- 5

~ ~ 2 . 5 , WI, I i PI i

a 1000 JOOO 5000 o 1000 2000 o 1000 o 7000 2000

Duration of drift. msec

20

15~ I 1 15

CIl
>-
t.l
C 10
.~ ~
~g
CIl ...
a:~ 5

2.5L,~tre ~
';", , . ':U\
0 10 20 30 40 SO 0to 20 30 40 500 70 20 30 40 500 10 20 30 40 50 ~,.,
Drift velocity. min/sec
Figure 32. Temporal characteristics of drift. Top: Univariate distributions of durations of drift in subjects L.A., N.B., I.S., and V.M. Bottom:
~
Univariate distributions of mean velocities of drift in the same subjects.
FIXATION MOVEMENTS OF THE EYES 57

character of interaction between drift and saccades. The amplitude-time

characteristic curves of drifts and saccades depend on the type of interaction
between these micro movements.
A defmite type of organization of fixation micromovements of the eye is
persistently found in a given subject during repeated tests over a long period of
time. The same type of organization is found when fixation micromovements of
both eyes are tested in the same subject. The maxima of the curves of
distribution of amplitudes of saccades and drifts of the right and left eyes
coincide with great accuracy (to within 2-3' of arc). The maxima of the curves
of distribution of drift velocities for the right and left eyes also coincide with
great accuracy (to within 1'/sec). At the same time, the difference between the
maxima of the curves of distribution of the direction of drifts and saccades in
the two eyes is somewhat greater than for the amplitudinal and temporal
characteristics, and in some subjects amounts to 60-70°.
The sufficiently close coincidence between the averaged characteristics of
fixation micromovements of both eyes still does not mean the complete identity
of these movements at every particular moment. The difference between
instantaneous values of amplitude of a saccade or drift is more often 3-4'. At
individual moments, however, this discrepancy between the movements of the
two eyes is considerably increased, and both drifts and saccades may in some
cases be in opposite directions.
The spatial organization of fixation micromovements of both eyes in two
subjects (N.P. and N.Z.) is shown in Figs. 33-35. In the case of subject N.P.,
most of the saccades displace the eyes in mutually opposite directions, and a
minority of saccades correct drifts (Fig. 33). The same type of organization in
this case is characteristic of both eyes. In subject N.Z., on the other hand,
saccades in the two eyes are opposite to drifts in direction, and they compensate
for displacement of the eye through drifts (Fig. 34). In darkness, in subject N.Z.,
the type of organization of the micromovements was modified: many of the
saccades acquired a different orientation, and most were aimed in two opposite
directions (Fig. 35).
The least variable characteristic of the micro movements of the eye is the
area within which the optical axis moves (Fig. 31). In the writer's investigations,
the maximum diameter of this area did not exceed 80-100' of arc; i.e., it
corresponds approximately to the dimensions of the fovea centralis of the retina.
In the absence of a fixation stimulus (in complete darkness), this area is
appreciably increased (by 2-3 times), and it no longer corresponds in size to the
fovea centralis of the retina (Figs. 36 and 37).
Comparison of these results with the character of the micromovements of
the eye in subject I.S. during fixation on a stationary point (see Figs. 27-32)
shows a change in the relationships between drift and saccades (in darkness, the
saccades started to compensate completely for the drifts). The most commonly
S8 CHAPTER TWO

Figure 33. Spatial orientation of micromovements of the two eyes. Monocular fixation in
subject N.P. is carried out by the right eye. The solid line represents the right eye, the
dashed line, the left eye. Remainder of legend as in Fig. 31.

observed durations of drifts were increased by 2.5 times; there was also an
increase in the amplitude of the saccades (by 2-3 times) and drifts (by 4-5
times). The velocity of drifts was increased by 6-7 times, reaching 120~ of
arc/sec.
Comparison of the velocity of drifts under different conditions (in the
presence or absence of a fixation stimulus) can serve as a basis for a conclusion
on the corrective role of drifts during fixation on a stationary point. According
to Comsweet (1956), drift has the same velocity when a fixation stimulus is
present and in darkness. On the basis of these findings, he considers that drift of
the eye is independent of visual afferentation, and is due to instability of the
oculomotor system, whereas correction of the displacements of the eye during
fixation is carried out exclusively by saccades. In the writer's own investigations,
on the other hand, a marked increase in the velocity of drift was found on
exclusion of the fixation stimulus. The corrective interaction between drift and
saccades was also increased. These findings provide solid grounds for the
suggestion that drift depends on visual afferentation and, together with saccades,
helps to correct displacement of the eye.
FIXATION MOVEMENTS OF THE EYES 59

Figure 34. Spatial orientation of micro movements of the two eyes. Monocular IlXation in
subject N.Z. is carried out by the right eye. Legend as in Fig. 33.

Analysis of the writer's fmdings indicates that not only the velocity but
also the duration of drift increases in darkness; i.e., the frequency of the
saccades is decreased. These findings could point to the dependence of the
frequency of saccades on visual afferentation. In that case, however, it would
have to be considered that not only the character of visual afferentation, but
also the motor task, is altered in darkness. In the absence of a fixation stimulus,
the subject must keep his eye in a specific fixed position.
According to Florentini and Ercoles (1966) and Steinman et al. (1967),
the character of micromovements of the eye under stable conditions of
illumination depends largely on the motor task: in response to an instruction to
fix on a stationary point, the frequency of microsaccades of the eye is greater
than to an instruction to hold the eye in a certain position. On the other hand,
during the concentration of attention on the solution of arithmetical problems,
the number of microsaccades of the eye decreases sharply (Filin and Sidorov,
1972). Not only visual afferentation, but also other systems, thus participate in
the correction of eye displacements during fixation.
The functional role of the proprioceptors of the eye muscles has not yet
60 CHAPTER'IWO

90°

Figure 35. Spatial orientation of micro movements of the two eyes in darkness. Investigation
of the same subject (N.Z.) as in Fig. 34. Legend as in Fig. 33.

14

21
Figure 36. Trajectory of movement of the optical axis of subject I.S. during a stay of 10 sec
in darkness. The numbers denote successive positions of the axis.
FIXATION MOVEMENTS OF THE EYES 61

180°r----i-----+____-+~~
~=--i"-;-;::;::_---~:---"--I'-----_J 3600 00
600

?f2- 10
>-
u
c
OJ
::l
C"
....~

o 1000 2000 3000 4000 5000

Duration of drift, msec

Figure 37. Micromovements of the eye in darkness. Top: Distribution of amplitudes of

saccades (unshaded area) and drift (shaded area) by direction in subject I.S. in darkness in
polar coordinates. p is the amplitude in minutes of arc. Bottom: Unidimensional distri-
bution of durations of drifts in subject I.S. in darkness.

been established by either psychophysiological (Brindley and Merton, 1960) or

electro physiological investigations (Keller and Robinson, 1971).
In the opinion of Matin et al. (1970), perception of a discrepancy between
the "effort" that arises when holding the eye in a certain position and the
"memory" of the "effort" that was applied during fixation on a stationary point
62 CHAPIERTWO

is of significant importance in the correction of eye displacements. The term

"effort" used by these workers is very close in meaning to the concept of
"motor image" of movement as used by N.A. Bernshtein. The existence of such a
"motor image" of fixation movements of the eyes is also confirmed by the
observations of Skavenski and Steinman (1970). These workers instructed the
subjects to make 30 voluntary saccadic movements of the eyes in different
directions in the course of a stay of 50 sec in darkness before returning the eyes
to the position of preceding fixation. The error that appeared under these
conditions did not exceed the changes in position of the eye that occurred in the
same subjects when they were instructed to hold the eyes in the position of
preceding fixation during the stay of 50 sec in darkness.
It is interesting to note that rnicronystagmus in a healthy person in
darkness resembles in its quantitative characteristics the nystagmus observed
during fixation on an illuminated fixation stimulus by patients with a patho-
logical lesion affecting the brainstem. The trajectory and quantitative charac-
teristics of drift in a patient with a neurofibroma of the auditory nerve in
daylight (Figs. 38 and 39) resemble the same quantitative characteristics of
rnicronystagmus in a healthy subject in total darkness (see Figs. 36 and 37). It
can be postulated that in this pathological condition, the functioning of the
mechanisms of the most delicate and fine stabilization of the optical axis are
disturbed, whereas the mechanisms of coarser stabilization of the gaze continue

L
20 /
20'

7
15

Figure 38. Trajectory of displacement of the optical axis during fixation for 10 sec by a
patient with a neurofibroma of the right auditory nerve. The numbers denote successive
positions of the axis.
FIXATION MOVEMENTS OF THE EYES 63

15

"#.
~70
c:

-
(I.)
:l
C"
....
(I.)

( I.)
>
.~ 5
Qi
a::
2.5

200 400 600 800 1000 200 400 600 800 2000 200 400 600

Duration of drift, msec

Figure 39. Unidimensional distribution of durations of drift in a patient with a neuro-

fibroma of the auditory nerve.

to function. Electro-oculography is an adequate method of investigating nystag-

mus with a higher amplitUde occurring under pathological conditions (Blago-
veshchenskaya, 1968).
An essential condition for functioning of the system of most accurate
stabilization of gaze is the presence of central vision: in patients with absence of
central vision, an increase in the amplitUde of drifts and saccades of the eye
compared with the amplitude in healthy subjects was observed (Fig. 40).
However, the interaction between drifts and saccades and the temporal charac-
teristics of the movements in these patients were not significantly different from
normal.
These investigations of fixation micromovements of the eyes show differ-
ences in the variability of the different parameters. The area of displacement of
the optical axis during fixation on a stationary point for a long period of time is
the least variable. This area corresponds in size to the most sensitive area of the
retina, the fovea centralis. The quantitative characteristics of individual drifts
and saccades are much more variable - from complete compensation of drifts
by saccades to their complete independence so far as correction is concerned.
The invariance of the area of displacement of the optical axis is deter-
mined mainly by the constancy of the task (fixation on a stationary point). At
the same time, the variance of the means by which the task is performed (the
quantitative characteristics of individual drifts and saccades and the interaction
between these movements) is also determined by the functional state of the
64 CHAPTER TWO

fO'L 10'

Figure 40. Displacement of the optical axis during fixation on a stationary point by a
patient with central scotoma. The record was made on stationary film with the use of a
Yarbus cap. Not only the amplitude of saccades, but also the velocity of drift of the eye, is
increased in the patient with central scotoma. Some saccades change their orientation
sharply in the course of movement.

oculomotor apparatus. A change in the task (an attempt to fix on an imaginary

point in darkness or in diffuse light, in the absence of a fixation point) leads to
an increase in the area of displacement of the optical axis, although the means of
performing this new task (individual drifts and saccades) are also changed - their
amplitude being increased by several times.
These results are thus further confirmation of the views expressed by
Bernshtein (1966) on the invariance of the final result of an action in accordance
with its purpose and the variance of the means of achieving this purpose.

Plasticity of the System for Stabilization of Fixation

Despite the varied and complex character of eye movements, during

fixation on a stationary point, the optical axes do not diverge Significantly from
the object examined. This holding of the eye in a certain position unquestionably
depends on afferent stimuli from the retina. To study the dependence of
micromovements of the eye on the character of these stimuli, experiments were
carried out in which the visual afferentation was modified. A Yarbus cap, the
anterior surface of which was covered by a transparent glass window, was used,
and a small mirror was fixed in front of it at an angle of 45°. The image of the
surrounding objects falls on the retina after reflection from this mirror (Fig. 41).
According to the laws of optics, turning the mirror through an angle a causes a
beam of light reflected from it to be deflected by twice that angle (2a).
Displacement of the images of surrounding objects, reflected from the mirror on
FIXATION MOVEMENTS OF THE EYES 6S

/.,.IL------- A

2- r-----

5~
6 _________________

1 sec
Figure 41. Electrooculographic recording of eye movements during examination of a
stationary point through a mirror Itxed to the eye (curves 3-6). Curves 1 and 2 show the
calibration of displacements of the eye through an angle of ISo without the mirror. At the
left is a diagram of a Yarbus cap giving a mirror image of surrounding objects on the retina.
(A) Fixation point; (AI) projection of IlXation point on the retina.

the retina, thus takes place at twice the speed and in the opposite direction. The
subject was instructed to fix on a stationary point (a neon lamp). After a small
movement of the lamp during this fixation, the subject developed the illusion
that the fixation point was oscillating in the field of vision. At the same time,
eye movements began to take place and were recorded by an electrooculographic
method.
At the beginning of the test (see Fig. 41), the eyes performed smooth
oscillatory movements of high amplitude and low frequency, resembling in
character the "floating" movements of the eyes in patients in a comatose state.
After a short time, these "floating" movements began to be interrupted by
saccades, a coarse nystagmus appeared, and its amplitUde decreased: 1.5-2 min
after fixation of the cap to the eye, the subject could fix his gaze relatively
steadily on the stationary object. Within a short time, the "floating" movements
of the eyes were thus replaced by steady fixation.
This successive change in the character of movements of the eyes is
66 CHAPTER TWO

evidence of the plasticity and the complex functional tuning within the system
of innervation of the eye muscles. The plasticity of this system was discovered
by Bechterew (1883), who sectioned the vestibular nerve in a rabbit and
observed the development of spontaneous nystagmus, which gradually disap-
peared after a few days. If the opposite vestibular nerve also was then sectioned,
nystagmus developed in the opposite direction, and this nystagmus also disap-
peared after a few days. If both vestibular nerves were sectioned at the outset,
nystagmus did not develop. The gradual disappearance of nystagmus after
unilateral division of the vestibular nerve is due to complex processes of
functional tuning in the central components of oculomotor innervation.
It can be postulated that one of the structures concerned in the
stabilization of fixation is the "eye-centering system" described by Bender
(1955): stimulation of the brainstem reticular formation in anesthetized
monkeys in any part leads to rotation of the eyes into the mid position. The
most important feature distinguishing the function of the "eye-centering system"
is its plasticity. According to Hyde (1964), during repeated stimulation of a
particular site in the brainstem, the eyes always remain in a specific fixed
position irrespective of their initial position. Presumably the "eye-centering
system" plays a role in keeping the eyes in a certain position regardless of their
displacement as a result of drifts and saccades. Stimulation or destruction of any
part of this extensive system can lead to the appearance of a more rapid drift in a
certain direction and to the appearance of spontaneous nystagmus. In lesions of
the rostral areas of the brainstem, vertical, rotatory, and converging nystagmus
arises, but in a lesion of the caudal areas, the nystagmus is horizontal. It can be
postulated on the basis of these findings that different parts of the "eye-
centering system" play different roles in the prevention of displacement of the
eye in different directions. It will be recalled that as Bender himself found, this
"eye-centering system" coincides in its location with the reticular formation of
the brainstem.
Szentagothai (1964) states that neurons of the reticular formation are
connected with motoneurons of the eye muscles by special small synapses that
differ markedly in structure from the large synapses located on the same
motoneurons, and that are responsible for the "rigid" connections of the
oculomotor system. In Szentagothai's opinion, the small synapses between
neurons of the reticular formation and motoneurons of the eye muscles create
favorable conditions for the "plastic" operation of the oculomotor system and
for the functional adjustments taking place in it.
 CHAPTER III

Tracking Movements of
the Eyes

During the perception of images moving in the field of vision, tracking

movements of the eyes arise. These movements assist in keeping the image
within the zone of optimal vision, and at the same time, they prevent adaptation
of the retinal receptors. These movements can appear only if the visual system
carries out continuous assessment of the velocity and direction of movements of
the object followed.

VJSual Perception of Moving Images

The perception of movement is of very great biological importance, for it
contributes to protection against harmful factors and to the organization of
many other behavioral responses.
For central vision, the minimum velocity perceivable by man is 1-2' of
arc/sec, and the maximum velocity is 12-32°/sec (R. H. Brown, 1961). At the
periphery of the retina, sensitivity to the perception of movement is much less
than in the region of the fovea centralis.
The results of psychophysiological tests of movement perception have now
been supplemented by recording of the activity of neurons responding to
movement of images in the visual field. A definite relationship has been
discovered in the retina between the firing rate of the neurons and the velocity
of movement of a visual stimulus. In the frog retina, this relationship holds good
over the range of velocities from 0.1 to 70° /sec (Kostelyanets, 1965). In the
pike, retinal neurons that respond to slow movements and neurons that respond
to fast movements have been identified (Zenkin and Pigarev, 1969). The
67
68 CHAPfER THREE

selective sensitivity of different neurons to different velocities of movement of

the visual stimulus has also been discovered in the rabbit retina (Barlow et al.,
1964). Neurons with the function of direction detectors, which responding with
the maximum number of spikes to movement of an object in one particular
direction, have been found in the retina of several animals (Barlow et aI., 1964;
Oyster, 1968; C. R. Michael, 1968). In the rabbit, these neurons are divided into
four groups - those sensitive to movement of the stimulus upward, downward,
to the right, and to the left (Oyster, 1968). In fishes, a similar subdivision of the
direction-detector neurons has been observed; in this case, the number of
neurons that are sensitive to horizontal movements of the visual stimulus is
greater than the number that respond to vertical movement (Cronly-Dillon,
1964).
The retina transmits information via a phylogenetic ally older pathway to
the mesencephalon and also through the lateral geniculate body to the cerebral
cortex. Neurons that respond to movement and possess selective sensitivity to a
certain direction have been found in the geniculate body of the cat (Kozak et al.,
1965).
Neurons that respond to movement of a visual stimulus within the field of
vision have been found in the visual cortex of rabbits, cats, and monkeys
(Vinogradova and Undsley, 1963; Arden and Ideka, 1967; Rubel and Wiesel,
1962, 1968). In cats and monkeys, neurons have been found that do not
respond to light, but are excited by movement of the stimulus in two opposite
directions or in the same direction. A distinguishing feature of the cortical
neurons is their selective sensitivity in their response to movement: their
response is completely inhibited during movement of the stimulus in a perpen-
dicular direction. Many visual cortical neurons possess selective sensitivity to a
certain velocity of movement of the visual stimulus. This "detection" of the
velocity of movement is carried out within limits of 0.1-20° /sec.
Neurons that detect direction and velocity have also been found in the
mesencephalon of rabbits and cats (Hill, 1966; Straschill and Taghavy, 1967;
Walley, 1967; Mcllwain and Buser, 1968). In cats the selective sensitivity of
neurons to the velocity of movement of a visual stimulus varies within wide
limits - from 0.5 to 20° /sec. The selective sensitivity of neurons of the superior
colliculus to the velocity of movement corresponds to the horizontal and vertical
axes of the visual field (upward, downward, to the right, to the left). Each
direction-detector neuron possesses selective sensitivity to movement in one
particular direction. On deviation from this direction by 45°, its sensitivity falls,
and with an even greater deviation, unit activity decreases sharply. If the
direction of movement is reversed, however, the response of the neuron
decreases or disappears completely (Straschill and Taghavy, 1967). After
removal or local chilling of the visual cortex, the selective sensitivity of
mesencephalic neurons to the direction of movement of the visual stimulus is
TRACKING MOVEMENTS OF THE EYES 69

lost (Wickelgren and Sterling, 1969). These findings may indicate that the
selective sensitivity of mesencephalic neurons to the direction of movement
depends on descending influences of the visual cortex, not on direct connection
with the retina. The presence of neurons sensitive to movement of an image in
the visual field at different levels of the visual system is of great importance to
the organization of tracking movements of the eyes.

Mechanisms of Extrapolation in the Control of Tracking Movements

of the Eyes

Smooth tracking movements of the eyes appear 0.15-0.17 sec after the
appearance of a moving object in the field of vision, and the velocity of these
movements synchronizes immediately with the velocity of displacement of the
target. The minimum velocity of movements of a visual stimulus that will evoke
a tracking movement is 5' of arc/sec, approximately the same as the threshold
of movement perception (Yarbus, 1965). With an increase in the velocity of the
object followed, the eye lags behind by a gradually increasing amount. At the
same time, the velocity of movement of the image over the retina increases, and
this increase is evidently the reason the visual acuity falls. One of the causes of
the decreased visual acuity with an increase in the velocity of movement of the
tracked stimulus over 60-70° /sec is the appearance of saccadic eye movements
(Reading, 1972). Smooth tracking movements of the eyes occur only if a moving
stimulus is in the field of vision. If no such stimulus is present, an attempt to
shift the gaze smoothly will be unsuccessful, and the eye movement will consist
of a series of stops and saccades. Analysis of the microstructure of tracking eye
movements shows that these movements repeat the trajectory of the stimulus
followed, changing their direction and velocity without any corrective saccades
(Fig. 42).
The smooth character of tracking movements of the eyes during changes in
direction and speed of the tracking stimulus is produced by a special mechanism
of prediction (extrapolation), which evidently functions in accordance with N.
A. Bernshtein's principles of "looking into the future." This mechanism provides
information on the position of the stimulus at a future moment of time on the
basis of data for its position at present and past moments. On the basis of this
information, an action "program" is formed and is manifested basically as
smooth tracking movements of the eyes. The role of the extrapolation mech-
anism in control of eye movements is seen particularly clearly with the sudden
appearance of moving stimuli at the periphery of the field of vision (Westheimer,
1954; Lauringson and Shchedrovitskii, 1965; Shakhnovich et at., 1965; Yarbus,
1965). In this case, the eyes carry out saccadic movements in response to the
new stimulus 200-300 rnsec after its appearance. During this latent period, the
stimulus moves through a certain distance from the point at which it appeared.
70 CHAPTER THREE

Figure 42. Micromovements of the eye during the tracking of a point making oscillatory
movements in the field of vision with an amplitude of 1° (recorded by Yarbus's method
with a spot of light on a moving film without any slit diaphragm in front of the film).

The saccadic movement of the eyes takes place with a correction for this
displacement of the stimulus, and immediately after the end of the movement,
smooth tracking movements of the eyes begin; in their direction and velocity,
they correspond exactly in character to the moving stimulus (Fig. 43). During
the latent period of the saccade, not only is the position of the new stimulus at
the moment of its appearance assessed, but also the velocity and direction of its
movement are computed and its position by the time the saccade ends is
extrapolated.
The extrapolation of the trajectory of eye movement can be found during
tracking even if the visual stimulus moving in the field of vision unexpectedly
disappears. After disappearance of the stimulus, the eyes continue to move for
some time along the curve repeating the trajectory of the preceding movement
of the stimulus, allowing for changes in the velocity and direction of its
movement. This phenomenon can be explained on the grounds that during
tracking, the trajectory of stimulus movement is extrapolated to some particular
moment of time ahead.
The chief characteristic of extrapolation is its duration, which varies from
200 to 550 msec, but is usually on the order of 300 msec. The smoothness of

1,,-j

0.5 sec
Figure 43. Electrooculogram of the initial period of tracking movements of the eyes. The
number 1 indicates the appearance of the stimulus to be followed.
TRACKING MOVEMENTS OF THE EYES 71

the tracking movements of the eyes evidently depends on the functioning of the
extrapolation mechanism. If a visual stimulus moving in the field of vision
periodically disappears, the tracking movements of the eyes lose their smooth-
ness only if the periods of disappearance of the stimulus exceed the duration of
extrapolation (300-350 msec). These findings are in agreement with the results
of psychophysiological and electrophysiological investigations. A person's sensa-
tion of movement is undisturbed even if the separate stationary points are
presented consecutively at time intervals of up to 400 msec and are located on
the retina at distances of up to 5° of arc from each other (Graham, 1951).
Microelectrode investigations have shown that the responses of the ganglion cells
of the retina are identical to flashing and movement stimuli if the interval
between the photic stimuli does not exceed 200 msec (c. R. Michael, 1968) and
the difference in the spatial projection of these stimuli on the retina does not
exceed 0.5° of arc (Barlow and Levick, 1965). A change in the position of the
stimulus on the retina thus acts as the signal for movements. There is no need,
however, for successive stimulation of all receptors.
Disappearance of the smoothness of following movements of the eyes and
their fragmentation into a series of stops and jerks are observed in various types
of pathology (Fig. 44).

~·L 2

1 sec

Figure 44. Fragmentation of tracking movements of the eyes in a patient with a tumor of
the frontal lobe. Electrooculogram: (1,2) Optokinetic nystagmus to the right and left; (3)
tracking movements of the eyes; (4) saccadic eye movements.
72 CHAPTER THREE

The question of the structural and functional organization of the mech-

anisms of extrapolation of following movements of the eyes is extremely
difficult and requires further study.

Electrical Activity of the Ocular Muscles During Tracking Movements

of the Eyes

To understand the mechanisms controlling eye movements, it is important

to study the behavior of single neurons at different levels not only of the visual
system, but also of the oculomotor innervation.
The functional state of motoneurons of the eye muscles can be estimated
by recording the activity of the motor units electromyographically. The
simplicity of this method presents great opportunities for the study of the
peripheral neuromotor system of the eye muscles under natural conditions
(Bjork and Kugelberg, 1953).
The motor unit is composed of a motoneuron, the axon arising from it,
and the group of muscle fibers innervated by it. By recording electrical impulses
with a needle electrode inserted into these muscle fibers, objective information
can be obtained on the functional state of the motoneuron. Recording of this
type, however, must not disturb the conditions for normal functioning of the
muscle. In the experiments of Matyushkin (1961, 1963), a tendon of an ocular
muscle was separated from the eye and the muscle was stretched in a bath of
mineral oil, where the conditions were favorable for recording the activity of
single motor units of the eye muscles. The disturbance of the muscle balance of
the eye and the change in the normal character of the stretch reflexes, however,
could have some effect on the results of the tests.
The writer investigated motor units of the eye muscles in rabbits without
detaching the tendons of these muscles from the eye, i.e., under natural
conditions (A. R. Shakhnovich and Nebieridze, I 967a,b ). The animal was fixed
to a wooden board inside a drum, on the inner white surface of which black
vertical strips were glued. The drum was rotated in both directions at constant
velocity (1 revolution in 10 sec). The electrooculogram was recorded by means
of needle electrodes inserted subcutaneously in the immediate vicinity of the
outer and inner angles of the palpebral fissure. A needle electrode was inserted
into the lateral or medial rectus muscle of the eye in order to record the
electrical activity of these muscles. The electrooculogram and electromyogram
were recorded simultaneously on a loop oscillograph. Altogether, 98 motor units
were recorded. The functional state of each motor unit was assessed with the
drum stationary and during its rotation in both directions, when optokinetic
nystagmus developed.
Analysis of the results showed that with the drum stationary, the intervals
between impulses of different motor units varied from 12.5 to 50 msec. These
TRACKING MOVEMENTS OF THE EYES 73

100
Il V
I 0.05 sec

Figure 45. Electrical activity of two motor units. Ocular muscles at rest.

intervals, however, were fairly constant for a given motor unit. Individual motor
units functioned independently (Fig. 45). Rotation of the drum led to the
appearance of optokinetic nystagmus in the animals. The firing pattern of
one-third of the motor units was unchanged under these circumstances
(Fig. 46A). The firing pattern of two-thirds of the total number of units
recorded was connected with the rhythm of nystagmus (Fig. 46B,C).
During tracking, a definite relationship is found between the character of
discharge of the motor unit and the duration of the phases of nystagmus (Figs.
47 and 48). The interval between spikes in this case decreases by an exponential
law
T=Ae-bt+C
where T is the interval between spikes; A is a constant equal to T - C when
t = 0; t is the time after activation of the motor units, and C = T min is the
interval between spikes when t -+- 00, i.e., the value of the interval as established
between spikes for the second phase; € = lib is the time constant of the given
motor unit, the time during which the duration of the interval between spikes
reaches the fraction lie of its initial value at time t = 0 (e is the base of natural

A BIIII rill'llllli 1\11111111111111111 tttJj 11111H1111111111111111111' 11111111I11111~tto

1001 ~

Il V r 0.1 sec
B 1111111111, I III\i'I"IIII'·" I
iii ' ,11111

elllllllllllllill II\! 1111111::111 11:1 IH\lIIIIIIIIIII111111111UIIIH.I:IIIIIIII

I:

------~------------------------------------~~
Figure 46. Electrical activity of ocular muscles during optokinetic nystagmus. In each pair,
the top curve is the electromyogram, the bottom curve, the electrooculogram. (A) Motor
unit that does not alter its firing pattern during optokinetic nystagmus; (B,C) motor units
that alter their firing pattern during optokinetic nystagmus; (B) agonist muscle of saccade,
(C) agonist muscle of tracking.
74 CHAPTER THREE

• • ••••• +H H H
II' I I' '~' I tl'III' ~ II~r~ ij'H~
t t + t • • • • t • • • HH HHHHHUHHHH
I til ~J ~ 11111'ij'ijd'dIH'il~P~J",jl"J~'I\H'lu~H~llp~I~,'~~jl'!
B

0.1 sec
c
T
0,05 3,5
4,5
D
5,5
6,5
0,02
7.5
ao!
'--_-'-__'--_--'-_----' t. sec 8.5
0,2 0.4 0,6 0,8 {e(T-T;"in)

Figure 47. Activity of motor units of an ocular muscle during slow phases of nystagmus of
different duration, (A,B) Electrical activity of lateral rectus muscle during slow phases of
nystagmus of different duration. In each pair, the top curve is the electromyogram, the
bottom curve, the electrooculogram. Arrows indicate the spikes generated by the same
motor unit. (C) Changes during interspike intervals T indicated by arrows in A and Bare
plotted against the time from activation of the motor unit, t. The solid curve and the open
circles show changes in interspike interval during the short phase of tracking (A), and the
dashed curve and the solid circles show changes in interval during the long phase of tracking
(B), (D) Logarithm of interval as a function of time for the same motor units, The natural
logarithm of the interspike interval is plotted against the time from activation of the motor
unit, t.

72
_ /0
U
31 8
.g6
4
2

a8 1.0 1.2
Duration of tracking phase, sec
Figure 48. Time constant of discharge of a given motor unit as a function of duration of 14
consecutive phases of tracking during optokinetic nystagmus.
TRACKING MOVEMENTS OF THE EYES 7S

logarithms). Taking the logarithms of this expression yields a linear function,

thus confirming the exponential character of the relationship given above (see
Fig. 47). The time constant is then determined from the straight-line rule (Fig.
47 D). From the graph of time constant vs. duration of the slow phase of
nystagmus (Fig. 48), it can be concluded that the shorter phases of nystagmus
correspond to a smaller time constant of discharge of a given motor unit.
The relationship between the time constant of discharge of motor units
and the duration of the phase of tracking in nystagmus thus obtained enables a
number of suggestions to be put forward regarding the mechanisms whereby the
rhythm of nystagmus is controlled. It can be concluded from these results that
the firing pattern of the motor unit at the beginning of the slow phase of
nystagmus can be used to predict the duration of that phase and the time
interval after which the next saccade will arise. The duration of the slow phase
of nystagmus is thus determined at its origin. The existence of a definite
"pacemaker" of nystagmus can be postulated in the nervous system. This
"pacemaker" constantly produces the "microprograms" of nystagmus that
determine the duration and character of its subsequent phases. In accordance
with this "program" of each separate phase of nystagmus, the character of
discharge of the motor units (their time constant) is determined at the very
beginning. The important role of "anticipation" or "programming" in the
control of eye movements is also confirmed by the presence of postnystagmus
- a series of regular eye movements after withdrawal of the optokinetic
stimulus (Kislyakov and Neverov, 1966).
One cannot rule out the possibility that the duration of the individual
phases of nystagmus is determined by excitation of the stretch receptors of the
eye muscles at the end of the slow phase, and that this excitation acts as the
stimulus for the next saccade. The duration of the slow phase of nystagmus is
determined at its very beginning, however, and this is evidence against a role for
a peripheral mechanism in the regulation of the rhythm of nystagmus. That the
rhythm of nystagmus is independent of excitation of the receptors of the eye
muscles is also confirmed by the fmdings of De Kleyn and Magnus (1921), who
observed normal nystagmus after anesthesia of the eye muscles. Most probably,
the constant circulation of impulses around neuronal orbits, maintaining a
defmite state of excitation for long periods, plays the essential role in the
regulation of a rhythmic movement such as nystagmus (Lorente de No, 1935,
1939; Fessard, 1962).
With the great variability of the functional characteristics of individual
motor units, certain of their individual properties can be found, among which a
specific fixed order of activation and inactivation of individual motor units is
seen with particular clarity in the repeated phases of nystagmus (Figs. 49 and
50). The intervals between the moments of their activation and inactivation
vary, however, although only within narrow limits. During the fast phase of
76 CHAYI'ER TIlREE

Figure 49. Electrical activity of ocular muscles during optokinetic nystagmus. In each pair,
the top curve is the electromyogram, the bottom curve, the electrooculogram. The order of
activation of motor units (a, b, c) in repeated phases of nystagmus remains constant.

nystagmus, many motor units in the agonist muscles of the saccade are activated
simultaneously. These motor units cease to discharge both during the saccade
and after its end, i.e., at the beginning of the tracking phase. The order of
activation and inactivation of the different motor units in the repeated phases of
nystagmus is thus strictly regular in character.
The increase in electrical activity of the eye muscle during tracking is due
to gradual activation of fresh motor units, and also to an increase in their firing
rate.
The specific fixed order of activation of different motor units evidently
depends on the individual properties of the motoneurons of the eye muscles. For
skeletal muscle, such a dependence is well known. Henneman et al. (1965)
recorded the unit activity in five filaments of the first sacral ventral root during
stretching and relaxation of the triceps muscle. The order of appearance and
disappearance of activity in these fibers remained constant during stretching and
relaxation of the muscle. These workers explain this phenomenon by the
different sizes of the motoneurons. In small motoneurons, the surface of the
soma membrane is small, and for that reason, during activation of the synapses
the density of the depolarizing and hyperpolarizing current will be much greater
than with large neurons during excitation of the same number of synapses. In
small neurons, a steeper rise of the postsynaptic potentials ought therefore to be
expected in the region of the soma, with a correspondingly lower threshold of
excitation. In the investigations of Ashworth et al. (1967), who compared
voluntary activation of postsynaptic reflexes with monosynaptic activation of
motoneurons, in most cases the same order of excitation of identical motor units
was discovered. This structural hierarchy of the Q-motoneurons could be
modified under the influence of voluntary effort in only 20% of the motor units
studied. One cannot rule out the possibility that the specific fixed order of
activation of motor units during tracking depends on different sizes of the
motoneurons and, correspondingly, on differences in their threshold of exci-
tation. This author's observations, however, do not suggest that the order of
 o-j

~~
a b a b a b ~
~ H t t
~~j p ~ d~! 1:1 S +,... qi i'j11~~ 'H'~!" 'I ! I~ l~'I~ i- ~
t!l
s s e ••
~
o"%l
100 p.V II a b a b ab
~ ~ t t H :it!l
~~_ I i \1' I ~I l~j !H~_t~t~ j 'I b J
I j I. dl~' II j L~.4 1 ~
~
a b ab a b
~ t # t t
~\ I I I \i ~ ~~ ~ ~ It i II Ii I' ~. 1~~ • t , h f·
~ - .
0.1 sec
Figure SO. Activation of motor units in successive phases of tracking during optokinetic nystagmus. In each pair, the top curve is the
electromyogram, the bottom curve, the electrooculogram. Arrows a and b indicate repeated phases of nystagmus.

.....
.....
78 CHAPTER THREE

activation of motoneurons is strictly fixed regardless of the character of the

motor task.
Dear dependence of the character of the firing pattern of motoneurons
innervating the ocular muscles on the motor task was discovered in the
investigations of Robinson (1970). At rest, for every position of the eye, there is
a corresponding specific frequency of motoneuron discharge. During tracking
movements, though, this frequency may be increased or decreased (depending on
the direction of movement). The degree of this increase or decrease depends on
the velocity of the tracking movement. In Robinson's opinion, this differential
change in firing rate of the motoneuron during the performance of different
motor tasks (fixation and tracking) depends on the nature of function of the
supranuclear structures. For a given motoneuron, the ratio between the dis-
charge frequency and the velocity of the tracking movement is fairly constant.
The ratio differs for different motoneurons.
Thus, the visual system contains neurons that act as detectors of the
velocity of movement of the visual stimulus, and the effector motoneurons of
the oculomotor system show a clear dependence on the velocity of the tracking
movements of the eyes. Complex interaction between these various neurons lies
at the basis of the organization of tracking movements of the eyes.
 CHAPTER IV

Saccadic Eye Movements

With a change of the fixation points, saccadic movements of the eyes,

characterized by great speed and accuracy, take place. Saccadic eye movements
are of great importance for the visual perception of surrounding space.

Saccadic Eye Movements and Visual Functions

A decrease in perception during saccadic eye movements was familiar to
the very first investigators of eye movements (Dodge, 1900). Ditchburn (1955)
studied visual functions during saccadic eye movements with the aid of a contact
lens and mirror fitted to the eye. A beam of light reflected from this mirror was
projected onto a photoelectric cell. The potential generated in the photoelectric
cell was amplified and fed into a cathode-ray oscilloscope. Displacement of the
beam on the oscilloscope screen occurred only during saccadic eye movements.
This displacement of the beam on the oscilloscope screen could be observed by
the experimenter but not by the subject himself, on whose eye the contact lens
and mirror were fitted. Ditchburn concluded from these fmdings that visual
perception is considerably decreased during saccadic eye movements. The
perception of the afterimage during saccadic eye movements is also decreased or
completely absent (Yarbus, 1965). During saccades, the visual acuity and the
sensitivity to light fall by 1-2 logarithmic units (Volkman, 1962; Zuber and
Stark, 1966; J. A. Michael, 1967). The recognition of pictures presented during
saccadic eye movements is also impaired (Yakimov, 1972). This phenomenon
has been called "saccadic suppression." The decrease in visual perception takes
place not only during the saccade, but also before it begins.
Saccadic movement of the eyes in total darkness, when optical factors are
excluded, is accompanied by depression of electrical phosphene (Riggs et al.,
79
80 CHAPTER FOUR

1974). Structural differentiation of the visual field (the presence of boundaries

between areas of different intensity of illumination and of additional visual
objects) increases the "saccadic suppression." Under these circumstances, the
boundaries between drops of brightness do not necessarily coincide with the
direction of eye movement (Yakimov, 1973). Displacement of the background
in front of one eye leads to "saccadic suppression" of a stimulus presented to the
other eye. Immediately before a saccade, not only is visual perception reduced,
but also incorrect determination of the spatial location of a momentarily
presented stimulus occurs. The error may be of considerable magnitude - about
half the angular size of the saccade. Incorrect determination of the location of
an object of this sort may arise within the range of time from -150 msec to +60
msec relative to the beginning of the saccade (Mateev, 1973).
It has been concluded from these fmdings that "saccadic suppression" is
central in origin (Zuber and Stark, 1966; J. A. Michael and Stark, 1967;
Volkmann et ai., 1968), and that it is responsible for the "constancy" of visual
perception during voluntary eye movements (Beeler, 1967). The appearance of
"saccadic suppression" before the beginning of the saccade may indicate that this
phenomenon is connected with the "motor pretuning" that arises before any
voluntary movement (Gurfinkel' et ai., 1965; A. R. Shakhnovich et ai., 1971).
"Saccadic suppression" is manifested not only as a change in the sensitivity
of the eye to light, but also as a decrease in the amplitude of objectively
recorded reactions such as the pupillary reflex to light. In the period of most
marked "saccadic suppression," the response of the pupils to light amounts to
only 10% of its usual amplitude (Zuber et ai., 1966).
This author found, however, that the amplitude of constriction of the
pupil to a high-intensity flash during a saccade was unchanged, and only the
speed with which the pupil subsequently dilated was reduced (Fig. 51). This
"saccadic tonicity" of the pupil was discovered in this author's experiments, in
which a bright flash (duration 4 msec) was applied at different time intervals
after a change of fixation points. For this purpose, two neon lamps, the distance
between which was 20° of arc, were placed in the subject's visual field. By means
of a special switch, one lamp could be switched on and the other simultaneously
switched off. Simultaneously with the switching over of the neon lamps, the
time-delay unit of a universal stimulator (Disa) was activated, and this stimulator
in tum activated the flash lamp through a special relay. The saccadic eye
movement and pupillary response were recorded by means of a photoscanning
pupillograph (A. R. Shakhnovich and V. R. Shakhnovich, 1964). Whenever the
Hash coincided with the period of saccadic eye movement, no change was
observed in the amplitude of constriction of the pupil. At the same time, the
rate of dilatation of the pupil after the initial constriction was reduced by more
than half. This "saccadic tonicity" of the pupil is evidently attributable to a
change in tone of the parasympathetic innervation of the pupil during saccadic
eye movements.
SACCADIC EYE MOVEMENTS 81

•
O""'O~'I"'O"lf,.o" •• t'O'O"'f"tf"ttf'
15 mm

O"""tOtftf' •• ftfotf"'f".t."ftf.ftffft'

;"OOI~610"IOIO'OOODfOO'OO'
ooummOWft
.om' llooowm'~owwu
Ot,ooO~O"'fO'Oot

·0110111 OHwmmmum
'O"'~',ooo"'t'
Figure 51. Reaction of pupil to a flash during saccadic eye movement (bottom three
tracings). Reaction of pupil to the same flash at rest (top two tracings). Recorded with a
photoscanning pupillograph (10 strokes on the tracing = 1 sec; black dots mark the flash).

Mechanisms Controlling Saccadic Eye Movements

Saccadic eye movements are characterized by a rapid shift of the gaze
from one fIxation point to another. The velocity of a saccade of a given
amplitude cannot be varied at will, and it is independent of the initial position of
the eye and of the direction of movement. An increase in the velocity of a
saccade of the eye is observed only if its amplitude is increased. By comparing
data given by different workers for the maximum velocity of saccades, Leushina
(1966) found a defInite relationship between the maximum velocity and
amplitude of the saccade. The spatial relationships between the initial and fmal
fIxation points in this case were measured by the visual system even before the
eyes began to move (Leushina, 1974). The amplitude of the saccade is also
dependent on its mean velocity: with an increase in amplitude of the saccade, its
mean velocity rises (Ditchbum and Ginsborg, 1953). The clear correlation
between the amplitude and velocity of the saccade indicates that as the saccade
is about to begin, the muscular effort that is required to produce it and that is
able to make the eye move at a velocity corresponding to its amplitude is
"programmed."
Saccadic eye movements can be classed as ballistic movements, which are
characteristic of all goal-directed actions (e.g., walking, running, typewriting,
playing a piano), for these movements ensure the greatest degree of accuracy
(Wilkie, 1949; Hubburd, 1960; and others).
An important role in the elucidation of the mechanism of organization of
82 CHAPfER FOUR

saccadic eye movements is played by experiments with electrical stimulation of

the brain. Robinson and Fuchs (1969) used electrooculography to investigate
saccadic eye movements during stimulation of the frontal optomotor area in
monkeys. By means of this method, they showed that eye movements arising in
response to stimulation of that area have the same quantitative characteristics as
voluntary "saccadic" eye movements. In this case, the amplitude, duration, and
direction of the saccadic eye movements are independent of the intensity of
electrical stimulation if above threshold in strength. These workers concluded
from their fmdings that electrical stimulation sets in motion a definite cycle of
excitation in neuronal circuits located evidently in the brainstem. The circulation
of an impulse in the neuronal circuits continues irrespective of the stimulus
inducing it. This "explosive" character of activity in the corresponding neuronal
circuits is accompanied by the appearance of saccadic eye movements. By using
paired stimuli, these workers found periods of absolute and relative refractori-
ness, when the response to the second stimulus was absent or weak. No sign of
refractoriness could be found if the second stimulus acted on the opposite
hemisphere. On the basis of these findings, it was concluded that eye movements
in different directions are caused by the appearance of excitation in different
neuronal circuits.
The functional role of "programming" in the control of saccadic eye
movements is manifested particularly clearly in experiments with visual feed-
back. I carried out experiments of this type on a patient with the sequelae of a
head injury and unilateral ophthalmoplegia, but whose vision was preserved.
Two fixation stimuli (neon lamps) separated by a distance of 30° of angle, were
projected separately, first on the right eye, then on the left. Their projection
always coincided with the horizontal meridian of the retina. The fixation stimuli
were applied alternately. In addition, a spot of light moved along a perimetric
arc situated horizontally in the field of vision and measuring 30° of arc. When
this spot of light oscillated in the visual field of the left (mobile) eye, this eye
performed oscillatory movements of the same amplitude as the photic stimulus.
In response to similar stimulation of the fixed right eye, the left eye again
performed oscillatory movements, the amplitude of which was much greater
than the amplitude of the oscillations of the stimulus. This experiment gives
further confirmation of the dependence of tracking movements of the eyes on
the velocity of movement of the image over the retina. During stimulation of the
fixed eye, the image on the retina moved much faster than during stimulation of
the normal eye, causing the appearance of tracking eye movements of much
greater velocity and amplitude than normal.
In response to switching over of the fixation stimuli in the visual field of
the left (mobile) eye (Fig. 52), a saccade of the same eye appeared, corresponding
in amplitude to the character of the stimulus. A decrease in the distance between
the photic stimuli and the fixation point led to a corresponding decrease in
SACCADIC EYE MOVEMENTS 83

A B c

- I

\w-
:
..
'--
Figure 52. Electrooculogram of movements of the left eye in a patient with total paralysis
of the muscles of the right eye. Top row: Character of the movement of the photic stimulus
in the visual field. (A) Sinusoidal stimulation; (B,C) jerky stimulation of varied amplitude.
Middle row: Movement of the left, mobile eye during stimulation of the same eye. Bottom
row: Movement of the left eye in response to stimulation of the right, ilXed eye. The scale
in the top left-hand comer shows the angular displacement in degrees and the time in
seconds (recorded on the VEKS-ol cathode-ray oscilloscope).

amplitude of the saccade. Similar stimulation of the right (ftxed) eye led to the
appearance of saccades of the left eye, the amplitude of which was much greater
than the distance between the ftxation stimuli; not only the amplitude but also
the form of the saccades was changed.
During stimulation of the mobile eye, it suddenly ceased to move; this
could have been caused only by the operation of a special "braking system,"
preventing the action of forces of inertia at the end of the saccade. During
photic stimulation of the fIXed eye, the effect of this "braking system" on the
muscular apparatus of the eye was evidently not felt, and for that reason,
saccades with increased amplitude appeared in the mobile eye, followed by a
smooth transition to stopping of the eye in the new position. Furthermore, in
response to repetitive photic stimulation of the ftxed eye, the amplitude of the
saccade varied within much wider limits than during stimulation of the mobile
eye. The accuracy of a saccade thus depends on the functioning of the "braking
system" at the end of the saccade. The role of the "braking system" in the
sudden stopping of the eye at the end of the saccade is manifested particularly
clearly when the dynamics of the velocity and acceleration are analyzed during
saccades of the normal eye in response to stimulation of the same eye and also
of the opposite, fIXed eye. Saccadic movements begin identically in both cases,
but they end differently; in the ftrst case (A), a saccade has a sudden end, but in
the second case (B), it has an increased amplitude and a smooth, gradual end
(Fig. 53). The change in acceleration during the saccade gives an idea of the
changes of the force acting on the eye (because force is proportional to
84 CHAPTER FOUR

t·
0.1 sec

C o
(a)

OM
I~I~ "
900 ~
5,f000 : I H
750
(b)
900
55000
750
5l ~ 1;.5000 I 45000

il3~~~O i/'
--." 500 GOO
35000
450
3" " 25000 I , 25000
ClQ. 300 , 300
co:O 15000 I 15000
- - 150 I 150
5000 I 5000
0 0
-5000 -5000
200
t. msec t. msec
Figure 53. Electrooculograms of two types of saccadic eye movements (recorded on the
VEKS-Ol cathode-ray oscilloscope): (A) Saccadic movement of the eyes stopping suddenly;
(B) saccadic movement stopping gradually. The time marker on curves A and B is a 50-Hz
setting; the scale at the top left shows the angular displacements of the eyes in degrees and
the time in seconds. (C,D) Change in velocity w (solid line) and acceleration {3 (dashed line)
with time t during saccadic movements of the left eye with a change of fixation points in
the field of vision of the same eye (C) and in the field of vision of the right (fixed) eye (D).
(el) Maximum of the active force "triggering" the saccade; (C2) maximum of the passive
force "braking" the saccade (friction, viscosity of muscles); (C3) maximum of the active
force "braking" the saccade; (M) maximum velocity of the saccade.

acceleration). Both types of saccades attain their maximum velocity almost

simultaneously. The velocity decreases very rapidly during saccades that end
suddenly (Fig. 53A), but slowly in sacca des that end smoothly (Fig. 53B).
During saccades with a sudden end, the phase of retardation lasts twice as long as
the phase of acceleration. During a saccade that ends smoothly (Fig. 53), the
phase of retardation is much longer than the phase of acceleration.
During the phases of acceleration and retardation of the saccade, it is
possible to judge the relative magnitude of the forces acting on the eye. The
strongest force of muscular contraction acts on the eye at the beginning of the
saccade, during acceleration of the motion. The magnitude of this force is almost
identical in different types of saccades. The force that "brakes" the saccade,
however, is much less than the force that "triggers" it. A considerable difference
SACCADIC EYE MOVEMENTS 85

can be seen in the duration of the phase of retardation in the two different types
of saccades. The same passive force, the action of which is evidently due to
mechanical factors (e.g., viscosity of the muscles, friction), helps to brake
saccades of both types. An additional active force, however, is required to brake
the saccade that stops suddenly. This force begins to act on the eye immediately
before the end of the saccade, and it stops the eye in a certain position.
How can the absence of "braking" of the saccade during stimulation of the
fixed eye be explained? It may be recalled that the patient with ophthalmoplegia
was instructed to carry out an exact movement: to change two fixation points.
The "program" of this saccade provided for interaction between two forces -
one "triggering" and the other "braking" the saccade. To carry out this
"program" and to operate the "brake" of the saccade at the right time, however,
additional afferentation is necessary during the saccade; its absence <luring
stimulation of the fixed eye led to the appearance of a saccade with increased
amplitUde and with a smooth ending (Le., to the appearance of sacca des
"without brakes"). What afferentation is absent when the fixed eye is stimu-
lated? In the first place, there are no proprioceptive impulses from the muscles
of that eye. Proprioceptive impulses arrive from the muscles of the other
(normal) eye, however, and can provide afferent information for the system
controlling saccadic eye movements. It therefore seems more likely that visual
afferent impulses indicating a sudden change in position of the image of the
retina during the saccade are necessary to activate the "braking" system of the
saccade.
During stimulation of the fixed eye, these visual impulses indicating a
change in position of the image of the retina are absent, and this absence
evidently leads to the appearance of saccades "without brakes" in the other eye.
To determine the role of these impulses from the retina in the control of
saccadic eye movements, it was necessary to change the character of the afferent
impulses, which was done by the use of a cap fitted with a mirror at an angle of
45°, which gave a mirror image of surrounding objects on the retina. During
movements of the eye, the images of surrounding objects on the retina move in
the opposite direction at twice the velocity (Fig. 54). Under these conditions, a
very small displacement leads to the appearance of oscillatory eye movements of
large amplitude and to "swimming away" of the surrounding objects. After a
short time (1-1.5 min), however, the gaze can be "stopped" on the fixation
point, and the saccadic eye movements to a change in fixation points can then
be studied. To study these movements, the lamp fixed by the eye is switched off
and another lamp at the periphery of the visual field is switched on. This
switching over of the lamps leads to "programming" of saccades to the new
stimulus. During the performance of this saccade, the image of the new stimulus
does not approach the fovea centralis of the retina, but, on the contary, moves
away from it at twice the velocity (because of the optical laws of reflection).
86 CHAPTER FOUR

1 \ ,_ _ _ __

2-'

5~

6~

7~
1 sec
I I

Figure 54. Electrooculographic record of eye movement during a change of fixation points
when examined under ordinary conditions (1,2) and through a mirror IIxed to the eye
(3-7). Neon lamps, separated by a distance of 15° in the field of vision, serve as fixation
points. The lamps are switched on from left to right (1, 3-7) and from right to left (2). The
arrangement of the cap with the mirror and photic stimuli is shown on the left.

The saccadic eye movements during perception of the surrounding space through
the mirror and after switching the neon lamps are completely indistinguishable
from the ordinary type, being identical in amplitude and stopping suddenly
(Fig. 54, 1-7).
Mter the first saccade, which did not lead to displacement of the image of
the stimulus into the region of the fovea centralis, the "search" for this stimulus
by a series of subsequent saccades begins. This finding suggests that some "rigid
program" for the saccade exists and is formed during the latent period of this
movement. The performance of this "program" cannot be disturbed by any
marked change in character of the afferent impulses from the retina during the
saccade. The total absence of such impulses, however, as obtains when the fixed
SACCADIC EYE MOVEMENTS 87

eye is stimulated, prevents the second part of this "program" - activation of the
"braking" system of the saccade - from being carried out. To activate the
"braking" system of the saccade, what is important is evidently not the
qualitative aspect of impulses from the retina during this movement, but that
such impulses exist at all.
That the performance of motor programs is independent of sensory
feedback has also been demonstrated by electrophysiological experiments
(Vaughan et ai., 1970). The evoked response in the EEGs of monkeys disappears
during active voluntary movement, such as conditioned-reflex extension of the
hand. In the opinion of Vaughan and co-workers, these findings indicate that
kinesthetic feedback to the motor cortex is blocked during performance of the
voluntary movement, which can take place because of the central motor
program that is formed in the process of training. This program can be put into
effect without kinesthetic feedback. Inhibition of the transmission of somatic
(cutaneous) afferentation through the lemniscal system before the beginning and
during the performance of the conditioned-reflex movement has been found
during electrical stimulation of the superficial radial nerve in cats (Ghez and
Lenzi, 1970, 1971; Coulter and Thies, 1971). Since inhibition of transmission of
afferent volleys takes place before the beginning of movement, it is evidently
connected with descending influences on the relay points for transmission of
afferentation in the lemniscal system. Recent electrophysio10gical data can thus
help to explain the mechanisms of temporarily blocking of sensory correction
during the performance of "programs" of eye movements.
The functional role of "programming" in the control of saccadic eye
movements in man has also been demonstrated electroencephalographically
(Becker et ai., 1972). By averaging of the electroencephalographic data, four
different potentials preceding or accompanying voluntary saccadic movements
of the human eye were discovered: (1) a "readiness potential" - slow negative
changes of cortical potential spreading bilaterally with maximal amplitude over
the vertex and starting about 1 sec before the saccade; (2) a positive premotor
cortical potential starting about 150 msec before the beginning of the saccade;
(3) a positive spike at the beginning of the saccade, possibly muscular in origin;
(4) an evoked potential in the parietooccipital region, with a positive wave
arising 200 msec after the saccade (this potential does not disappear even if the
eye movement is made in darkness).
Functional changes in the nervous system preceding voluntary movement
have been found by the study not only of eye movements, but also of other
voluntary movements. Neurons with a firing pattern that changed about 100
msec before the beginning of a conditioned-reflex movement of the contralateral
hand have been found in the motor cortex of monkeys (Evarts, 1966). These
observations suggest a causative connection between the initiation and prompt-
ing of the movement and activity of the pyramidal neurons. The activity of most
88 CHAPTER FOUR

pyramidal neurons is connected chiefly with the development of muscular force,

and it also correlates with the amplitude of the conditioned-reflex movement
(Evarts, 1969; Humphrey et a/., 1970; Humphrey, 1972). Changes in unit
activity preceding conditioned-reflex movement are observed not only in the
motor cortex, but also in the ventrolateral nucleus of the thalamus; this finding
suggests that thalamic neurons play an important role in the control of motor
cortical activity before movement (Evarts, 1970). Changes in unit activity
preceding conditioned-reflex movement in monkeys have also been found in the
Purkinje cells of the cerebellum and in cells of the dentate and intermediate
nuclei (Thach, 1968, 197Uz,b, 1972). It can be postulated on the basis of these
findings that the cerebellum also participates in the organization of initiation and
prompting of a certain type of movement. In investigations on man, sufficiently
definite changes preceding voluntary movement have been found in the EEG
(Walter, 1964; Vaughan et a/., 1968; Deecke et a/., 1969), and also during
monosynaptic testing of the spinal segmental apparatus (Kots, 1975).
This "motor pre tuning" is manifested particularly clearly in response to
electrical stimulation of the motor cortex (A. R. Shakhnovich et a/., 1971). This
investigation was carried out on a patient who had undergone an operation for a
tumor of the wing of the sphenoid bone on the left side. An electrode inserted
into the brain substance in the region of the precentral gyrus, in the area of
representation of the forearm, was fixed to the edge of the burr-hole with acrylic
glue (Fig. 55). The electrode consisted of two platinum wires held closely
together. One wire was completely insulated, and the active surface consisted of
the area of cross section (d = 0.2 mm) at its tip. This platinum wire was used to
detect changes in the local blood flow and brain metabolism by a polarographic
method in order to assess the effectiveness of treatment after operation. The
other platinum wire, of the same diameter, was stripped of insulation for a
length of 1 cm. The active surface of the electrodes was located in the cortex.
The electrode that was bare for a considerable length was used for electrical
stimulation. The reference electrode was a lead plate covered by a wet cloth,
held in the patient's hand. Monopolar electrical stimulation was applied with the
Disa "Multistim" apparatus. The electromyogram was recorded with a Disa
electromyograph using a cup electrode fixed to the surface of the right forearm
in the region of the extensor muscles.
These experiments showed that with single stimuli of threshold strength

Figure 55. Motor pretuning during stimulation of the motor cortex. Lateral (left) and
anteroposterior roentgenograms of the patient's skull after insertion of electrode into the
left precentral gyrus. The graph shows changes in amplitUde of synchronized response
during preparation for and performance of voluntary movement plotted against the time
between stimulus for voluntary movement and electrical stimulation of the motor cortex.
The control amplitude (100%) is indicated by the dashed horizontal line.
"* 600
~. 500

=1.{]()
::l

a.
~ 300
c
";;; 200
C>
~ 700
~

U OL---~~~~---L----~--~----~--~
fOO 200 JOO 400 sao 500
Time. msec
90 CHAPTER FOUR

and 1-msec duration, the right hand made a movement consisting of supination
with simultaneous flexion at the elbow and extension of the wrist. A syn-
chronized response appeared on the EMG of the extensor carpi radialis muscle
18 msec after stimulation (Fig. 56). The synchronized character of this response,
its appearance after application of a single stimulus, and the stability of its latent
period can be attributed to the monosynaptic nature of the connection between
the pyramidal tract and spinal motoneurons in man (Kuypers, 1964). A weak
acoustic stimulus (a click), applied through earphones, was used as the stimulus
for voluntary movement. The patient was instructed to extend the right hand in
response to this signal. At various time intervals after acoustic stimulation, the
motor cortex was stimulated by single pulses 1 msec in duration. These
investigations alternated with control stimulation of the motor cortex unac-
companied by clicks (Fig. 56, C).
With an increase in the interval between the acoustic stimulus and
stimulation of the motor cortex, changes in the character of the synchronized
response were observed. With an interval of 20 msec, a statistically significant
increase (p<0.01) in the amplitude of this response compared with that of the
control was seen for the first time (Fig. 56). This time was much shorter than
that during determination of motor pretuning with the aid of the H-response
(Gurfmkel' et af., 1965). Such a short latent period of motor pretuning in the
present investigations was evidently due to the special features of the technique
used, by means of which changes in excitability of pyramidal neurons as well as
spinal motoneurons could be detected. The change in the character of the
response with an increase in the time interval between acoustic and electrical
stimuli is interesting. A "pure" synchronized response is observed with time
intervals of not more than 50 msec. With a further increase in this interval, a
synchronized response arises against the background of asynchronous waves,
evidently as the result of a change in excitability of the motoneuron pool during
motor pretuning.
In the present investigations, the time interval between the synchronized
response and the subsequent myogram of movement was never less than 170
msec. The existence of this interval can be explained by the presence of long
inhibition in the motor cortex after excitation of the pyramidal neurons. The
same factor evidently lies at the basis of the statistically significant (p<0.0 1)
increase in latent period of the simple motor response (about 20%) when
electrical stimulation of the motor cortex was carried out 18 msec after acoustic
stimulation.
In every case, when the synchronized response coincided with the begin-
ning of the voluntary movement, a long period of silence was observed. When
the stimulus was applied immediately after movement and 400 msec after the
click, the synchronized response appeared against the background of asyn-
chronous waves, just as in the case of motor pretuning.
SACCADIC EYE MOVEMENTS 91

50 msec
~

SR .:../---

100 msec 100 msec 100 msec

1---1 ~ 1--1

C ;.J 80
~ 250
t-+
10 "
I r' 100
~ 300
~
.~
20 .,; I_a:. 120
~ .oot-
30t-- 140
~ 500 ~,.. •

40~ 160
~ 600 "1·1

60~ 200~ 700 ~

Figure 56. Electromyograms of synchronized response (SR) during preparation for and
performance of voluntary movement. (C) Synchronized response to the control stimulation
(without the click). The numbers to the left of all other tracings denote the time interval (in
msec) between the click and electrical stimulation of the motor cortex.
92 CHAPTER FOUR

The experiments with electrical stimulation of the motor cortex thus

demonstrate the occurrence of "motor pretuning" preceding voluntary move-
ment. A similar "pre tuning" evidently arises in the optomotor cortex during
preparation for saccadic eye movements. One cannot rule out the possibility that
this motor "pre tuning" lies at the basis of the appearance of a "readiness
potential" on the EEG and also of the decrease in visual perception immediately
before saccadic eye movements.

Electrical Activity of the Ocular Muscles During Saccadic Eye Movements

The speed and stability of saccadic eye movements depend on the

organization of the motoneuron pool of the oculomotor system. Some infor-
mation on the properties of this organization is given by investigation of the
electrical activity of the eye muscles. Electromyographic investigations indicate
that a sudden burst of activity arises in the agonist muscle of the saccade (Bjork,
1955; J. Miller, 1958; Tamler et ai., 1959). The mean duration of the saccade is
60 msec, and it clearly depends on the amplitude of the saccade. According to J.
Miller (1958), with a saccade of 2.5 0 the duration of the burst of spikes in the
agonist muscles of the saccade is 30 msec, compared with 150 msec for a saccade
of 400 • The high-frequency burst in the agonist muscle of the saccade is
accompanied by inhibition of activity in the antagonist muscle (Bjork, 1955).
Reciprocal relationships between the agonist and antagonist muscles of the
saccade were also discovered in experiments on rabbits (A. R. Shakhnovich and
Nebieridze, 1967a,b). These investigations showed that if a muscle is an agonist
of a saccade, a high-frequency burst of activity, which weakens gradually, is
recorded in it. With a change in the direction of the saccade, the electrical
activity in that same muscle is inhibited. At the end of the saccadic movement,
however, an increase in electrical activity was recorded in the antagonist of the
saccade (Fig. 57); this increase is evidence of active inhibition of this movement,

0.1 sec
Figure 57. Increase in electrical activity in antagonist muscles at the end of a saccade. In
each pair, the top curve is the electromyogram, the bottom curve, the electrooculogram.
SACCADIC EYE MOVEMENTS 93

and indicates that it is ballistic in character. In the opinion of Alpern (1962),

however, a burst of electrical activity is characteristic in agonist muscles of a
ballistic movement only in the early stage of this movement. Nevertheless, in this
author's experiments, a high-frequency burst of spikes in the agonist muscles
continued throughout the saccade, and it was gradually inhibited at the
beginning of the next tracking phase. This gradual decrease in electrical activity
in the agonist muscles of the saccade was due to a decrease in the firing rate of
the single motor units and to their inactivation. In the repeated phases of
nystagmus, the order of inactivation of single motor units was constant. The
burst of electrical activity in the agonist muscles thus continued throughout the
phase of the saccade and ended gradually only in the subsequent phase of
tracking. These findings can hardly contradict the view that saccadic eye
movements are ballistic in nature. It is known, for example, that a ballistic
movement such as that of an experienced tennis player hitting the ball IS
accompanied by a sudden increase in electrical activity of the agonist muscles
throughout the phase of striking (Slater-Hammel, 1949).
With an increase in amplitude of the saccade, the combined electrical
activity of the agonist muscle increases, and the number of active motor units
and the duration of their firing both increase (Fig. 58). It can thus be predicted
from the intensity of the electrical activity of the eye muscles at the beginning
of a saccade what the amplitude of a movement will be. These findings are
further confirmation of the hypothesis of preliminary "programming" of
saccadic eye movements.
The marked difference in quantitative characteristics of the different eye
movements served as the basis for attempts to link them with different motor
systems (Matyushkin, 1961, 1963). The attempt by Breinin (1962) to discover a
slow motor system in the eye muscles was unsuccessful, however, and it was
accordingly postulated that the eye muscles are physiologically homogeneous.
Besides slow (tonic) and fast (phasic) muscles, the skeletal musculature
also contains fibers with an intermediate position. According to Granit (1957),
during muscular contraction, phasic motoneurons have the most important role;
in the uninjured organism, however, it is very difficult to demonstrate tonic
motor units, for they are few in number compared with the phasic fibers, and
their activity is low.
Matyushkin (1961, 1963) recorded the potentials of single fibers of an
ocular muscle intracellularly, and found that some of these fibers are perma-
nently active. Low (10-28 mY) and long (10-20 msec) potentials with
frequencies of 10-75/sec arise in them. In Matyushkin's opinion, these are
"tonic" fibers. Other fibers (phasic) were activated only during fast contractions
of the muscle, and they were characterized by high (60-90 mY) and short
(2-msec) action potentials. In Matyushkin's opinion, "phasic" fibers are active
during the fast phase of nystagmus, whereas "tonic" fibers are active during the
 94 CHAPI'ER FOUR

~ ~ • i ~I
l

! tI '. ,. \1 ,I ~ ... l'~ '~I~' t, ~ !' ~I!! ~ "!I:_~I~ ~ .t! .~1

100 .vl ~. ~ ~IIIII ~ I!~ it~ ~1"1.~th!t' )t"~f \~ ~.. 2

0.1 sec
"t~.'.I.I'.II~""""""H~II~~II~li~"""""~••'W~11~'1..... 4
~~--------------~----------~------ 5
100 JlV1 ,$lr'l'I''II[ 1!
~~~'------------------------------~'-~----------------
O.1sec
Figure 58. Electrical activity of the ocular muscles during optokinetic nystagmus. In each
pair, the top curve is the electromyogram, the bottom curve, the electrooculogram. (1,2)
Electrical activity of lateral rectus muscle when acting as agonist of a saccade. Activity of a
motor unit, unconnected with the phases of nystagmus, is shown on the curves. Another
motor unit with spikes of higher amplitude is activated during the saccades, and the
duration of its activity increases with an increase in amplitude of the saccade. (3) Increase in
combined electrical activity of an ocular muscle during an increase in amplitude of the
saccade. (4,5) Increase in duration of activity of single motor units and activation of fresh
units with an increase in amplitude of the saccade. The arrow indicates the saccade during
which the activity of one motor unit was recorded. This motor unit is activated in the
saccade, and continues to discharge during the subsequent tracking phase.

slow state. Matyushkin's hypothesis on the functional role of the two motor
systems of the ocular muscles was the basis for construction of a mathematical
model (Petrov and Sragovich, 1967).
OUf own investigations, however, do not support Matyushkin's views, and
they in tum served as the basis for further development of theoretical models
(A. R. Shakhnovich and Shapiro, 1973). It was shown electromyographically
that the same motor unit can be active at rest and also in the phase of tracking
and the saccade during optokinetic nystagmus in different directions (Fig. 59).
In the character of its action potentials, this motor unit corresponds to
Matyushkin's "phaSic" fibers. At rest, the interspike interval is approximately
cunstant; in the tracking phase, it decreases gradually; in the phase of the
saccade, it increases.
Matyushkin evidently did not find motor units of this type because in his
experiments, the natural functioning of the muscle was disturbed (the tendon
SACCADIC EYE MOVEMENTS 95

was detached from the eye and the muscle was stretched in a bath of mineral
oil).
Meanwhile, investigation of the electrical activity of the eye muscles under
normal physiological conditions showed that the same motoneurons can partici-
pate in the organization of different eye movements (following and saccadic),
and they are thus a "final common path" for various supranuclear influences (A.
R. Shakhnovich and Nebieridze, 1967a,b).
Robinson (1970), Fuchs and Luschei (1970), and Keller and Robinson
(1972) reached a similar conclusion after microelectrode investigations in which
the unit activity was recorded in the nuclei of the oculomotor and abducens
nerves in monkeys in a waking state. The same neurons, located in these nuclei,
showed specific changes in firing pattern during different types of eye move·
ments (fixation, following, saccadic, convergent). The burst of spike activity
preceded the beginning of the saccade, on the average, by 7 msec, and it ended
10 msec before the end of the saccade. During saccadic eye movements, the
mean firing rate was 400 spikes/sec, but in some cases, it was as much as 800
spikes/sec. During a change in the direction of a saccade to the opposite, the
activity of this particular neuron ceased or was greatly weakened.
According to Henn and Cohen (1972, 1973), motoneurons of the ocular
muscles of monkeys may be active during fixation (tonic motoneurons), and also
during saccades (phasic motoneurons). Some motoneurons also have character-
istic types of activity during both slow and fast eye movements (phasic-tonic
motoneurons). The firing rate of the motoneuron during fixation is determined
by the characteristics of the preceding saccade. Phasic and tonic components of
motoneuron activity thus cannot be controlled separately, but are determined

1~~[~tnt'1/·t ,t tl:t ttjr t4t!tt1~ t~ t-t:tt

l l 1

~~~t .::::1: t, 1et t1r[1~t5t ~1~~fttet12

tl

Figure 59. Activity of the same motor unit with the drum stationary (at rest) and during
rotation in different directions (in the phase of tracking and saccade). In each pair, the top
curve is the electromyogram, the bottom curve, the electrooculogram. (1) Drum stationary;
(2) muscle recorded is an agonist of tracking; (3) muscle recorded is an agonist of the
saccade.
96 CHAPTER FOUR

by a single process. Eckmiller (1974), in his investigation, also showed that the
discharge activity of motoneurons of the ocular muscles during fixation is
dependent on the preceding saccade. Neurons in the region of the nuclei of the
3rd, 4th, and 6th cranial nerves responded by an increased firing rate to saccades
in the on-direction and a decrease in the firing rate in the off-direction. With the
eyes in the same position, the discharge frequency of these neurons was
approximately 15 spikes/sec greater if the eyes came to that point as a result of
the saccade in the on-direction than if they did so as a result of the saccade in
the off-direction. This property was called static hysteresis.
Neurons giving a burst of spikes 7-8 msec before the saccade have also
been found in monkeys in the immediate proximity of the nuclei of the cranial
nerve - in the central gray matter of the aqueduct of Sylvius. The firing rate
during this burst is rather less (average 240 spikes/sec) than in the nuclei of the
cranial nerve. The most important feature of these neurons is that their bursts of
spike activity are independent of the direction of the saccades (Matsunami,
1972). More marked "anticipation" of the beginning of the saccade by bursts of
unit activity both in light and in darkness is found in the superior colliculi (by
30-300 msec). A differential relationship between the burst of spike activity
and the direction of the saccade is revealed (Wurtz and Goldberg, 1971, 1972).
The activity of reticular units located around and anteriorly to the nuclei
of the abducens nerves also correlates to some extent with saccadic eye
movements. The beginning, duration, and intensity of the complete burst of
spikes of many neurons depend on the direction, duration, and velocity of
saccadic eye movements, and they usually precede a burst of spikes in the
neurons of the abducens nucleus (Luschei and Fuchs, 1972). These neurons may
thus generate a burst of spikes before the beginning of a saccadic eye movement;
this "anticipation" differs at different levels of oculomotor innervation.
The "anticipation" of the beginning of saccadic eye movements by a burst of
unit activity may be assumed to be linked with the "programming" of these
movements.
Electromyographic and microelectrode investigations both indicate that the
appearance of eye movements of different types (following, saccadic, fixation,
convergent) depends on the nature of the supranuclear control mechanisms, rather
than on the existence of specialized sub populations of motoneurons in the nuclei
of the corresponding cranial nerves.
 CHAPTER V

Convergent Eye Movements

Visual perception of three-dimensional space is characterized by stereoscopy and

ability to assess the relative distance of objects examined. Convergent eye
movements, which ensure that the projection of images on the retina of both
eyes corresponds, are of great importance to stereoscopic vision.

Convergent Eye Movements and Stereoscopic Vision

Normal binocular vision is characterized by its stereoscopic character and

by fusion of the paired retinal images. Stereoscopic vision is manifested as a
sensation of solidity of the surrounding objects and also by the assessment of
their relative distance. Fusion prevents the appearance of double vision following
the projection of an image on the retinas of the two eyes.
The founders of the theory of binocular vision were Muller (1826) and
Hering (1942). According to this theory, identical (corresponding) photo-
receptors are found in the retina of each eye. These include photoreceptors in
the region of the fovea centralis of each eye as well as other photoreceptors on
either side of the fovea centralis and equidistant from it. When an image falls on
these identical (corresponding) photoreceptors, it is projected as a single image.
If it falls on non corresponding (disparate) points of the retina, however, fusion
does not take place, and the image is seen double. Should an object fixed by the
two eyes be seen double, convergent eye movements arise and continue until the
disparate character of the image on the retina is minimal.
If near objects are examined, coordinated contraction of three different
groups of ocular muscles takes place: convergence of the eyes due to simul-
taneous contraction of both medial rectus muscles, and simultaneous contrac-
tion of the synergists of these muscles - the superior and inferior rectus muscles.
97
98 CHAPTER FIVE

The antagonist muscles - the lateral rectus and both oblique muscles of the
eyes - are relaxed. As a result of convergence, both optical axes converge on the
object examined, the image of which falls on identical retinal points in the
region of the fovea centralls. At the same time, the muscles constricting the
pupils contract, thereby reducing diffraction and aberration and ensuring a
clearer image on the retina. The muscles of accommodation also increase the
curvature of the lenses and their refractive power, thus increasing the sharpness
of the image on the retina.
The opportunities presented by the use of psychophysiological methods of
investigation of stereoscopic vision (determination of the threshold of stereo-
scopic perception, determination of the nearest point of clear vision, and so on)
have now been greatly extended, thanks to the use of objective methods of
recording the eye movement.

Eye Movements and Reactions of the Pupils During Convergence

In understanding the mechanism of convergence of the eyes, considerable

information is given by analysis of the quantitative characteristics of this
movement as well as by its study in patients with disorders of refraction and
disturbances of binocular vision.
Pupillographic investigations of the process of convergence were carried
out by V. R. Shakhnovich (1957,1958), Samoilov et af. (1961), and Sokolova
(1971). In these investigations, distant and near objects of fixation were placed
in the midline relative to the subject's eyes. The persons whose convergence was
investigated were of different ages. In some cases, they were elderly subjects
with features of presbyopia, for whom accurate binocular fixation of near
objects was difficult without the use of glasses because of their defective
accommodation. These investigators therefore chose an average distance,
namely, 14 cm, that corresponded to an accommodative power of 7 D in persons
with emmetropia, and at which the circles of dispersion in persons with
presbyopia were not too large to interfere with binocular fusion. The accuracy
of fixation was determined by the small size of the objects for fixation, which
sub tended an arc of approximately 10.
Assuming the mean distance between the centers of the two eyes to be
60 mm, one can draw two equal right triangles, each having one leg equal to half
the distance between the centers (3 cm) and the other leg equal to the distance
to the object of fixation (14 cm). The tangent of the required angle in this case
is about 0.22, so that the angle will be 12.5 0 • The combined convergence of the
axes of the two eyes during fixation at 14 cm is therefore 25 0 • The degree of
convergence of the optica1 axes during fixation at a near point can easily be
measured on any pupillogram. The millimeters of displacement of each eye when
fixation has to shift from a far point to a distance of 14 cm can thus be easily
CONVERGENT EYE MOVEMENTS 99

determined. All calculations during the investigations of convergence are carried

out in degrees, not in millimeters. The calculation used by Helmholtz (with later
refinements by Gullstrand) for the distance from the center of rotation of the
eye to the apex of the cornea, which he took to be 13 mm, can be used for this
purpose. By subtracting from this figure the depth of the anterior chamber and
the thickness of the cornea, the distance from the center of rotation of the eye
to the level of the pupil is obtained; it is about 10 mm. Displacement of the eye
by 1 mm thus means its rotation through an angle with a tangent of 0.1, i.e., an
angle of 5.5°.
On the basis of such calculations, pupillograms obtained from 10 healthy
subjects of different ages were analyzed. The subjects were characterized by full
visual acuity in both eyes, good binocular vision, and emmetropic or near-
emmetropic refraction of both eyes (deviations of not more than ±1.0 D). The
ages of the subjects ranged from 17 to 48 years. Despite accurate centering, the
movements of the right and left eyes of the subjects during the process of
convergence were unequal. The difference in the angles of convergence of the
right and left eyes averaged 2°, reaching 4.5 or even 5° in some cases. At the
same time, in 50% of all subjects, the difference between the movement of
convergence of the right and the left eye was either zero or not more than 0.5°.
The mean amplitude of the convergence movements for all 20 eyes of the 10
persons examined was 12.5°, in exact agreement with the calculated value. If the
combined convergence of the optical axes of both eyes of each subject is
analyzed, the degree of convergence varies in individual cases from 20 to 29.5°,
so that the deviation from the calculated value is no more than 20% on either
side.
The time required for completion of convergence varies in individual cases
from 0.1 to 0.7 sec; only in one of 20 eyes was it as much as 1.0 sec. The right
eye of this same subject completed the same movement in 0.3 sec. The
difference in the time of convergence movements of the two eyes of the same
subject may therefore be considerable under normal conditions.
The duration of the period from the beginning of convergence of the
optical axes to the beginning of constriction of the pupils (the delay time of the
pupillary reaction) is constant but varies in different subjects from 0.2 to 0.6
sec. The duration of this period may also differ in the right and left eyes of the
same subject.
The amplitude of the pupillary contraction during convergence varies in
individual cases from 1 to 3 mm. The time from the beginning of constriction of
the pupils to their maximum constriction varies from 0.5 to 1.3 sec, almost
twice the duration of normal constriction of the pupil to light.
During a pupillographic investigation of convergence in a subject with a
relatively slight degree of hypermetropia of the right eye, but with compound
hypermetropic astigmatism of the left eye that could not be completely
100 CHAPTER FIVE

corrected with glasses, the right eye converged by 14°, but the left eye by only
3°. The total convergence of the optical axes was thus only 17°, much below
normal (from 20 to 29.5°). Constriction of the pupils was also minimal (by
1 mm in both eyes). Absence of normal binocular vision is thus accompanied by
disturbance of convergence of the eyes.

Interaction Among Innervation Mechanisms of the Various Eye Muscles

During Convergence

Convergent eye movements arise when fixation is transferred from a far to

a near object. The stimulus for these movements is the loss of sharpness of the
image of the near object on the retina (accommodation stimulus) and falling of
the image on unsymmetrical points of the retina (fusion stimulus). Under the
influence of these stimuli, a "program" of coordinated activity of the various
eye muscles is formed. This "program" includes some degree of convergence of
the eyes as well as contraction of the accommodative muscle and constriction of
the pupil.
After an analysis of the published data, I..eushina (1966) concluded that
there is a functional relationship between the angle of convergence and the
velocity of the eye movements: with an increase in the angle, the velocity of
convergence increases. These observations indicate that the relative distance of
far and near objects of fixation is assessed by the visual system before the eye
movements begin. In correspondence with this preliminary assessment, a "pro-
gram" of eye movements is formed, an important feature of which is a specific
fixed relationship between the amplitude and and velocity of convergence. This
"program" also provides for a specific degree of interaction between the
extrinsic muscles of the eyes and the accommodation muscles and the sphincters
of the pupils. This interaction possesses definite flexibility.
With the same degree of convergence, an object examined may appear
sharp if converging or diverging lenses are placed between it and the eye. In these
experiments, different degrees of accommodation correspond to the same degree
of convergence. Only by the use of very powerful lenses can the object examined
be made indistinct. The difference between the greatest and smallest possible
values of accommodation for the same degree of convergence is called the range
of relative accommodation. The existence of this quite wide zone within which
accommodation is independent of convergence is of great importance to the
understanding of the mechanism of coordination of the various eye muscles
concerned with stereoscopic vision.
Much more interesting, however, is the study of the zone within which a
change of accommodation inevitably leads to a change in convergence, and vice
versa. Convergence concerned with the power of accommodation is called
accommodative convergence. It was investigated as follows: Far and near objects
CONVERGENT EYE MOVEMENTS 101

of fixation, located on the same axis, were placed in front of one of the subject's
eyes. By means of a special shutter, the near object of fixation was hidden from
,the other eye. The near and far objects of fixation were of equal angular
dimension (7'), and they were presented alternately. The reactions of both
pupils and the movements of both eyes were recorded simultaneously. Under
these conditions, the only stimulus that led to the appearance of convergence
was an indistinct image of the near object of fixation on the retina of one eye.
Accommodation of the lens was accompanied, however, by convergence of the
optical axes and constriction of both pupils (Fig. 60, right). The eye from which
the far stimulus was hidden by the shutter apparently moved "idly"; i.e., the
movement did not lead to the appearance of an image of the near stimulus of the
retina of that eye, and consequently no fusion stimulus was present.

25

I'" ImI IJ ' , II II

Figure 60. Accommodative convergence (right) and asymmetrical convergence (left) for
different distances of the fixation stimulus from the eyes (40, 33, 25, and 20 cm,
respectively). In each pair, the top curve is for the right eye, with far and near objects of
fIxation placed before it, the bottom curve is for the left eye. Time calibration: 10 strokes
on the curve = I sec.
102 CHAYfER FIVE

As stated above, convergence of the optical axes under these conditions is

called accommodative convergence. If the screen separating the near stimulus
from one eye is removed, however, both the loss of sharpness of the image on the
retina and stimulation of asymmetrical points of the retina will act as stimuli for
the appearance of convergence. Under these conditions, ordinary, asymmetrical
convergence will be produced (Fig. 60, left). It was therefore necessary to
determine the role of a combination of different stimuli (fusion and accom-
modative) and their application separately in the organization of the complex
synergism of the various muscle groups characteristic of the process of conver-
gence. It was also extremely important to determine whether this complex
synergism can be regulated, i.e., adapted to stimuli of different intensity.
To study these factors, accommodative and asymmetrical convergence
were compared in the case of a near object at different distances from the eye.
Bringing an object closer to the eye leads to an increase in the degree of
convergence of the optical axes and in the amplitude of constriction of the pupil
in both accommodative and asymmetrical convergence. No significant difference
in the character of asymmetrical and accommodative convergence can be
discovered if the object is placed at the same distance from the eye. These
observations point to a stable system of interaction between the mechanisms of
innervation of the various muscle groups, which are able to develop the same
degree of contraction whether the accommodation stimulus is used alone or
combined with a fusion stimulus. This system of interaction is so strong that it
cannot be disturbed even by abolishing the effect of accommodative conver-
gence by paralysis of the muscle of accommodation.
To produce such paralysis in a healthy subject, homatropine was instilled
into the eye in front of which the distant and near objects for fixation were
placed. The near object was always at the same distance from the eye. The other
conditions of the tests were the same as in the previous experiment. The
pupillograms were recorded before instillation of homatropine and every 5 min
after (for 40 min). Meanwhile the nearest accommodation point was determined.
During development of paralysis of the muscle of accommodation, the degree of
convergence of the optical axes during accommodative convergence increases
(Fig. 61). Under these circumstances, the convergence movement of the eye
breaks up into two movements separated by a short interval.
These fmdings suggest that complex synergism of the ocular muscles
connected with the process of convergence operates in response to the action of
the accommodative stimulus alone. If such a movement does not restore
sharpness of the retinal image lost as a result of the paralysis of the muscle of
accommodation, further movement takes place under the influence of a
voluntary impulse. The only possible afferentation that ran correct this move-
ment consists of impulses from the retina indicating loss of sharpness of the
CONVERGENT EYE MOVEMENTS 103

1 JI

Omin
II 111111111 I I 1 r;m I III IJ 1.1111

3 rI'Prr,, "wn!J1l

ill ,,1 1t I I <If

Figure 61. Accommodative convergence (right) and asymmetrical convergence (left) during
development of paralysis of accommodation of one eye. In each pair, the top curve is for the
right eye, into which homatropine was instilled and in front of which distant and near
stimuli were placed, and the bottom curve is for the left eye. The figures in the center show
the time after instillition of homatropine and the distance to the nearest accommodation
point. Time calibration: 10 strokes on the curve = 1 sec.

image. These results point to a definite role for the "programming" of

accommodative convergence. Even though accommodation is absent and the
image on the retina remains blurred, convergent eye movements still arise.
Despite the essential role of loss of sharpness of the retinal image (the
accommodative stimulus), stimulation of asymmetrical points on the retina is of
decisive importance. The phenomena of disparity of the retinal image in the two
eyes arising under these circumstances are the principal stimulus that determines
the direction and velocity of convergence (Rashbass and Westheirner, 1961a,b).
According to Westheimer and Mitchell (1969), normal convergence and diver-
gence arise even when a separate pair of stimuli, one of which differs sharply
from the other, acts on disparate points of the retinas of the right and left eyes.
These stimuli may be totally unlike in shape and in contrast, or they may differ
104 CHAPTER FIVE

in the site of the image on the retinas of the two eyes in the vertical plane (by as
much as several degrees of angle). The two stimuli may be presented consecu-
tively, at an interval of up to 100 msec.
The role of disparity of the retinal images in the production of conver-
gence was studied in the author's investigations, in which the fusion stimulus was
applied separately from the accommodative stimulus. The subject was instructed
to fix on a distant object, and various diverging prisms wert placed in front of
one eye. An increase in the deflecting power of the prism leads to stronger
convergence of the optical axes and to an increase in the amplitude of the
pupillary reaction (Fig. 62). The distant object of fixation becomes gradually

Figure 62. Fusion convergence when prisms with different refracting power are used. In
each pair, the top curve is for the right eye and the bottom curve is for the left eye, in front
of which the prism is fixed. Time calibration: 10 strokes on the curve = 1 sec.
CONVERGENT EYE MOVEMENTS lOS

less sharp, indicating simultaneous contraction of the muscle of accommodation.

The coordinated activity of the various ocular muscles thus arises in response to
separate application of accommodative and fusion stimuli. Regardless of which
stimulus is used, the degree of constriction of the pupils depends on the degree
of convergence of the optical axes (Fig. 63). These findings confirm the presence
of complex synergism of the various ocular muscles concerned with stereoscopic
vision. Regardless of the character of the visual stimulus, the degree of
interaction among the mechanisms of innervation of these muscles remains
relatively constant.
The combination of reflexes of the ocular muscles concerned with
stereoscopic vision is one of the most demonstrative examples of synergism
among different muscle groups. Many neurologists have examined the mech-
anism of this synergism (Darkshevich, 1922; Gordon, 1936; Behr, 1925). No
final decision has yet been reached on the location of the integrative mechanisms
of convergence, however, and indeed their very existence is still in dispute.
A problem of immediate importance is that of the mechanism of
coordinated function of the different muscles during the process of convergence.
Analysis of the clinical material indicates that this coordinated activity of the
different eye muscles does not always take place during convergence. The
author's pupillographic investigations on the patients with disturbances of
refraction (moderately severe myopia and hypermetropia) showed no abnor-
mality of convergence of the eyes. These findings may indicate that convergence is
to some degree independent of accommodation, evidently as a result of the
flexibility and wide range of possible functional adjustment possessed by the
corresponding brain structures. The range of this functional adjustment is not
however, unlimited: in a patient with a severe disturbance of refraction

E 4-
E
~3
::J

....a.
o 2
c:

,
o
.~
.;:
~
c:
o
U O~L-~~-L~~L-~~-L~__L-~~-L~__L-L-~-L~
1 2 3 4- 5 8 7 8 9 10 11 12 13 14 IS 10 17 18 19 20
Convergence of optical axes, deg

Figure 63. Reactions of pupils as a function of degree of convergence of optical axes in

different types of convergence: (I) asymmetrical; (II) accommodative; (III) fusion conver-
gence.
106 CHAPTER FIVE

(compound hypermetropic astigmatism), stereoscopic vision and convergence of

the eyes were absent.
Convergence and accommodation, it must be emphasized, can take place
independently within very narrow limits (the zone of relative accommodation
and convergence). Outside these limits, convergence is inevitably accompanied
by accommodation, and vice versa. The existence of this "inflexible" connection
between accommodation and convergence is confirmed by the author's experi-
ments, in which a pupillographic analysis was made of accommodative conver-
gence. These experiments showed that stimulation of one eye by an accom-
modative stimulus induces normal convergence, the same as is found in response
to binocular stimulation with an accommodative and fusion stimulus. Fairly
strong contraction of the muscle of accommodation thus invariably leads to
convergence of the eyes and constriction of the pupils.
How is this "inflexible" connection between accommodation and conver-
gence effected? One suggestion is that during contraction of the muscle of
accommodation, a flow of afferent impulses arises and causes excitation of the
innervation mechanism of convergence. This suggestion is not supported,
however, by the results of experiments in which paralysis of accommodation of
one eye was produced by instillation of homatropine. In response to the action
of the accommodative stimulus on this eye, increased convergence of the eye
developed. This experiment rules out any possible role of afferent stimuli from
the muscle of accommodation and the appearance of accommodative conver-
gence, and it shows that there is a connection between the central mechanisms
of accommodation and convergence. The placing of prisms of different refractive
power in front of one eye produced fusion convergence by preventing the action
of an accommodative stimulus. The fusion convergence of the eyes arising in this
case was accommpanied by accommodation and by constriction of the pupils.
Accommodation and convergence are thus closely interconnected. Convergence
can be evoked by both an accommodative and a fusion stimulus, and in every
case it is accompanied by constriction of the pupil. The amplitude of this
constriction is determined entirely by the degree of convergence of the eyes, and
is independent of the character of the stimulus.
It can be concluded from the analysis of these pupillographic records of
convergence that constriction of the pupil always begins with a certain delay
after the beginning of convergence of the optical axes. This delay may be
attributable to the secondary character of the pupillary response relative to
convergence of the eyes. It can be postulated that simultaneous contraction of
the medial rectus muscles of the two eyes leads to the appearance of a flow of
afferent impulses that excite the pupillary innervation mechanisms. Constriction
of the pupils also arises during contraction of only one medial rectus muscle (in
asymmetrical convergence). When contraction of the medial rectus muscle of
one eye is accompanied by contraction of the lateral rectus muscle of the other
CONVERGENT EYE MOVEMENTS 107

eye, however, the rotation of the eyes to the side that results is not normally
accompanied by constriction of the pupils. These observations make it unlikely
that constriction of the pupils during convergence is caused by afferent impulses
from the medial rectus muscles of the eyes. Excitation of the innervation
mechanisms of convergence can be assumed to spread to the innervation
mechanisms of the pupil, as a result of which constriction of the pupil arises
with a short delay after the beginning of convergence of the optical axes. Jampel
(1959) found by electrical stimulation of various points of the cortex in
monkeys that isolated convergence, accommodation, and constriction of the
pupil can be evoked. That this convergence can arise in isolation, without
constriction of the pupil, makes it improbable that the reaction of the pupil is
secondary in character and associated with the spread of excitation from the
innervation mechanisms of convergence.
Row does the coordinated activity of the innervation mechanisms of
convergence, accommodation, and pupillary constriction take place? In addition
to the isolated appearance of accommodation, convergence, and the reactions of
the pupils in response to stimulation of certain points of the cortex, all these
three effects were also shown to arise simultaneously in some cases. There is thus
a system at the cortical level for integrating the activity of the innervation
mechanisms of convergence, accommodation, and the pupil. This system is
activated voluntarily, and the duration of its action is controlled by fusion and
accommodative stimuli (stimulation of asymmetrical points and loss of sharpness
of the retinal image).
The experiments of Rubel (1959, 1960) and Rubel and Wiesel (1962)
showed that sensory integration during binocular stimulation is characteristic of
the highest levels of the visual system. These experiments established the
presence of neurons in the lateral geniculate bodies that respond to stimulation
of only one eye. Neurons responding to binocular stimulation (Le., to photic
stimulation of both the right and the left eye) appear for the first time in the
occipital cortex.
Of particular interest are the data of Barlow et al. (1967), who found in
the cat cortex specialized neurons, each of which responds only to a particular
degree of disparity of the retinal images (i.e., stimulation of asymmetrical points
of the retina). For instance, the fusion stimulus arising during stimulation of
asymmetrical points of the retinas of the right and left eyes is directly connected
with the visual cortex. Presumably, this fusion stimulus leads to excitation of
visual cortical neurons responding to binocular stimulation and to excitation of
the "integrative" mechanisms of the ocular muscles concerned with stereoscopic
vision. The activity of these muscles abolishes the phenomena of disparity on the
retina and causes the action of the fusion stimulus to cease. There are no
adequate grounds, however, for the suggestion that visual cortical neurons
responding to binocular photic stimulation are connected in a simple manner
108 CHAPTER FIVE

with the motor integrative mechanisms of the ocular muscles concerned with
stereoscopic vision.
One cannot rule out the possibility that the mesencephalon also partici-
pates in the organization of this connection. The investigations of Keller (I973)
showed that the changes in unit activity of motoneurons of the ocular muscles
are identical in character in monkeys during convergent and version movements
of the eyes. The change in motoneuronal activity is thus determined by the angle
of fixation, and is independent of the type of movement used to achieve this
angle. The separate volleys controlling version and vergence probably combine at
the same supranuclear level. Penfield (I938) and Penfield and Roberts (I965)
showed by stimulating the visual cortex (area 17) in man during neurosurgical
operations that visual perception is localized in the opposite half of the field of
vision in strict correspondence with the retinal projection. At the same time,
during electrical stimulation of the peristriate cortex (area 19), visual percep-
tions ("flashes of light," "colored rings" and other shapes) appear in both halves
of the field of vision. Penfield concluded from these findings that efferent fibers
run from area 17 into the mesencephalon, where they converge on neurons that
give off afferent fibers to areas 18 and 19 of both hemispheres. The functional
role of the mesencephalon in the control of convergence is well known: the act
of convergence is disturbed in lesions of the midbrain.
The question of the functional role of different levels of the visual system
and of the oculomotor innervation in the organization of synergism among the
ocular muscles concerned with stereoscopic vision is extremely complex and
requires further study.
 CHAPTER VI

Eye Movements and Higher

Cortical Functions

The interdependence of eye movements and higher cortical functions was clearly
demonstrated by Balint (1909), who studied a patient with a bilateral lesion of
the parietooccipital brain systems. This patient had no object agnosia, yet he was
able to perceive only one object at a time in the field of vision. The patient also
had a curious form of wandering of the gaze. He could not switch his fixation
smoothly from one object to another. The syndrome was called "psychic
disturbance of fixation." In Balint's opinion, the disturbance of the higher visual
function depends largely on the disturbance of eye movements. By means of
modern neurophysiological methods, it is possible to make a more detailed
analysis of the functional role of the cerebral cortex in the control of eye
movements.

Eye Movements and Cortical Unit Activity

To study the role of the cerebral cortex in the control of eye movements,
it is essential as a first step to analyze the behavior of single neurons. Correlation
of different character between unit activity and eye movements is found in
different parts of the cortex. In the visual association area in cats (the anterior
zone of the middle suprasylvian gyrus, or area 7, which is connected with the
thalamopulvinar complex and not with the lateral geniculate body), there were
found neurons the activity of which increased before or simultaneously with the
onset of a saccade. Neurons the activity of which increased 40-80 msec after
the beginning of saccadic eye movements were also found in the same region.
These findings indicate that area 7 is concerned with the coordination of the
109
110 CHAPTER SIX

visual and oculomotor systems (Straschill and Schick, 1974). Delay of firing of
the neurons relative to the beginning of the eye movements was also found in
monkeys in the posterior area of the middle frontal gyrus - area 8. This same
area is connected with the visual receptive field. There is reason to suppose that
area 8 is more remote from the final common pathway than the other motor
areas, and that it can be regarded as an intermediate opticomotor zone (Moller et
al., 1973).
Bizzi (1967) studied the unit activity of the frontal opticomotor area of
the monkey cortex during optokinetic and vestibular nystagmus, and found
neurons the activity of which increased during the fast or the slow phase of
nystagmus. These neurons accounted for 10% of the total number of neurons
recorded. The increase in unit activity during the slow phase of nystagmus took
place during movement of the eye through a certain position of fixation
irrespective of the direction of movement. The increase in discharge activity of
different neurons corresponded to different positions of fixation. Bizzi also
found other neurons the activity of which increased only during the fast phase
of nystagmus: a high-frequency burst of spikes appeared only when the eyes
moved in one direction.
This precise selectivity of unit activity with respect to the direction of eye
movements is not found in the posterior opticomotor area in the visual cortex.
The author recorded the unit activity in this area in experiments on the rabbit
(A. R. Shakhnovich and Shtil'man, 1969). The animal was in a waking state. A
drum with black and white stripes on its inner surface was used for optokinetic
stimulation. The drum moved in different directions, and its speed could be
varied. The animal was fixed inside the drum. To record the unit activity, a
micromanipulator was securely fixed to the animal's skull at the edges of a
burr-hole above the visual cortex. The design of the micromanipulator was such
that the rnicroelectrode could be insertea by means of a hydraulic drive under
remote control. The unit activity was recorded extracellularly by glass micro-
electrodes. Eye movements were recorded by an electrooculographic method. In
addition to optokinetic stimulation, on-and-off responses of the cortical neurons
to photic stimulation were also studied.
During analysis of the records, the unit activity could be compared with the
rhythm of optokinetic nystagmus. The results showed that most of the neurons
(180 of the 220 neurons recorded) had no connection with the rhythm of
optokinetic nystagmus. The other neurons (40) were clearly dependent on the
rhythm of nystagmus, as shown by an increase in strength or decrease in
frequency of the unit activity at a certain moment of the nystagmus cycle. The
period of change of unit activity corresponded to different moments of the
phase of tracking (beginning, middle, end) and also to the phase of the saccade.
Changes in unit activity were manifested as bursts of spikes, or a faster or slower
firing rate or complete cessation of activity. The duration of the individual
bursts could vary in successive cycles of nystagmus.
EYE MOVEMENTS AND HIGHER CORTICAL FUNCTIONS 111

In neurons the firing rate of which increased at certain periods of the

tracking phase, unit activity outside these periods was characterized by low
frequency, and it consisted of irregular single spikes or groups of spikes. The
neurons of this type did not give on-and-off responses to photic stimulation.
Altogether, 28 neurons of this type were found. The period of increased firing
rate corresponded to a specific moment of the tracking phase, and for a given
neuron, this period remained relatively constant in consecutive phases of
nystagmus. In different neurons, this period could correspond to the middle,
beginning, or end of the phase of tracking (Figs. 64-66). Unit activity beginning
at the end of the tracking phase continued in some cases during the subsequent
saccade (Fig. 66).
The time from the beginning of the tracking phase to the moment of
increase of unit activity was relatively constant for a given neuron. The
variability of this time was independent of the variability of duration of the slow
phases of nystagmus.
In the period of increased unit activity, the frequency and number of
spikes in the course of this period were inconstant in consecutive phases of
nystagmus. Single spikes, long high-frequency bursts of spikes, and total absence
of spikes could be observed in the same period of consecutive phases of tracking
(Fig. 66). Despite the variability of duration of individual bursts of spikes,
however, the duration of these bursts for a given neuron was relatively constant.
These bursts consisted of either single or paired spikes (Fig. 64), as well as longer
periods of spike generation (Fig. 65).
The duration of the period of more rapid unit activity reached half the
total phase of tracking. With a change in the direction of nystagmus, the
relationship between the activity of a given unit and the tracking movements of
the eyes remained the same as before. With such a change, the duration of the
burst of spikes and the firing rate changed a little during this burst. The changes
in unit activity, however, were very slight.
A burst of spikes from some neurons appeared during the saccade
(Fig. 67). Usually, such a burst of unit activity began 30-50 msec after the

200
p.V
1 ~
0.1 sec

'.11 .~! ~tI • t •. ;rU'. l t ~ t r 'Rb~rl"l

Figure 64. Unit activity in the rabbit visual cortex during optokinetic nystagmus. The top
curve shows the unit activity; the bottom curve is the electrooculogram. Single and paired
spikes arise at the beginning of the tracking phase.
112 CHAPTER SIX

I
1200/.LV .....- 0.2 sec

) fI~flp4 ~"bi ~",. '~A~fF+~~·'~'''··~ 4H~

Figure 65. Unit activity in the rabbit visual cortex during optokinetic nystagmus. The top
curve is the electrooculogram; the bottom curve shows the unit activity. A burst of spikes
appears at the beginning of the tracking phase.

beginning of the saccade and lasted for 100-400 msec, covering the beginning of
the tracking phase. When it began during the saccade, the maximum increase in
unit activity usually corresponded with the beginning of the tracking phase.
Neurons the discharge activity of which increased during the saccade did
not give off or on responses to photic stimulation. Altogether, 6 neurons of this
type were found.
Neurons that ceased to discharge during the saccade (6 neurons) formed a
special group. These neurons were characterized by a high firing rate during the
slow phase of nystagmus and also at rest, in the absence of nystagmus. The
period of cessation of unit activity lasted 150-300 msec, and as a rule, it
covered the beginning of the next tracking phase (Fig. 68). Cessation of spike
discharge during the saccade was observed in the same neuron during nystagmus
in different directions. The principal feature distinguishing neurons that ceased
to discharge during the saccade was the appearance of on-and-off responses to
photic stimulation, and these responses also took the form of cessation of unit
activity. The latent period of the response of these neurons to light varied within
wide limits (from 25 to 150 msec). Neurons that ceased to discharge during a
saccade were thus characterized by high spontaneous activity and by the
presence of a response to photic stimulation, which distinguishes them from all
other neurons connected with the rhythm of nystagmus.
In accordance with the classification of lung (1964), the cessation of firing
as on-and-off responses to photic stimulation is characteristic of a small group of
visual cortical neurons (3-5% of the total number). Our own observations

Figure 66. Unit activity in the rabbit visual cortex during optokinetic nystagmus. The top
curve shows the unit activity; the bottom curve is the electrooculogram. A burst of spikes of
varied duration arises at the end of the tracking phase.
EYE MOVEMENTS AND mGHER CORTICAL FUNCTIONS 113

Figure 67. Unit activity in the rabbit motor cortex during optokinetic nystagmus. The top
curve is the electrooculogram; the bottom curve shows the unit activity. A burst of spikes
begins in the phase of the saccade.

indicate that these neurons cease to discharge during the fast phase of
optokinetic nystagmus.
One cannot rule out the possibility that neurons that cease to discharge
during a saccade are connected with the mechanisms of "saccadic suppression,"
which is manifested as a lowering of the photosensitivity of the eye during a
saccade and for the 40-60 msec before it begins (Zuber and Stark, 1966;
Volkmann et al., 1968). "Saccadic suppression" is evidently one of the mech-
anisms of stabilization of the environment during eye movement (Beeler, 1967).
Neurons the activity of which ceases during saccadic eye movements thus
evidently have an important role to play in the constancy of visual perception.
The correlation thus discovered between eye movement and visual cortical
unit activity in rabbits is in harmony with the results of an investigation of
neurons in the cat visual cortex (Noda et al., 1972). Delay of a burst of unit
activity in the cat visual cortex relative to the beginning of saccadic eye
movement usually measured 20-100 msec, but in a few cases, it exceeded 100
msec. A burst of unit activity during saccadic eye movements may arise not only
in light, but also in darkness. Inhibition of discharge during and after a saccade is
observed in some neurons. The appearance of a burst of unit activity during a

Figure 68. Unit activity in the rabbit visual cortex during optokinetic nystagmus in two
directions: (A) to the left and (B) to the right. The top curve in each pair shows the unit
activity; the bottom curve is the electrooculogram. The unit activity is inhibited in
optokinetic nystagmus in both directions during saccadic eye movements.
114 CHAPTER SIX

saccade in darkness is evidence against any dependence of this burst on visual

afferentation. A more likely hypothesis is that neurons the activity of which
depends on eye movements form part of a reverberating circuit in which
impulses circulate during optokinetic nystagmus. The order of excitation of the
neurons composing this circuit differs at different levels of ocular motor
innervation. In the mesencephalon, a burst of unit activity precedes a saccade
(by 7-8 msec in the nucleus of the oculomotor nerve and in the central gray
matter of the aqueduct of Sylvius, and by 150 msec in the superior colliculus).
Meanwhile, in the visual cortex the burst of unit activity is delayed after the
beginning of the saccade. The duration of this delay usually exceeds 20 msec,
and in some cases, it may exceed 100 msec.
The comparison of all the data on the character and order of excitation of
neurons at different levels of the oculomotor innervation may help to shed some
light on the mechanisms of its structural and functional organization.

Eye Movements and Local Cerebral Blood Flow

To study the functional role of different parts of the brain in the

regulation of eye movements, other indicators than changes in unit activity can
be used, e.g., the dynamics oflocal cerebral blood flow. The blood supply to the
brain is known to change during an increase or weakening of its functional
activity in accordance with the metabolic concept of regulation of the cerebral
blood flow (Roy and Sherrington, 1890). The problem of correlation of blood
supply with functional activity of the brain has attracted the attention of many
investigators. Fulton (1928) described a patient with an arteriovenous aneurysm
in the occipital lobe of the brain. When this patient read, he heard a sudden
noise in his head, evidence of an increased blood flow. Sokoloff et al. (1955),
using Kety's method, found no changes in the total cerebral blood flow in
various types of intellectual activity.
Risberg and Ingvar (1968) determined the blood volume in the brain by
the use of Risa's non diffusing radioactive indicator, injected intravenously.
During a test requiring the memorizing of picture cards, the blood volume in the
occipital region increased by 10%, whereas in the parietal and frontal regions, a
decrease in blood volume was found. In tests in which the subject had to pick
out a common detail in a series of geometrical figures, the blood volume
increased in the frontal, postcentral, and oCcipital regions. During reading of
"colored" words, when a situation of conflict was produced by a difference in
the color of the letters and the meaning of the word, the blood volume increased
in the OCcipital region by about 10%. In another test, a series of simple numbers
from 4 to 9 was read to the subject, who was instructed to repeat them in the
opposite order. In this test, the increase in blood volume in the frontal region
amounted to 4.8%. At the same time, the blood volume in the region of the
EYE MOVEMENTS AND HIGHER CORTICAL FUNCTIONS 115

central gyri decreased by 5.3%. Measurement of the regional cerebral blood flow
by intraarterial injection of 133Xe was carried out during performance of the
same test of repeating numbers (Ingvar and Risberg, 1967). The results showed a
mean increase in the cerebral blood flow in the suprasylvian region by 2.2
ml/lOO g per min, or 5%. In the cortical gray matter, the cerebral blood flow
increased by 5.7 mi/IOO g per min, and in the white matter, by 1.8 ml/lOO g per
min. In the temporal region, when the same test was used, the cerebral blood
flow decreased. In tests involving abstract thinking, the blood flow increased in
the parietal, temporal, occipital, and frontal regions. In some cases, the increase
in blood flow in the parietooccipital region reached 40% (Risberg and Ingvar,
1971 ).
A detailed investigation of the free oxygen level in patients with different
functional loads imposed by means of electrodes implanted into deep brain
structures was carried out in N. P. Bekhtereva's laboratory. A definite relation-
ship was found between the changes in the free oxygen level and the emotional
state of the patients, their various motor responses, and so on (Bekhtereva,
1971; Grechin, 1966).
By means of thermoelectrodes, R. Cooper et al. (l965) found an increase
in local cerebral blood flow in the occipital lobe during visual perception of
various objects. With the thermoelectrode technique that Cooper used, however,
no quantitative data on the cerebral blood flow can be obtained; all that can be
concluded is whether it has increased or decreased.
The object of our own investigations was to obtain quantitative data on
changes in local cerebral blood flow during eye movements and the performance
of certain other functions: reading, calculation, and speech (A. R. Shakhnovich
et al .. 1970, 1972, 1974; A. R. Shakhnovich and Razumovskii, 1974). The local
cerebral blood flow was investigated in 26 patients undergoing operative
treatment for aneurysms of the cerebral vessels (7), arteriosinus anastomoses
(l2), and brain tumors (7). To monitor the cerebral blood flow for a sufficiently
long time and to assess the effectiveness of treatment in the postoperative
period, insulated platinum electrodes with an active surface of 0.2 mm 2 at the
tip, implanted into the brain substance, were used on these patients both during
the operation and in the postoperative period. Usually, two electrodes, one
8 mm shorter than the other, were inserted together. The reference electrode was
an iron plate, 20 cm2 in area, secured over a damp cloth to the patient's arm.
The polarogram was recorded by means of the PE-312 polarograph. The local
cerebral blood flow was recorded by the hydrogen clearance method. A positive
voltage of 0.3 V, which is unanimously agreed by many workers (Aukland,
1965,1967; Aukland et al., 1964; Fieschi et al., 1965; Lubbers, 1968; Lubbers
et al., 1969) to increase the sensitivity of the electrode selectively for hydrogen,
was applied to the platinum recording electrode. The patient took one breath of
hydrogen, causing a sharp rise of the polarographic curve, followed by a period
116 CHAPTER SIX

of decline, corresponding to elimination of hydrogen from the brain tissue. The

local cerebral blood flow (CBF) was determined by the equation

69.3
CBF = - ml/IOO g per min
TI/2

where TI/2 is the half-elimination time of hydrogen. Investigation of local

cerebral blood flow was carried out at rest and during optokinetic nystagmus,
the direction of which was described relative to its fast component. The results
thus obtained were compared with those of investigation of the cerebral blood
flow in certain types of intellectual activity (reading, speech, mental arithmetic).
A complete investigation using all the function tests listed above was carried out
only on those patients in whom the electrode could be left in the brain tissue
long enough. Investigations of the cerebral blood flow at rest and during the
various function tests was carried out alternately.
These investigations revealed some special features distinguishing the
spatial organization of the mosaic of the resting cerebral blood flow (Fig. 69). If
the electrodes were close together (200.um between centers), synchronized
fluctuations of the cerebral blood flow were seen in two neighboring points of
the brain. The period of these fluctuations was about 1.5-2.0 hr, and their
amplitude reached 20 ml/IOO g tissue per min. If the distance between the
electrodes was increased to 8 mm, however, asynchronous fluctuations of the
cerebral blood flow with about the same frequency were observed. The mosaic
of the cerebral blood flow was thus characterized by the presence of small areas
within which synchronized fluctuations of the cerebral blood flow occur. At the
same time, in neighboring areas a short distance apart, these fluctuations may be
completely asynchronous. The synchronous character of the fluctuation in small
areas of the brain enables functional units of the cerebral circulation to be
distinguished. These functional units may vary in size. During functional loads,
the spatial organization of the cerebrovascular mosaic is altered, and the
character of the changes remains relatively constant on different days. An
example of these regular changes in the cerebral blood flow is given by the
results of an investigation on a patient in whom the electrode was inserted in the
posterior areas of the left parietal lobe. Although the blood flow at rest varied
considerably on different days of the investigation, an increase of the blood flow
by an average of 88% was always observed while this patient was reading (Fig. 70
and Table 1). Another example of regular changes in the cerebral blood flow
during a function test (speech) on different days is given by the results of test on
a patient with electrodes inserted into the left parietal lobe (Figs. 71-73). To
standardize the conditions of psychological testing (automatized speech), the
patient was instructed to repeat all the months of the year in about 10 sec (fast
speech - Fig. 71) and 30 sec (slow speech - Fig. 71). Under these conditions,
EYE MOVEMENTS AND IDGHER CORTICAL FUNCfIONS 117

60

A
50
c:
'E
- 40
'Cl
0 II
0
!::. 30
E
I.L.
IX! 20
....J

10

o 10 20 30 40 50 60 70 80 90 100 110
Time, min
50

c: 40
'E
'Cl
-
o 30
o
....
~
E 20
I.L. II
IX!
....J to

o 10 20304050 60 708090100120140160180200220240
Time,min

Figure 69. Fluctuation of blood flow at rest in neighboring points of the brain. (A)
Synchronized fluctuations of blood flow in the lower parts of the right parietal lobe in a
patient undergoing operation for aneurysm of the supraclinoid portion of the right carotid
artery. Distance between centers of electrodes: 200 I'm. (B) Asynchronous fluctuations of
blood flow in posterior zones of the right superior temporal gyrus in patients undergoing
operation for a tumor of the right parieto-temporal region. Distance between centers of
electrodes: 8 mm-

no significant difference was found between the degree of increase of blood flow
on different days (Figs. 72 and 73). likewise, no significant difference was
found between the changes in the blood flow during fast and slow speech
(Figs. 71 and 72). The range of changes in the resting cerebral blood flow was
118 CHAPTER SIX

8 "
EYE MOVEMENTS AND HIGHER CORTICAL FUNCTIONS 119

TABLE 1
Local Cerebral Blood Flow in Posterior
Areas of the Left Parietal Region

Velocity of cerebral blood flow

(ml/lOO g per min)

At resta ReadingO

42* 105*
62*
53* 66*
29t 53. It
31.3t 58t
33.lt
46.5:1: 83.7:1:
43.5t 115:1:

M= 42.5 M= 80.1
a=±107 a=±25.7
m = ±3.8 m = ±10.7
tL _ _ _ _ p < 0.05 _ _ _ _-11
a Symbols denote consecutive tests: (*) 1st day; (t)
2no oay; t.J:J Jrd oay.

""'"-
1 min
Figure 70. Local cerebral blood flow in posterior areas of the left parietal lobe in a patient
undergoing operation for arteriovenous aneurysm of the left parietooccipital region of the
brain. (A,B) Roentgenograms of the skull; (C) Hydrogen clearance at rest (top) and during
reading (bottom). The arrows indicate: (1) the beginning of inhalation of hydrogen and
(2,3) the beginning and end of reading aloud.
 ...
N
o

c
] ELECTRODE A
Cl

8...
........ ~
E ~001 p>~
LL
IX! ~P>0.5~
...J
10 20 30 40 50 60 70 80 90 100 110120 130 140150 160 170
Time, min
A
ELECTRODE B

P > 0.001
~
I ~P > 06
O.!~ 1_IUltll,
~ . ~peecfi,

10 20 30 40 50 60 70 80 90 100 110 120 130140150 160 170

J~,~I~~~;~~~I~~~I~I~.
~
Time, min

g
~
~

~
 B c
Figure 71. (A) Dynamics of local blood flow (LBF) in the same day in the left parietal lobe of a patient undergoing operation for a left-sided
carotid-cavernous anastomosis, at rest and during functional loading (speech). (B,C) Roentgenograms showing the location of the electrodes.
 N
N
-
ELECTRODE A
c
'E
........
C) ~
o
o
... .0.001
~P < 0.001
........
• est
E peech P > O. 7~~~g
u.
In
-.J

II ,v v
c
"' ELECTRODE 8

P < 0.001 P 0.001

~<
~P>01~
~ .t=
-.J 14 7 6 10 5 5 8 5 5 12 5 5 12 5 5
!~mlm ~II mil ~;I ~Im
Figure 72. Mean values of local blood flow (LBF) in the left parietal lobe at rest and during functional loading (speech) on different days (I-V)
in the same patient as in Fig. 71. Q

~
In
S<
EYE MOVEMENTS AND HIGHER CORTICAL FUNCfIONS 123

120
r- - r- -
*-.80
u.
-- r- l"-
r-- r-
CO
<J
40

o I II III IV V
11 8 8 6 9

Lp > O.,-.J L p > 0.3J L p > O.,-.J L p > 0.2 J

I p> 0.5
" p> 0.6 I
I P>0.7 I Lp>o.,-.J
'-------p>0.3 _ _ _-.J1 L p>0.6J
Figure 73. Increase in cerebral blood flow (in %) during speech compared with the resting
state in the same patient as in Fig. 71. No significant differences can be seen among the
increases in mean value of the blood flow on different days.

much smaller than during function tests. At rest, the absolute values of the
cerebral blood flow changed within narrow limits (from 65 to 20 ml/IOO g tissue
per min), depending on whether the electrodes were in the gray or white matter
of the brain. During function tests, however, the contrast in the cerebrovascular
mosaic became more pronounced, and the fluctuations increased considerably
(from 13 to 220 ml/lOO g tissue per min). The increase in the velocity of the
cerebral blood flow evidently depends on increased neuronal activity in the
particular part of the brain concerned. On the other hand, the reduction in local
cerebral blood flow can be explained both by a decrease in unit activity and by
the character of redistribution of the blood: "robbing" one area to increase the
blood flow in a neighbOring area of the brain.
To determine whether the mechanism of the decreased blood flow during
functional loads is neuronal or circulatory, the unit activity must be recorded.
Comparison of the character of changes in the cerebral blood flow
recorded by two electrodes in neighboring areas of the brain, situated 8 mm
apart, is particularly interesting. This comparison revealed widely different
relationships among the changes in local cerebral blood flow. The absence of any
change in blood flow in one area during a particular function test could be
combined with an increase or a decrease in blood flow in the neighboring area of
the brain. In some cases, a marked difference in the degree of change of the
cerebral blood flow was observed in neighboring areas of the brain during the
same function test. The maximum difference in the degree of change in local
124 CHAPTER SIX

cerebral blood flow was observed in neighboring areas in the left parieto-
temporooccipital region during reading aloud; in the area of electrode A, the
cerebral blood flow was increased by 70%, but in the area of electrode B, it was
increased by 236% (Fig.74 and Table 2). On the assumption that in this
particular case the degree of change in the cerebral blood flow increased
gradually between the two electrodes A and B situated 8 mm apart, it is possible
to speak of a certain gradient of change in the cerebral blood flow. This gradient
can be expressed as a percentage (21 % in 1 mm) or in absolute values of changes
in the cerebral blood flow (14.4. ml/l00 g per min in 1 mm).
In neighboring areas of the brain, changes in the cerebral blood flow
during the same function test were different not only in degree, but also in direc-
tion. For example, in the right parietal lobe during the performance of mental
arithmetic, the blood flow in the area of electrode A increased by 69%, whereas
in the neighboring area of electrode B, it decreased by 47% (Fig. 75 and Table 3).
These reciprocal relationships between neighboring areas of the brain are
manifested particularly clearly during a change in the direction of optokinetic
nystagmus: in the middle areas of the right precentral gyrus during optokinetic
nystagmus to the left in the area of electrode A, the blood flow was increased,
but in the neighboring area of electrode B, it was reduced; during optokinetic
nystagmus to the right, the changes in local blood flow in the area of each
electrode were opposite in character (Fig. 76 and Table 4). However, such
reciprocal relationships between neighboring areas of the brain during a change
in the direction of optokinetic nystagmus are not always manifested (Fig. 77 and
Table 5).
The fmdings described above are evidence of a distinctive cerebrovascular
mosaic, the character of which depends intimately on the functional state of the
brain. This functional mosaic consists of individual areas of increased and
reduced cerebral blood flow.
The equal degree of change in the cerebral blood flow discovered in some
cases in neighboring areas of the brain during the same function test gives some
idea of the size of the areas of increase or decrease in the cerebral blood flow.
For example, in the left parietotemporooccipital region during optokinetic
nystagmus to the right (see Fig. 74 and Table 2), an equal degree of increase in
the cerebral blood flow was observed (p> 0.5). Assuming that the increase in
blood flow reached the same degree throughout the area of the brain between
electrodes A and B, it is valid to conclude that the size of the area of increased
cerebral blood flow was not less than 8 mm, i.e., not less than the distance
between the tips of electrodes A and B.
Indirect data on the size of the functional zone of increased cerebral blood
flow reveal a unique phenomenon - elevation of the polarographic curve after
the end of the function test and subsequent slow elimination of hydrogen, the
same as at rest (in the area of electrode B during reading aloud; Fig. 74 and
EYE MOVEMENTS AND HIGHER CORTICAL FUNCTIONS 125

Table 2). This phenomenon can evidently be explained by diffusion of hydrogen

from the surrounding areas of the brain. This diffusion of hydrogen can
evidently take place only if the area of increased blood flow is small, and this
was evidently the reason this phenomenon was rarely seen in our investigations.
Functional loads affect not only the absolute values of the blood flow, but
also the character of their fluctuation. Changes of this kind in the degree of
fluctuation when the brain is in different functional states indicate that they
depend on fluctuations in the level of neuronal activity. Differences in the
degree of fluctuation in different areas of the brain under these circumstances
may depend on the existence of "inflexible" and "flexible" components in the
system providing for psychological activity (Bekhtereva, 1971). Regular changes
in blood flow differ in character in the same brain areas under the influence of
different functional loads, which is evidence of their functional heterogeneity.
Moreover, regular changes in blood flow may take place in the same brain areas
under the influence both of elementary functional loads (flashes, optokinetic
nystagmus, motor tests) and of more complex psychological tests (speech,
reading, arithmetic, and so on; see, for example, Fig. 78 and Table 6). When the
electrodes were located in the right parietal lobe, regular changes in blood flow
occurred during both optokinetic nystagmus and speech. These changes, how-
ever, differed in character (Fig. 79). In some brain areas, on the other hand, no
change in blood flow occurred in response to either simple function tests
(optokinetic nystagmus) or more complex texts (reading) (Fig. 80 and Table 7).
Functional heterogeneity of individual brain areas does not rule out the
possibility that the degree of change in the neurocirculatory mosaic depends to
some extent on the difficulty of the functional load (Fig. 81). During an
elementary function test (optokinetic nystagmus), significant changes in blood
flow were "absent in nearly half the brain areas in which the electrodes were
placed. During the performance of arithmetical operations, the number of these
"silent" areas was smaller, and during speech, they were absent altogether.
These fmdings suggest that the same neurophysiological mechanisms may
be concerned with the formation of behavioral responses of widely different
levels of difficulty. With increasing difficulty of a function test, the organization
of these mechanisms evidently becomes more complex, and the level of their
integration is raised; this could be the cause of the diffuse changes in the cerebral
blood flow with increasing difficulty of function tests. Regular changes in blood
flow during the performance of the same psychological tests have been observed
in widely different areas of the dominant left hemisphere and also of the
nondominant right hemisphere, as well as in the cerebellum. Ingvar and Schwartz
(1974) observed more limited changes in the cerebral blood flow during
psychological tests corresponding to the representation of the particular func-
tion. For example, during speech, an increase in blood flow occurred in the
premo tor area and in the rolandic and suprasylvian regions of the dominant
A

B
EYE MOVEMENTS AND HIGHER CORTICAL FUNCTIONS 127

hemispheres. More diffuse changes in blood flow in our own investigations

evidently depend on differences in the methods used. Ingvar's radioisotope
method revealed more global changes of blood flow in those parts of the brain
that play the most important role in the organization of the particular function.
The more sensitive electrode method that we use reveals the wide representation
of the given function in different parts of the dominant and nondominant
hemispheres. This extensive representation of function throughout the brain
evidently lies at the basis of the tremendous powers of compensation in the
nervous system. Presumably, the diffuse change in blood flow during functional
loads, which occurs far outside the limits of the areas in which pathological
lesions disturb the particular function, is due to activation of the diffuse
nonspecific brain systems. However, the precisely differentiated responses to

C
t2

~
~.,
~
.' ''f
k
' ,

f H t--;
1 min
Figure 74. Local cerebral blood flow in the left parietotemporooccipital region in a patient
undergoing operation for an arteriovenous aneurysm of the mediobasal portion of the left
occipital lobe. (A,B) Roentgenograms of the skull. (C) Hydrogen clearances. The top four
hydrogen clearances correspond to blood flow in the area of electrode A at rest, during
reading, and during optokinetic nystagmus to the left and right. The bottom four hydrogen
clearances correspond to blood flow during the same function tests in the area of electrode
B. The arrows indicate: (1) the beginning of inhalation of hydrogen; (2,3) the beginning and
end of reading aloud; (4,5) the beginning and end of optokinetic nystagmus to the left; and
(6,7) the beginning and end of optokinetic nystagmus to the right.
 TABLE 2
Local Cerebral Blood Flow in the Left Parietotemporooccipital Region

Velocity of cerebral blood flow (ml/100 g per min)

Optokinetic nystagmus

Reading aloud To the left I To the right At rest

Aa Ba A B A B A B

87 173 116 173 154 231 87 76

49.5 231 139 116 139 116 58 53.3
116 231 139 231 154 139 69.3 77
126 231 139 173 116 139 53.1 81.7
83.5 231 139 154 139 81.7 99
86.7 231 63.1 99
86.7 231 63.1 63
139 231 63.1 57.6
86.7 231 49.5 69.3
92.3 49.5 46.2
43.5 57.6
49.5 49.5
49.5 62.8
43.5 53.4
43.5 69.3
43.5 49.5
49.5 38.7
43.5 69.3
43.5 69.3
69.3
63.1
69.3

M: 93.4 219.4 134.4 169.4 140.7 152.8 54.9 65.2

a: ±24.4 ±22.1 ±10.3 ±41.6 ±17.98 ±44.9 ±10.92 ±13.57
m: ± 7.35 ± 6.98 ± 4.6 ±18.6 ± 8.99 ±20.05 ± 3.45 ± 4.09

p < 0.01
p < 0.001
p < 0.001
p < 0.01
L- p < 0.UU1 ----l
L-- p < 0.01---1
L-p < 0.01----1
L - p < 0.05 ---J
p < 0.02
p < 0.01 I
L-p < 0.001----1 Lp > 0.1-..J Lp > 0.5J
L - p > 0.6 ----.J
L - p > 0.6-----.J
a A and B are different electrodes.
EYE MOVEMENTS AND HIGHER CORTICAL FUNCfIONS 129

variation in the character of the functional load when the level of activation is
the same make this hypothesis improbable. For example, in the inferior areas of
the parietal lobe of the non dominant right hemisphere, a reduction in the blood
flow was observed during subtraction from 300 by 2's, but during subtraction
by other numbers (1, 3, 5, 4, and so on), the blood flow was increased by
different degrees (Fig. 82 and Table 8).
Differential changes in blood flow during the performance of arithmetical
operations were observed not only in the cerebral hemispheres, but also in the
cerebellum. The results of an investigation of the blood flow in the left
cerebellar hemisphere during arithmetical operations (subtracting from 300 by
2's, 3's, and 4's) are shown in Fig. 83. In every case, a significant increase in
blood flow was observed, and this increase differed depending on the character
of the arithmetical operation (the blood flow increased more in the case of
subtracting from 300 by 2's than in the case of subtracting by 3's and 4's). In
all these observations, a change in the character of the arithmetical operation
was not accompanied by any marked change in the degree ofits difficulty. The
differential character of the changes in blood flow in these cases therefore could
not depend on a change in the level of activation of the diffuse nonspecific brain
system. The wide representation of the neuronal systems in different regions of
the brain does not rule out the possibility of differences in the quantitative and
qualitative composition of neurons in particular brain areas in which lesions give
rise to a disturbance of the particular function concerned. The investigations
show that various and widely separated brain formations participate in the
mechanisms of different behavioral responses. The functional role of these
formations varies. The organization of neuronal groups from originally poly-
functional components into dynamic, multicomponent systems lies at the basis
of the high flexibility and reliability of the work of the brain. With differences in
the functional state of the brain, the pattern of the neuroCirculatory mosaic is
altered in different brain areas; an area of increased blood flow under the
influence of one load may correspond to an area of reduced blood flow in a
different functional state of the brain.
These changes in local cerebral blood flow depend on the functioning of
different neuronal groups, and they are in full agreement with views regarding
the dynamic organization of functional systems of the brain (Filimonov, 1940;
Luriya, 1962). According to this theory, the loss of any component of a
complex functional system will cause that function to be disturbed. The
functional system as a whole will either disintegrate under these circumstances
or its organization will be modified, according to the "topological" and not to
the "metrical" principle, so that the necessary function can be taken over by a
new series of structures. That disturbance of a functional system can arise in
lesions of any of its components does not mean that the function is disturbed
equally by lesions of all parts of the brain. There are no grounds for considering
130 CHAPTER SIX

B
EYE MOVEMENTS AND HIGHER CORTICAL FUNCTIONS 131

-
1 min

Figure 75. Local cerebral blood flow in the medial zones of the right parietal region in a
patient undergoing operation for a meningioma of the fissure of Sylvius. (A,B) Roent-
genograms of the skull. (C) Hydrogen clearances. The top five curves correspond to blood
flow in the area of electrode A; the bottom five curves, to blood flow in the area of
electrode B. The arrows indicate: (1) the beginning of inhalation of hydrogen; (2,3) the
beginning and end of reading aloud; (4,5) the beginning and end of mental arithmetic; (6,7)
the beginning and end of optokinetic nystagmus to the left; and (8,9) the beginning and end
of optokinetic nystagmus to the right.
132 CHAPIERSIX

TABLE 3
Local Cerebral Blood Flow in the Right Parietal Region

Velocity of cerebral blood flow (ml/lOO g per min)

Optokinetic nystagmus

Reading Mental To the To the

aloud arithmetica left right At rest

Ab Bb A B A B A B A B

34.4 22.4 63.1 11.6 30.1 20.4 33.1 31.3 33.1 26.3
30.1 22.4 69.3 12 30.1 21 34.3 33.1 36.3 24.4
31.3 21.7 69.3 16.5 31.3 21.7 30.1 31.3 41 22.4
33.1 22.4 58 13.9 30.1 22.4 34.4 38.3 43.5 27.4
30.1 21 46.5 11.8 31.3 23.1 33.1 30.5 38.3 23.1
31.3 21.7 58 12 31.3 20.4 36.5 38.3 36.5 26.3
29 22.4 53.1 13.6 30.1 21.7 34.4 33.1 33.1 27.4
33.1 21 53.1 16.9 30.1 22.4 28.1 34.4 43.5 26.3
27.4 22 69.3 15.8 26.3 21
26.3 53.1 16.1 30.1 24
63.1 30.1 24.4
26.3 23.1
34.4
41

M: 30.6 21.7 59.6 13 30.5 21.6 32.9 33.7 35.2 24.6

a: ±2.7 0.6 7.8 5.7 0.6 0.97 2.6 3.1 5.7 2
m: ±0.87 0.2 2.3 1.8 0.2 0.34 0.92 1.01 1.5 0.57

P < 0.02
p < 0.001
p < 0.001 I
'--- p > 0.1 ---'
p < 0.01
p < 0.001
p < 0.01 I
L - p < 0.001-----1
a Subtraction from 300 by 17's.
b A and B are different electrodes.

that the antilocalizationists are correct and that the brain works as a single
"equipotential" entity. Higher cortical functions can thus be disturbed by
lesions of widely different parts of the brain. These higher cortical functions are
disturbed differently, however, by lesions affecting different parts of the
functional system. Consequently, higher cortical functions are based on the
EYE MOVEMENTS AND HIGHER CORTICAL FUNCTIONS 133

combined activity of many areas of the cerebral cortex, each of which makes its
own special contribution to the functional system as a whole.
A. R. Luriya illustrates these general principles of the theory of the
dynamic localization of functional systems of the brain by using disturbances of
writing as an example. The process of writing can take place normally only if the
complex interaction among cortical areas over almost the entire brain, but
forming a highly differentiated system, is intact. At the same time, each
component of this system has its own highly specific function to perform. This
complex interaction among cortical areas participating in the act of writing can
be changed at different stages of formation of the skill. The writing process can
be disturbed by local lesions of the cortex in widely different parts of the brain,
but in each individual case, the disturbance of writing will have special qualities
that depend on the site of the lesion. If the auditory cortex is damaged, the
organized perception of a flow of sounds will be impossible. A patient with such
a lesion will not possess a precise "program" of the word he must write,
although the principal motor skills and graphemes are preserved. In lesions of the
parietooccipital areas of the cortex directly associated with visuospatial analysis,
the perception of the acoustic composition of words remains intact, but the
process of "recoding" them into visuospatial schemes (graphemes) is disturbed,
and the topological scheme of the letters and spatial arrangements of their
elements are modified. In local lesions of the motor cortex, the kinetic
organization of the act of writing is disturbed: the patient has difficulty in
switching from one motor element to another, the smoothness of the necessary
movement is disturbed, and so on.
A complex functional system can thus be disturbed by cortical lesions
affecting widely different parts of the brain, but each disturbance is specific in
character. Functional systems are affected and reorganized specifically in each
local lesion. The study of the structure of disturbance allows the primary defect
that led to the appearance of the symptoms observed to be isolated. It must be
remembered that a lesion of a separate, localized area of the brain causes the
appearance, not of a symptom, but of a disturbance of a whole group of
functional systems in the organization of which this particular area of the brain
participates.
The multiple functional role of individual areas of the brain brought to
light by local brain lesions can thus also be demonstrated by recording the local
cerebral blood flow. A change in the functional activity of specific neuronal
populations leads to corresponding changes in their energy metabolism. It is
therefore not surprising that the local cerebral blood flow provides a quantitative
measure of the degree to which a particular part of the brain participates in a
particular behavioral response.
Investigation of the local cerebral blood flow in optokinetic nystagmus
demonstrates the wide representation of the system controlling eye movements
A

Figure 76. Local cerebral blood flow in the middle zones of the right precentral gyrus in a
patient undergoing operation for carotid-cavernous anastomosis. (A,B) Roentgenograms of
the skull. (C) Hydrogen clearance. The top six curves correspond to blood flow in the area
of electrode A at rest, during speech, reading aloud and to himself, and optokinetic
nystagmus to the left and right. The next two hydrogen clearances correspond to rest and
the performance of mental arithmetic after operation. The remaining curves correspond to
 I---f
1 min

blood flow during the same function tests in the area of electrode B. The arrows indicate:
(1) the beginning of inhalation of hydrogen; (2,3) the beginning and end of speech; (4,5) the
beginning and end of reading aloud; (6,7) the beginning and end of reading to himself; (8,9)
the beginning and end of optokinetic nystagmus to the left; (10,11) the beginning and end
of optokinetic nystagmus to the right; and (12,13) the beginning and end of mental
arithmetic.
 TABLE 4
Local Cerebral Blood Flow in Middle Areas of the Right Precentral Gyrus

Velocity of cerebral blood flow (ml/l00 g per min)

Optokinetic nystagmus
Mental Mental Reading
arith- arith- to Reading To the To the
At rest meticil At rest b meticb himself aloud Speech left right
---
AC BC B A A A B A B A B A B A B

43.5 34.4 27.4 58 63.1 53.1 34.4 63.1 63.1 73 53.1 69.3 22.4 34.4 43.5
49.5 30.1 33.1 58 58 53.1 30.1 63.1 53.1 69.3 63.1 72 22.4 30.1 43.5
53.1 34.4 30.1 53.1 58 53.1 34.4 58 53.1 69.3 53.1 69.3 23.1 34.4 41
53.1 27.4 31.3 58 63.1 53.1 38.3 63.1 53.1 69.3 53.1 77 24.4 34.4 43.5
53.1 29 33.1 58 58 53.1 33.1 69.3 46.5 69.3 69.3 77 23.5 33.1 43.5
46.5 33.1 34.4 53.1 58 53.1 38.3 69.3 53.1 63.1 63.1 72 24.4 30.1 38.3
46.5 34.4 29 58 58 49.5 30.1 69.3 58 69.3 63.1 69.3 26.3 33.1 41
46.5 34.4 34.4 58 63.1 49.5 34.4 63.2 53.1 63.1 63.1 72 24.4 33.1 41
53.1 33.1 53.1 23.1
46.5 30.1
53.1 33.1
53.1 33.1
53.1 34.4
36.3
M: 50 32.6 31.6 56.7 59.9 52.3 37.6 64.7 54.1 68.2 60.1 72.2 23.7 32.8 41.9
a: ±3.6 ±2.5 ±2.6 ±2.2 ±2.7 ±1.6 ±4.6 ±4.1 ±4.6 ±3.4 ±6.1 ±3.1 ±1.2 ±1.8 ±1.9
m: ±1.0 ±0.67 ±0.92 ±0.78 ±0.96 ±0.53 ±1.6 ±1.46 ±1.6 ±1.2 ±2.1 ±1.1 ±0.4 ±0.64 ±0.67

Lp > 0.2-'
L -_ _ _ _ _ _ _ p
> 0.2 _ _ _ _ _ _ _-1
L -_ _ _ _ _ _ _ _ _ _ p < 0 . 0 0 1 - - - - - - - - - - - '

____________________~p_<~O.=OOI--------------------~
____~--~~--------------~p~<~O~.O~OI~~~------------------~
p < 0.001--------------------1
L p >0.3 J
I P
> 0.5 _ _ _ _ _ _ _....J
'-----------p < 0.00l-------------.J
L -_ _ _ _ _ _ _ _ _ _ _ _ p < 0 . 0 0 1 - - - - - - - - - - - - - - 1
L -_ _ _ _ _ _ _ _ _ _ _ _ _ _ P < 0 . 0 0 1 - - - - - - - - - - - - - - - - - - . !

L -_ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ P < 0 . 0 0 1 - - - - - - - - - - - - - - - - - - - - - J

L p >0.3-'
L - p > 0.2-----.J

a Subtracting from 300 by 17's.

b Tests carried out after operation.
C A and B are different electrodes.
A

B
EYE MOVEMENTS AND HIGHER CORTICAL FUNCfIONS 139

in the brain: changes in the cerebral blood flow were observed when the
electrodes were situated in the frontal, temporal, parietal, and occipital regions
of the brain. In some areas of the brain, an equal degree of increase in the
cerebral blood flow was found during nystagmus in both directions (the left
parietotemporooccipital region; see Fig. 74 and Table 2). This phenomenon is
evidently due to the existence of neurons in the visual cortex that change their
firing pattern equally during optokinetic nystagmus to the right and to the left
(A. R. Shakhnovich and Shtll'man, 1969). Changes in the cerebral blood flow in
optokinetic nystagmus to the right and to the left were much more often found
to be different in character, however. In the right premotor and right occipital
regions, the increase in the cerebral blood flow during optokinetic nystagmus to
the right was greater than during optokinetic nystagmus to the left. In the right

Figure 77. Local cerebral blood flow in the right occipital lobe of a patient undergoing
operation for an arteriosinus anastomosis. (A,B) Roentgenograms of the skull. (C) Hydrogen
clearances. The top six clearances correspond to blood flow in the area of electrode A. The
bottom four hydrogen clearances correspond to blood flow in the area of electrode B. The
arrows indicate: (1) the beginning of inhalation of hydrogen; (2,3) the beginning and end of
reading aloud; (4,5) the beginning and end of optokinetic nystagmus to the left; (6,7) the
beginning and end of optokinetic nystagmus to the right; (8,9) the beginning and end of
reading to himself; and (10,11) the beginning and end of speech.
140 CHAPTER SIX

TABLE 5
Local Cerebral Blood Flow in the Right Occipital Lobe

Velocity of cerebral blood flow (ml/l00 g per min)

Optokinetic nystagmus
Reading
Reading to To the To the
At rest aloud himself Speech right left

Aa Ba A B A A A B A B

41 34.4 63.1 139 21.7 49.5 27.4 41.4 24 63.1

25.3 31.3 99 70 46.5 36 27.4 63.1 18.3 76
27.4 31.3 90 139 53.1 63.1 24 49.5 48.9 116
33.1 33.1 33.1 103 65 58 38.3 43.5 24 38.3
24 31 69.3 254 46.5 77.6 24 63.1 23.1 84
31.3 85 93
18.9 76 49.5
31.3 41

M: 29.1 32.3 69.6 139.2 46.5 60.9 28.2 52.1 21.7 75.9
a: ±6.7 1.41 23.1 69.4 15.18 19.03 6.9 10.6 2.85 28.4
m: ±2.37 0.63 8.11 14.5 7.08 7.21 2.65 4.75 1.26 12.7

L-p < 0.01---.J

L - p < 0.001----1
I P < 0.02
p < 0.05
p < 0.01
p > 0.6
p < 0.05
p < 0.01
a A and B are different electrodes.

parietal region, the increase in the cerebral blood flow during optokinetic
nystagmus to the right was accompanied by a decrease in the blood flow during
optokinetic nystagmus to the left in the region of electrode B (see Fig. 75 and
Table 3). Thus, in optokinetic nystagmus in a direction toward the cerebral
hemisphere in which the electrode was located, a more marked increase in
cerebral blood flow was observed more often than during optokinetic nystagmus
in the opposite direction. In certain neighboring areas of the brain, however, the
velocity of the blood flow during optokinetic nystagmus in the direction
opposite to the location of the electrode was not increased, but was reduced.
Changes in the cerebral blood flow thus indicate that a more marked increase in
neuronal activity is possible during optokinetic nystagmus in a direction toward
EYE MOVEMENTS AND HIGHER CORTICAL FUNCfIONS 141

the hemisphere into which the electrode is implanted than during optokinetic
nystagmus in the opposite direction. It is difficult to compare these findings
with clinical evidence that optokinetic nystagmus is disturbed toward the
opposite hemisphere in patients with lesions of the parietotemporooccipital and
also of the posterior frontal areas of the brain.
Analysis of the relationship between changes in the cerebral blood flow
and the direction of optokinetic nystagmus is made extremely difficult by the
fact that areas of reduced blood flow are detected in the immediate vicinity of
areas of increased blood flow. Also, as has already been stated, in certain
neighboring areas of the brain, reciprocal relationships are found in the changes
in the cerebral blood flow during optokinetic nystagmus in different directions.
A functional neurocirculatory mosaic is thus revealed in the cerebral
hemispheres during optokinetic nystagmus, and its pattern bears an extremely
complex relationship to the direction of nystagmus.

Eye Movements and the "Constancy" of Visual Perception

The "constancy" of visual perception plays an important role in inter-

action between the organism and the surrounding world, and according to
Gellhorn (1953), it is one of the most complex types of homeostasis. When an
object moves in space, its image moves over the retina. A similar displacement
arises if the head or eyes are turned. The visual system has to distinguish
between true displacement of images of surrounding objects and false displace-
ment due to movements of the eyes, and this distinction can be made only if
constant information regarding the position of the eyes in the orbit and their
movement is provided.
Different views are held on the sources of this information. According to
Sherrington (1918), most of the information on the position and movement of
the eyes reaches the brain from the proprioceptors of the ocular muscles. The
existence of proprioceptors in the ocular muscles has been demonstrated by
histological and electro physiological methods. The work of Brindley and Merton
(1960) and of Ludvigh (1952), however, has provided convincing evidence that
impulses from the proprioceptors of the ocular muscles do not give rise to
sensations relative to the position and movements of the eyes. Sherrington's
hypothesis is thus in conflict with more recent advances in the physiology of
vision.
Another hypothesis, put forward by Helmholtz (1896), also envisages a
constant stream of information to the visual system on the position and
movements of the eye. In Helmholtz's opinion, however, the source of this
information is not the proprioceptors of the ocular muscles, but "replicas" of
the command or "volitional messages." The morphological structures responsible
for this "duplication" of the command and for the provision of information on
A

B
EYE MOVEMENTS AND HIGHER CORTICAL FUNCTIONS 143

its nature to the appropriate brain structures are the axon collaterals of motor
neurons at different levels of the nervous system (Ramon y Cajal, 1899). In the
spinal cord, these axon collaterals of motoneurons form synapses with Renshaw
cells, which play an important role in the regulation of movements.
Helmholtz's hypothesis lies at the basis of modern views on the mech-
anisms of constancy of visual perception (Sperry, 1950; Holst, 1954; Walsh,

~ ~
tf t t

~
"
~ t,

~
.11/

+, ~,
t,

~3
t, ~
"
.1.1

~?
" - 1 min

Figure 78. Local cerebral blood flow in the superior areas of the right premotor region in a
patient before operation for arteriovenous aneurysm of the anterior parietocentral gyrus.
(A,B) Roentgenograms of the skull. (C) Hydrogen clearances. The hydrogen clearances
correspond to blood flow at rest, during reading aloud and to himself, speech, optokinetic
nystagmus to the left and right, and arithmetic. The arrows indicate: (1) the beginning of
inhalation of hydrogen; (2,3) the beginning and end of reading aloud; (4,5) the beginning
and end of reading to himself; (6,7) the beginning and end of speech; (8,9) the beginning
and end of optokinetic nystagmus to the left; (10,11) the beginning and end of optokinetic
nystagmus to the right; (12,13) the beginning and end of subtracting from 300 by 17's;
(14,15) the beginning and end of subtracting from 300 by 2's; and (16,17) the beginning
and end of multiplying two-cligit numbers by 4.
 TABLE 6
Local Cerebral Blood Flow in Superior Areas of the Right Premotor Region

Velocity of cerebral blood flow (ml/l00 g per min)

Optokinetic
nystagmus

Difficult Simple Reading Reading To the To the

subtractiona subtractionb MultiplicationC to himself aloud Speech left right At rest

53.1 38.3 63.1 27.4 43.5 53.1 38.3 46.5 19.8

58 38.3 63.1 30.1 53.1 53.1 33.1 43.5 19.3
63.1 43.5 69.3 34.4 53.1 63.1 38.3 46.5 20.4
58 38.3 69.3 33.1 46.5 53.1 33.1 43.5 20.4
63.1 36.3 63.1 36.5 46.5 53.1 38.3 41 21
63.1 41 69.3 34.4 43.5 53.1 34.4 43.5 19.8
63.1 38.3 69.3 36.5 46.5 53.1 34.4 46.5 24
63.1 38.3 69.3 33.1 49 63.1 38.3 46.5 25.4
69.3 17.3
14.4
23.1
19.8
22.4
19.3
 M: 60.5 39 66.9 33.1 47.7 57.1 36.0 44.6 20.4
0: ±3.8 2.2 3.6 2.4 3.9 4.4 2.4 2.1 2.7
m: ±1.3 0.78 1.2 0.85 1.38 1.45 0.85 0.75 0.72

L-p < 0.001---1 L- p < o.oOI--.J

1..-_ _ p < 0.001--.....J
1..-_ _ _ _ _ p < 0.001----~

1..-_ _ _ _ _ _ _ P < 0.001----------'

'------------p < 0.001------------1
1..-_ _ _ _ _ _ _ _ _ _ _ _
p < 0.001--------------1
1..-_ _ _ _ _ _ _ _ _ _ _ _ _ _ _ p <0.001------------------1
1..-_ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ p <0.001--------------------1

a Subtraction from 300 by 17's.

b Subtraction from 300 by 2's.
e Multiplication of two-digit numbers by 4.
146 CHAPTER SIX

<I

<1<1 <I

<I
<l<l c:
<l
00 <l<l ~ "E
0 00
0 00
---0
Cl

o
o ~ ....
0
o ---E
~ N
u.
CIl
<:I ..J
)C
""'"
~)C )(x x
~ )(
~

2 ~ ~ ~ ~ ~ ~ ~
u!w/6 OOL/IW '[~81
B
c
Figure 79. Blood flow in two areas of the right parietal lobe in a patient undergoing operation for a right-sided carotid-cavernous anastomosis:
(circles) at rest; (triangles) speech; (crosses) optokinetic nystagmus to the left. (A) LBF in the right parietal region. The subscripts refer to the
two electrodes. (B,C) Roentgenograms of the skull showing the positions of the electrodes.
A

B
EYE MOVEMENTS AND HIGHER CORTICAL FUNcrIONS 149

1957; Gregory, 1958; Hein and Held, 1965). N. A. Bernshtein's ideas on the
origin of the "motor image" and the "programming" of movements in the
nervous system are of great importance to the development of these views. In
accordance with these views, it is postulated that a "program" of eye movements
is formed in the opticomotor structures of the brain; the appearance of this
program leads to appropriate functional adjustments in the visual system. As a
result of this "preparation" of the visual system for the reception of information
concerning movement of images over the retina, all surrounding objects appear
stationary during voluntary movements of the eyes.
Under certain conditions, a "discrepancy" between different items of
information may arise, and this gives rise to a sensation of motion of the
surrounding objects in the field of vision. Such a "discrepancy" was observed in
a patient with paralysis of the ocular muscles of the right eye, but with intact
visual function of both eyes. If the left eye was closed and the patient attempted
to turn the right eye w the side, she developed a temporary illusion that
surrounding objects were moving in the same direction. This phenomenon

.---
1 min

Figure 80. Local cerebral blood flow in the medial areas of the left parietotemporooccipital
region in a patient undergoing operation for an arteriosinus anastomosis. (A,B) Roent-
genograms of the skull. The hydrogen clearance values correspond to blood flow at rest,
during reading aloud, and during optokinetic nystagmus to the left and to the right. (C)
Hydrogen clearance values. The arrows indicate: (1) the beginning of inhalation of
hydrogen; (2,3) the beginning and end of reading aloud; (4,5) the beginning and end of
optokinetic nystagmus to the left; and (6,7) the beginning and end of optokinetic
nystagmus to the right.
150 CHAPTER SIX

TABLE 7
Local Cerebral Blood Flow in Medical Areas of the Left Parietotemporooccipital
Region

Velocity of cerebral blood flow (ml/lOO g per min)

Optokinetic nystagmus

To the right To the left Reading aloud At rest

87 87 87 99
99 99 87 69.3
99 87 87 69.3
63.1 77.5 99.6 77.5
87 87 87 77.5
87
69.3
87

M: 87 87 89.4 77.5
a: ±20.8 ±8.48 ±7.61 ±33
m: ± 9.3 ±3.95 ±3.41 ±12.1
L-_ _ _ _ _ _ _ _ _ _ _ _ p > 0.5------------.....J
L-_ _ _ _ _ _ _ p > 0.6 _ _ _ _ _ _ _....J
P > 0.2 -----'
,-I- - -

can be explained on the basis of Helmholtz's hypothesis. In an attempt to move

the stationary eye, information reaches the visual system only on the magnitude
of the stimulus arising in the opticomotor structures of the brain, but no
information is obtained on movement of the image over the retina. Under these
conditions, the illusion arises that surrounding objects are moving. During
passive movement of the eye caused by pressing with the finger over the angle of
the palpebral fissure, information is obtained only on movement of the image
over the retina. "Matching" of this information with information from the
opticomotor structures of the brain is not observed, however, so that a sensation
that objects are moving in the field of vision appears. These fmdings suggest that
"afferentation of the command," i.e., direct monitoring of the state of the
opticomotor structures of the brain, is essential for the control of voluntary eye
movements. This "afferentation of the command" also evidently leads to the
appearance of information that is compared with information from the retina.
The term afferentation as applied to the system controlling voluntary
movement is undoubtedly provisional, and must be used with caution. The
essential qualitative difference between this "afferentation of command" and
 EYE MOVEMENTS AND HIGHER CORTICAL FUNCTIONS 151

SPEECH

ARITHMETIC

OPTOKINETIC NYSTAGMUS

+'*
+

LBF increase: 0 < + ~ 50%,50 < + ~ 100%,100 <

LB F decrease: 0 < - ~ 50%, 50 < - ~ 100%. No change: 0
+~ 150%,150 < +~ 200%
Arrows indicate direction of optokinetic nystagmus relative to the fast component

Figure 81. Summary of changes in blood flow in the right and left cerebral hemispheres
during different functional loads.

the activity of receptor formations at the periphery must be taken into account.
Since the object of this "afferentation" is the action "plan" or "program," the
afferent stimuli must also contain information about this program (Bernshtein's
principle of "peeping into the future"). Because of these stimuli, the visual
system undergoes functional retuning, and it is prepared for the reception of
information on movement of the images over the retina. "Constancy" of visual
152 CHAPTER SIX

•
u!w/6 00 L/lw •::181
B c
Figure 82. (A) Mean values of blood flow in the inferior areas of the right parietal region in a patient undergoing operation for righHided
carotid-cavernous anastomosis at rest (shaded) and in the act of subtracting by different numbers (1, 2, 3, etc.) from 300. (B,C)
Roentgenograms of the skull showing the positions of the electrodes.
 154 CHAPTER SIX

TABLE 8
Local Cerebral Blood Flow in the Inferior Area of

LBF during subtraction from

At rest 2 3 4 5 6 7 8

69.3 231 24.8 150.6 105 115.6 169.1 154 105

63.1 210 38.5 119.4 97.6 119.4 169.1 169.1 105
46.3 231 30.1 119.4 110 138.6 138.6 182.3 105.3
63.1 210 34.7 138.6 105 123.7 150.6 191.6 113.5
69.3 169.1 29 119.4 97.6 138.6 143.5 210 105
69.3 169.1 38.5 138.6 99 123.7 138.6 182.3 105.3
57.7 182.3 40.8 138.6 97.7 119.4 150.6 182.3 97.6
63.1 154 33.1 119.4 99 123.7 191.6
53.3 210 69.3 119.4 105 123.7
63.1 53.3 119.4 99
57.7 36.4 128.3
69.3 46.3 169.1
69.3 30.1 138.6
69.3 43.4 169.1
69.3 30.1 154
76.1 57.7 150.6
69.3 33.1
69.3 29
69.3 53.3
63.1 57.7
69.3
69.3
69.3
63.1

aM: 65.3 197.3:1= 40.4:1= 131.1 :1= 101.5:1= 125.1 :1= 151.5:1= 183:1= 105.2:1=
(1: ±6.3 ±28.4 ±11.5 ±19.2 ±4.8 ±8.2 ±13.0 ±15.9 ±4.2
m: ±1.28 ±9.46 ±2.61 ±4.8 ±1.54 ±2.73 ±5.2 ±5.67 ±1.68

a Difference from resting value significant: .p < 0.01; tp < 0.05;:I=p < 0.001.
 EYE MOVEMENTS AND HIGHER CORTICAL FUNCTIONS ISS

the Right Parietal Lobe During Mental Arithmetic

During During
300 by: addition multiplication

9 10 11 17 2+2+2+ ... 3+3+3+ ... 4x4x4x ...

ISO.6 94.9 119.4 lOS 69.3 69.3 86.6

191.6 lOS 130.7 83.4 69.3 72 99
169.1 lOS 13S.8 92.4 7S.S 7S.S lOS
182.2 83.4 138.6 lOS 63.1 97.6 97.6
IS4 lOS lS0.6 92.4 86.6 86.6 86.6
lS0.6 83.4 138.6 l1S 72.2 63.1 69.3
123.7 110 lS0.6 92 86.6 69.3 86.6
138.6 123.7 119.4 lOS 7S.S 69.3 99
94.9 123.7 92.4
110 lOS 97.6
86.6
92.4

lS7.S:\: 111.5:\: 131.3:\: 96.6:\: 74.7' 76.1t 91.2t

±22.S ±16.3 ± 13.3 ±9.1 ±8.3 ±11.2 ±11.3
±8.03 ±S.2S ±4.29 ±2.67 ±2.92 ±4.0 ±4.03
156 CHAPrERSIX

u!w/6 OOL/IW •:181

«
B c
Figure 83. (A) Mean values of blood flow in the left cerebellar hemisphere in a patient undergoing operation for a tumor of the fourth ventricle,
at rest (shaded) and in the act of subtracting by 2's, 3's, and 4's from 300. (B,C) Roentgenograms of the skull showing the positions of the
electrodes in the left cerebellar hemisphere. Myodil injected at ventriculograp.hy (drops of myodil are visible on the roentgenograms) and the
positions of th" ~iectrodes in the left frontal lobe can be seen.
158 CHAPTER SIX

perception, i.e., a sensation of the immobility of surrounding objects despite the

appearance of voluntary eye movements, is thereby ensured.
Determination of the levels of oculomotor innervation and of the visual
system at which interaction between these systems ensuring the "constancy" of
visual perception takes place is a problem of great importance. The experimental
study of states in which the "constancy" of visual perception is disturbed is an
important aspect of the study of this problem. One such state is vertigo arising
during vestibular stimulation and in nystagmus. It can be postulated that the
disturbance of the "constancy" of visual perception in vertigo is due to the
involuntary character of the vestibular nystagmus and the absence of impulses
from those brain structures that control voluntary eye movements bringing
about appropriate functional retuning of the visual system
To test this hypothesis, experiments were carried out in which a stationary
blind spot was created in the center of the retina - an artificial scotoma (A. R.
Shakhnovich, 1965a). Tests were carried out on six healthy adults. In all
subjects, the left eye was covered with a bandage, and the local anesthetic 1%
decicaine was instilled in the right eye. To prevent blinking, the upper and lower
lids of the right eye were fixed by strips of adhesive tape, and a specially
designed Yarbus cap was secured to the eyeball immediately opposite the pupil.
The anterior surface of this cap was covered by a thin glass "window" through
which the subject could examine surrounding objects. A black shutter, 1.2 cm in
diameter, was fixed in front of this window by means of thin steel wires 2 cm
long. Under these conditions, the subjects sawall the surrounding objects at the
periphery of the field of vision, but its central part was covered by the black
shutter (Fig. 84).
The labyrinth was stimulated in all subjects by rotating them in a Baniny
chair with the head tilted forward 30° (10 turns in 20 sec). After the chair was
suddenly stopped, all the subjects developed nystagmus and vertigo (a sensation
that objects were moving in the field of vision). Against the background of the
moving surrounding objects, the artificial scotoma appeared stationary. In this
investigation, no information from the central parts of the retina, which were
covered by the shutter, reached the visual system, and there were no corre-
sponding stimuli of the "command afferentation" (eye movements in vestibular
nystagmus are involuntary), so that the sensation that the artificial scotoma was
stationary appeared.
By removal of this mismatching between the information arriving from the
central areas of the retina and from the "command afferentation," the vertigo in
the center of the visual field could be, as it were, "stopped" experimentally.
After cessation of the vertigo and nystagmus, the subjects were asked to carry
out active rotation of the eyes. In the course of these attempts, all the subjects
developed an illusion of movement of the scotoma in the same direction
(Fig. 84). This movement of the scotoma can be explained on the basis of
EYE MOVEMENTS AND HIGHER CORTICAL FUNCrIONS 159

s
a

Figure 84. Constancy of visual perception and its disturbances. (a) Yarbus cap on the
eyeball: (B) body of the cap; (W) window, (S) shutter. (b) Illusion of "movement of the
scotoma" during active rotation of the eyes and tracking. (c) Illusion of "stationary
scotoma" during vertigo evoked by stimulation of the labyrinth.

Helmholtz's hypothesis. The information on the size of the voluntary impulse

for rotating the eyes ("command afferentation") could not be matched by
information from the central part of the retina, which was covered by the
shutter, so that an illusion of movement of the scotoma appeared. Under these
circumstances, proprioceptive impulses from the ocular muscle cannot prevent
the appearance of the illusion that the artificial scotoma is moving during
voluntary rotation of the eyes.
There is every reason to suppose that these voluntary eye movements are
controlled by levels of oculomotor innervation at which the "command
afferentation" arises, i.e., that there is direct control over the state of the
optomotor structures of the brain. This "command afferentation" evidently
does not arise during every eye movement. During vestibular stimulation,
involuntary eye movements arise, and the most important factors in their
160 CHAPTER SIX

control are levels of oculomotor innervation the excitation of which is unac-

companied by information that could be compared with information arriving
from the retina. Thus, in vestibular nystagmus, there arises an illusion that
surrounding objects are moving - "vertigo." This view of one of the mechanisms
of vertigo is confirmed by clinical observations. In some patients with tumors of
the posterior cranial fossa, attacks of vertigo are accompanied by the appearance
of nystagmus. The vertigo can be stopped if these patients close their eyes.
Whereas vestibular nystagmus is accompanied by vertigo, in "spontaneous"
nystagmus, the "constancy" of visual perception may be preserved; i.e., all
surrounding objects appear stationary. To study the mechanisms of this
"constancy," an investigation was made of four patients with acoustic neuro-
fibromas, in whom marked spontaneous nystagmus was observed. These patients
had no vertigo. One eye of each of these patients was covered with a bandage,
and a cap with a shutter was secured to the other eye. When all these patients
turned their eye to the side, a marked degree of "spontaneous" nystagmus
developed, its amplitude reaching 20-30°. It seemed to the patients, however,
that the shutter fixed to the eye was stationary, like all the surrounding objects.
During an active transfer of fixation through a small angle 3-4 times smaller
than the amplitude of the nystagmus, however, all the patients developed an
illusion of movement of the shutter. The sensation of immobility of the shutter
during nystagmus may indicate that motor impulses evoking "spontaneous"
nystagmus do not lead to appropriate functional retuning in the receptive visual
centers. "Constancy" of perception of surrounding objects in the absence of
"command afferentation" can be explained by complex retuning in relationships
between the visual and oculomotor systems. This retuning does not take place at
once: in a patient developing acute nystagmus, vertigo usually appears at the
same time, but it soon stops despite the continued presence of the nystagmus.
The stability of perception of the environment and also the absence of an
illusion that the shutter fixed to the eye was moving in a subject with
involuntary spontaneous nystagmus cannot be explained by the simple hypo-
thesis of comparison between information of the "command afferentation" and
information from the retina. Considering the prolonged character of spon-
taneous nystagmus (which distinguishes it from nystagmus associated with
vestibular stimulation), the possibility of complex functional tuning in relation-
ships among different innervation systems must be taken into account.
One of the mechanisms creating the "constancy" of visual perception is
evidently what Beeler (1967) calls "saccadic suppression." This phenomenon is
based on functional inhibition of the visual system during saccadic eye
movements. Cessation of the spike discharge of certain neurons in the visual
cortex during saccadic eye movements may point to a connection between the
mechanisms of the "constancy" of visual perception and higher cortical
functions.
EYE MOVEMENTS AND HIGHER CORTICAL FUNCTIONS 161

Changes in unit activity in "sensory" areas of the cortex are found not
only during eye movements, but also during limb movements. A special
investigation of this important problem was made by Evarts (1972) on monkeys.
The unit activity of precentral (motor) and postcentral (sensory) neurons was
compared during performance of conditioned-reflex movement (flexion and
extension of the wrist) by the monkey. These experiments showed that the
postcentral neuron becomes active later than the precentral neuron. Usually,
precentral neurons became active 40-60 msec before the beginning of pressure
of the animal's paw on the turning handle (Le., 10-30 msec before changes in
the EMG of the agonist muscle). Postcentral neurons, on the other hand,
changed their activity at an interval of 0-20 msec after the beginning of pressure
on the handle (Le., 30-50 msec after changes in the EMG of the agonist
muscle). However, the earliest precentral neurons to become active did so
120-140 msec, and the earliest postcentral neurons 40-60 msec, before
pressure began to be exerted on the handle. Since most postcentral neurons
changed their activity after the pressure began, their discharges could be the
result of sensory feedback. One cannot rule out the possibility that early activity
of the postcentral neurons was also due to sensory feedback, because the time of
the earliest postcentral activity (40-60 msec before pressure began) coincided
with the time of reduced activity of the antagonists, which took place before the
changes in activity of the agonists. Evarts, however, does not rule out the
possibility that discharges of some postcentral neurons may begin even before
the effect of peripheral feedback. He draws support, in so doing, from the
theory of the corollary discharge (Sperry, 1950; Teuber, 1966), according to
which impulses run from the motor to the sensory region during the initiation
and motivation of voluntary movement, so that the sensory region of the cortex
is "warned" of the forthcoming movement before information about that
movement arrives through peripheral feedback. For this mechanism to function,
it is evidently necessary to have extensive connections between the precentral
motor cortex and the postcentral sensory cortex (Jones and Powell, 1969).
Taken as a whole, these fmdings suggest that activity of the precentral cortical
neurons before movement may modify the activity of the postcentral sensory
neurons before the arrival of impulses through sensory feedback, which operates
only after the movement begins.
Neuronographic investigations thus provide indirect information on the
spread of "copies of movement programs" from the motor to the sensory
regions of the cortex. Just as before, however, the most convincing findings in
support of the existence of these "copies of programs" that are so important to
the "constancy" of visual perception have been obtained by the use of
psychophysiological methods. Of the latest work in this direction, the experi-
ments of Mateev (1973) merit special attention. A photic stimulus, 100 JlSec in
duration, with a known delay relative to the beginning of the saccade was shown
162 CHAPTER SIX

on the screen of a television monitor. By changing the delay, the stimulus could
be presented before, during, and after the saccade. The stimulus was shown
against a dark screen to which an illuminated scale was fixed. Two colored
fixation points, which determined the amplitude of the saccadic eye movement
(l2°), were fixed at the edges of this scale. The stimulus was located in the
middle of the scale - immediately in front of the subject's eyes. The subject
performed a saccadic eye movement from the left fixation point to the right. He
then stated the scale division above which he had seen the stimulus.
These tests showed that during a saccade and for about 100 msec before it
began, the subject determined the position of the stimulus incorrectly, per-
ceiving it as displaced in the direction of the saccade. The maximum error in
determining the position of the stimulus occurred at the beginning of the
saccade, when it was 4-6°, equivalent to ~-~ the angular magnitude of the
saccade. In Mateev's opinion, these experiments show that "constancy" of visual
perception can be ascribed to the "copy of the motor command" that prepares
the visual centers for receiving information about movement of images over the
retina before eye movements begin. This mechanism ensures constancy of
perception of the location of an object except between the interval from -150
msec to +60 msec around the beginning of the saccade. Within this time interval,
a systematic error of determination of stimulus location is observed.
The findings described above indicate that interaction between the
oculomotor and visual systems, which determines the "constancy" of visual
perception, has a complex spatiotemporal organization. However, the question
of the levels of the visual system and of the oculomotor innervation at which
interaction takes place between these systems responsible for the "constancy" of
visual perception remains unsolved. Further investigations are necessary in order
that a solution to this difficult problem may be found.
 Conclusion

The functional role of the nervous system in the organization of goal-directed

behavior is one of the most important problems for study in modern neurology.
The progressive ideas expressed by Descartes 300 years ago on the "inflexible"
connection between stimulus and response are clearly contradicted by the basic
principles of modern neurophysiology. This theory received a severe blow a
hundred years ago from Sechenov who established that the character of the
response in the spinal frog depends not only on the characteristics of the
stimulus, but also on the initial position of the stimulated limbs (see Sechenov,
1926). Sechenov's ideas were developed further by Pavlov as a result of his
investigations, which showed that strengthening or extinguishing of the response
depends on reinforcement (see Pavlov, 1951).
The elementary notion of an "inflexible" connection between stimulus
and response has been replaced by new ideas on the ability of the nervous
system to plan goal-directed behavior on the basis of past experience. These
ideas have had a considerable influence on the subsequent development of
neurology, neurophysiology, neuropsychology, and neurocybernetics. They
formed the basis for concepts such as the "action acceptor" of Anokhin (1958),
the TOTE (test-operant-test-exit) scheme ofG. Miller etal. (1960), the "set" of
Uznadze (1958), and the principles of the "physiology of activity" of
Bemshtein.
Bernshtein pointed out that during movements, forces of inertia and
reactive (external) forces participate, as well as active muscular (internal) forces.
It is impossible a priori to take into consideration the effect of all these many
factors on the course and results of performance of movement. Accordingly,
Bernshtein (1947) postulated the existence of sensory corrections as an essential
mechanism of the construction of goal-directed movement. In addition to
163
164 CONCLUSION

instant correction of movement in the course of its performance (post factum

regulation), the pretuning of excitability of all motor and sensory units
participating in the performance of movement before it actually begins (ante
factum regulation) also plays an essential role. According to Bernshtein's
concept, any voluntary movement is preceded by the formation of a "motor
model" or "program" of movement in the nervous system. This "program" sets
out the basic characteristics and provides for the attainment of the end result in
accordance with the purpose of the movement.
The results of the author's experiments demonstrate the important role of
"programming" and "anticipation" in the control of eye movements (ftxation,
tracking, saccadic, convergent). The most general "programs" of a whole
movement are formed on the basis of simpler "subprograms." Interaction
between "programming" mechanisms of different degrees of complexity leads to
the solution of both tactical and strategic problems of movement organization.
The effecting of the motor "programs" is dependent in a complex manner
on visual afferentation. Under certain conditions, the effecting of motor
"programs" becomes independent to some extent of sensory correction. If there
is a marked change in the character of the afferent information, the effecting of
"programs" may be disturbed. In turn, motor "programs" have an effect on
visual perception, and in particular, they have an important role in maintaining
its "constancy."
The problem of the connection between mechanisms of movement
"programming" and particular brain structures is an important fteld for study.
Observations on patients with local brain lesions and the results of electrical
stimulation of the brain can help conSiderably in ftnding a solution to this
complex problem. The study of behavior of single neurons at different levels of
the oculomotor innervation is a particularly promising approach.
The functional role of "programming" of eye movements can be discerned
at the lowest level of the oculomotor innervation, namely, when discharges of
the motor units of the eye muscles are recorded: the character of this activity at
the beginning of the phase of tracking can be used to judge the subsequent
duration of this phase. This surprising ability of the motoneuron to "foresee the
future" is a manifestation of function of the innervation system of the ocular
muscles as a whole.
In understanding the mechanisms of organization of this integrated
system, Bernshtein's ideas on the functioning of "multilevel adjustments,"
headed by an appropriate "leading level," are extremely useful. In Bernshtein's
opinion, an important task in the study of the nervous mechanisms of movement
control is the discovery of the principles governing interaction among the various
interdependent subsystems (levels) of movement control. In the hierarchically
organized system of movement control, each lower level is not simply an
effector-relay system to transmit without distortion messages from the higher
CONCLUSION 165

level, but it is an active integrating part of the system as a whole (Gel'fand and
Tsetlin, 1962, 1966). One of the mechanisms of vertical organization of the
movement control system is the principle of "least interaction" (Gel'fand and
Tsetlin, 1962, 1966; Pyatetskii-Shapiro and Shlk, 1964). A characteristic
feature of this method of control is that the primary result of "vertical"
interaction between the various levels of the hierarchically organized system is a
change in the state mainly (if not entirely) of those "intermediate" elements
(intemeurons) at a lower level, which, in tum, are responsible for "horizontal"
interaction at that level. The change in state of the output elements for a
particular level is mainly the result of "horizontal" interaction, and is only to a
lesser degree the result of direct "vertical" influences from higher levels on the
output elements at the lower level.
The innervation mechanisms of the ocular muscles have a complex
"vertical" organization located at different levels of the central nervous system.
We can now compare the results obtained by destruction and stimulation of the
brain (Fig. 85) with the results of a direct study of unit activity and the
associated changes in the cerebral blood flow (Table 9). Unfortunately, these
datil are still not plentiful, but they nevertheless enable certain conclusions to be
drawn regarding the behavior of neurons at different levels of the oculomotor
innervation. The same motoneurons of the ocular muscles are the "final
common pathway" for different supranuclear influences, whether during fixa-
tion, tracking, saccadic, or convergent eye movements.
With an increase in the amplitude of saccadic eye movements, the number
of active motoneurons and their firing rate both increase. If the direction of the
saccade is reversed, the firing rate of the motoneurons is sharply reduced or
ceases altogether, to rise again only before the end of the saccade.
During tracking, the number of active motoneurons and their firing rate
both increase. The order of activation of individual motoneurons is constant in
the repeated phases of optokinetic nystagmus.
For a given motoneuron, the ratio between the firing rate and the tracking
speed is constant. At rest, however, each position of the eye corresponds to a
specific firing rate of a given motoneuron.
The behavior of cortical neurons differs considerably from that of the
nuclei of the cranial nerves. In the frontal opticomotor area, an increase in unit
activity arises only with a particular position of the gaze and regardless of the
direction of the tracking movement of the eyes. This "optimal" position of the
gaze differs for different neurons. During saccadic eye movements, an increase in
unit activity in the same area arises only in response to movement in a particular
direction. In the occipital opticomotor area, changes in the activity of a given
neuron (an increase or cessation) are identical in character during saccadic eye
movements in opposite directions. Neurons the activity of which increases
during tracking movements of the eyes are present in the same zone. Unlike the
166 CONCLUSION

~""""I--- '
~;......-- g

\.........~---- I()

Figure 85. System controlling eye movements and its connections with the visual and
vestibular systems (after Jung, with modifications). (1) Frontal zone for coordinated eye
movement (area 8); (2) frontooccipital association fibers; (3) pathways for horizontal and
vertical eye movement; (4) visual system; (5) zone of efferent fibers of the visual cortex
(area 18); (6) central area of the visual cortex; (7) fastigial nucleus of cerebellum; (8)
nodulus of cerebellum; (9) flocculus of cerebellum; (10) vestibular nuclei; (11) vestibulo-
spinal tract; (12) vestibular nerve; (13) vestibular organ and its receptors; (14) posterior
longitudinal bundle; (15) reticular formation; (16) lateral geniculate body; (17) fibers for
voluntary vertical eye movement; (18) fibers for voluntary horizontal eye movement;
(III,IV. VI) 3rd, 4th, and 6th pairs of cranial nerves, respectively.

case in the frontal opticomotor zone, however, this increase in unit activity
corresponds to a particular period of the tracking phase (beginning, middle, or
end), not to a particular position of the gaze. Unit activity in the visual cortex is
thus characterized by its indifference to the direction of eye movements; at the
same time, however, changes in the activity of a given neuron in the visual cortex
are defmitely dependent on the cycle of optokinetic nystagmus (the phase of the
saccade; the beginning, middle, or end of the phase of tracking). During tracking,
CONCLUSION 167

TABLE 9
Activity of Motor Units of Ocular Muscles, Neuronal Discharges, and Local
Cerebral Blood Flow at Different Levels of Oculomotor Innervation

Fixation Movements. The activity of certain neurons of the brainstem reticular formation
depends on the position of the gaze during fixation (Keller, 1974; Sparks and Sides, 1974).
The unit activity of the Purkinje cells of the flocculus of the cerebellum depends on
vestibular stimulation during active inhibition of v~stibulooculomotor reflexes, and is
independent of compensatory eye movements in darkness. These findings indicate that the
flocculus participates in visual inhibition of vestibulooculomotor reflexes (Lisberger and
Fuchs, 1974).
Each position of the eye at rest corr~sponds to a particular fuing rate of a particular
motoneuron of the ocular muscles (Robinson, 1970; Fuchs and Luschei, 1970).
The unit activity of motoneurons of the ocular muscles is unchanged after removal of
the cerebellum (Westheimer and Blair, 1973b).

Convergent Movements. During convergence, the unit activity of those motoneurons that
are functionally active during other types of eye mov~ment (tracking, saccadic, fixation) is
modified (Keller and Robinson, 1972).
The activity of motoneurons of the ocular muscles is identical in character in
convergent and version eye movements (Keller, 1973).

Tracking Movements. Increased unit activity arises in neurons of the frontaloptomotor area
during tracking when the gaze is fixed in a certain position irrespective of the direction of
movement. This position of the gaze differs for different neurons (Bizzi, 1967).
A burst of spike activity arises in various neurons of the occipital optomotor area at
different stages of the tracking phase (beginning, middle, or end). This period remains
constant for a given neuron in repeated phases of nystagmus and also during reversal of its
direction. There is no on-or-offresponse to light (A. R. Shakhnovichand Shtil'man,1969).
The number of active motor units in the agonist muscles of tracking gradually
increases, as does their frring rate also. The order of activation (and of inactivation in the
antagonist muscles) of the motor units is constant in repeated slow phases of optokinetic
nystagmus. The subsequent duration of this phase of nystagmus can be judged from the rate
of increase of the frring rate at the beginning of tracking (A. R. Shakhnovich and
Nebieridze, 1967a,b). The degree of change in the frring rate of the motoneuron depends on
the velocity of the tracking movement of the eyes. The ratio between frring rate and
tracking velocity is constant for a given motoneuron (Robinson, 1970).
The activity of some neurons of the reticular formation changes during smooth
tracking movements of the eyes (Sparks and Sides, 1974).

Saccadic Movements. An increase in the unit activity of neurons in the frontal optomotor
area arises during saccades in one direction only (Bizzi, 1967).
The frontal optomotor area (area 8) participates in opticooculomotor coordination
(Moller et al., 1973).
Changes in unit activity in neurons of the occipital opticomotor area are identical in
character during sacca des in opposite directions. A burst of spike activity arises 20-100
msec after the beginning of the saccades both in light and in darkness and continues for
100-400 msec, covering the beginning of the next tracking phase; there is no response to
Continued
168 CONCLUSION

TABLE 9 (Continued)

light. Discharge of other neurons ceases during the saccade and also as an on-and-off
response to light (A. R. Shakhnovich and Shtll'man, 1969; Noda et al., 1972).
In the visual association area (anterior parts of the middle suprasylvian
zone - area 7), unit activity changes before and during saccades and also 40-80 msec after
their beginning. Area 7 participates in the coordination of the visual and oculomotor
systems (Straschill and Schick, 1973).
Some neurons of the lateral geniculate body change their activity after the beginning
of saccades in darkness (BUttner and Fuchs, 1973).
Neuronal activity of the intralaminar portion of the thalamus usually precedes the
saccade; a relationship exists between the duration of the saccades and the burst of spike
activity. Changes in spike activity in the nonspecific thalamic nuclei usually precede the
saccade by 50-150 msec, and these changes can arise in darkness (Schlag et al., 1973,
1974).
In the superior colliculus, a burst of unit activity arises 30-300 msec before the
beginning of a saccade in a particular direction, in both light and darkness.
In the deep layers of the corpora quadrigemina, there are neurons the spike activity
of which precedes saccades of a specific amplitude and direction, and is unchanged during
saccades of greater or lesser amplitude (Wurtz and Goldberg, 1971, 1972).
The unit activity of the superior colliculus during sleep does not correlate with eye
movement. In the waking state, the same neurons respond selectively to the direction of the
saccades (increased activity in one direction, inhibition in the other direction) (Arduini et
al., 197 4a,b).
In the central gray matter of the aqueduct of Sylvius, a burst of unit activity precedes
the saccade by 7 -8 msec and is independent of its direction (Matsunami, 1972).
In the reticular formation, a burst of neuronal spike activity usually precedes the
beginning of the saccade (by 12-20 msec). The activity of other neurons is reduced during
the saccade (Luschei and Fuchs, 1972; Cohen and Henn, 1972b; Sparks and Sides, 1974;
Keller, 1974). Neurons of the pontine reticular formation have monosynaptic connections
with motoneurons of the oculomotor nerve (Highstein et al., 1974).
The Purkinje cells of the cerebellum show synchronized changes of unit activity with
fast eye movements (Harlay et al., 1974).
A burst of spike activity in motoneurons of the ocular muscles precedes the
beginning of the saccade by 7 msec and ends 10 msec before the end of the saccade
(Robinson, 1972; Fuchs and Luschei, 1970). With an increase in the amplitude of the
saccade, the number of active motoneurons and their firing rate both increase (A. R.
Shakhnovich and Nebieridze, 1967a,b). If the direction of the saccade is reversed, the firing
rate of motoneurons of the ocular muscles is sharply reduced or ceases altogether, increasing
again only before the end of the saccade (A. R. Shakhnovich and Nebieridze, 1967a,b;
Robinson, 1970).
Some motoneurons of the ocular muscles alter their activity during saccades (phasic
motoneurons). Other motoneurons alter their activity during saccades and tracking
(phasic-tonic motoneurons) (Henn and Cohen, 1972, 1973).
The activity of motoneurons of the ocular muscles depends on a preceding saccade
(static hysteresis) (Eckmiller, 1974).
Simultaneous recording of the activity of two motoneurons (A and B) shows that
during saccades in a particular direction, the activity of one neuron (B) never begins before
changes in the activity of the other neuron (A) (Eckmiller et al., 1974).
Continuea
CONCLUSION 169

TABLE 9 (Continued)

Repetitive Eye Movements - Nystagmus. Changes in the blood flow in neighboring areas of
the cerebral cortex of different character and degree (increase or decrease in flow) are
observed. These changes reflect reciprocal relationships during a change in the direction of
nystagmus. With elementary functional loads (optokinetic nystagmus), the changes in the
cerebral blood flow are less extensive in character than during more complex psychological
tests (A. R. Shakhnovichetal., 1970, 1972, 1974).
Simultaneous recording of activity from motoneurons of the ocular muscles and
vestibular neurons shows that the rhythm of nystagmus depends not on direct interaction
between bilateral vestibular nuclei, but on the activity of reticular neurons sensitive to
bilateral vestibular influences (Baker and Berthoz, 1974).
Both direct connections between vestibular and oculomotor systems (three-neuron
reflex arc) and polysynaptic connections through the reticular formation playa role in the
origin of vestibular nystagmus (Shinoda and Yoshida, 1974).
Different motor units of the ocular muscles function in different phases of
nystagmus: phasic fibers during the fast phase and tonic fibers during the slow phase
(Matyushkin, 1961, 1963, 1972).
The same motoneurons of the ocular muscles are the final common pathway for
different supranuclear influences at rest (fIXation) and in the different phases of optokinetic
nystagmus (A. R. Shakhnovich and Nebieridze, 1967a,b; Robinson, 1970; Fuchs and
Luschei, 1970).

neurons in the frontal opticomotor area are also indifferent to direction, and
their activity depends only on the position of the gaze. A defmite relationship
between unit activity and the direction of saccadic eye movements is found in
this area. In contrast, the activity of motoneurons in the nuclei of the 3rd, 4th,
and 6th pairs of cranial nerves depends on the direction of both tracking and
saccadic eye movements.
Thus, as the level of innervation of the ocular muscles rises, the responses
of its neurons have an increasingly less differentiated relationship to the
direction of eye movements. At the same time, the activity of a particular
neuron becomes increasingly more clearly dependent on a particular type of eye
movement (a change in spike activity during the saccade and also at the
beginning, middle, or end of the tracking phase). At the lowest level of
innervation of the ocular muscles in the nuclei of the cranial nerves, however,
the same motoneurons can be the "fmal common pathway" for various
supranuclear influences, and changes in its spike activity may differ in character
during different types of eye movement (fIxation, tracking, saccadic, and
convergent). These same motoneurons have, however, a clearly differential
response to the direction of movement. In the complex hierarchy of innervation
mechanisms of the ocular muscles, certain general principles governing the
behavior of single neurons can thus be distinguished: as the level of innervation
rises, unit activity becomes more clearly dependent on the type of eye
movement and less dependent on the direction of movement.
170 CONCLUSION

These findings provide a basis for the hypothesis that different types of
eye movements are connected with the function of different subpopulations of
neurons located at the highest levels of oculomotor innervation. These different
sub populations of neurons converge on motoneurons of the ocular muscles in
the nuclei of the 3rd, 4th, and 6th pairs of cranial nerves, which are the final
common pathway for various supranuclear influences. This complex function of
the oculomotor apparatus in "programming" movements is evidently the result
of interaction among neuron populations at different levels of innervation.
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 Index

Abducens nerve, eye muscle control by, 3-4 Cat visual cortex, neuron activity in, 113-114
Accommodation Central nervous system
convergence ana, 105-106 eye movements in, 87-88
"inflexible" connection in, 106 "motor pretuning" in, 88
range of, 100 posterior longitudinal bundle of, 4
Accommodative convergence, 100-101 role of in goal-directed behavior, 163
"programming" of, 103 vertical organization of innervation me-
Action acceptor concept, 163 chanisms in, 165
Activity, physiology of, 163 Cerebellar cortex
ft.iUa~l1~~~vu, -;~!::::~::::~ ~""up",u~nt ~nci _ 150 as "clock" for programmed movements, 14-
Afferentation of command, 150, 158 15
Afferent fibers, firing rate in, 16 eye movement and, 13, 88
Anesthesia, eyeball movement in, 6 "holding lines" in, 14
Aneurysm, tremor in, 36 lesions of, 15
Auditory nerve neurofibroma, drift and, 62 Cerebellum, eye movements and, 13, 88
Cerebral blood flow; see also Local cerebral
Basal ganglia, in eye movement control, 8-9 blood flow
Behavioral arousal reaction, eye movements changes in, 116, 123, 151
in, 5 decrease in, 123
Blind spot, artificial, 158 functional heterogeneity and, 125
Brain; see also Cerebral blood flow functional loads and, 125
blood supply to, 114-115 increase in, 117 -123
blood volume in, 114 local, see Local cerebral blood flow
dynamic localization of functional sys- resting, 116
tems of, 133 Cerebral cortex, eye movement regulation
free oxygen level and, 15 in, 9-10,109-114; see also Cerebral
functional systems of, 133 blood flow
Brainstem Colliculooculomotor tract, 18
electrical stimulation of, 6 Command afferentation, 158-160
"horizontal fixation center" in, 5 Convergence
lesions of, 3 accommodative, see Accommodative con-
microtremor and, 26 vergence
nystagmus and, 62 asymmetrical,102
strychnine in, 5 eye movements and pupil reactions during,
Bulbar encephalitis, tremor and, 28 98-100
185
186
Convergence (cont'd)
inflexible connection with accommoda-
tion, 106
innervation mechanism of, 106-107
paralysis of, 8
Convergent eye movements, 97 -107; see also
Convergence
asymmetrical convergence in, 102
convergence in, 98-100
eye muscles in, 167
innervation mechanisms in, 100-107
pupil reactions and, 98-100
stereoscopic vision and, 97-98
Corpora quadrigemina, 12
Cortex, cerebellar, see Cerebellar cortex; see
, also Cerebral cortex
Cortical lesions, functional system distur-
bance from, 133
Cortical unit activity, eye movements and,
109-114
Corticotectal tract, optic radiation and, 12
Cranial nerves, anatomy of, 2
Darkness
drift and, 59
fixation micromovements in, 59-61
micro nystagmus in, 62
saccade eye movements in, 79
Death, microtremors as indication in, 28-29,
35,37,40-41
Direction detectors, in retina, 68
Drift, 24
auditory nerve neurofibroma and, 62
change in direction of, 48
corrective role of, 58
darkness and, 59
quantitative characteristics of, 63
saccades and, 47-49, 51-53
temporal characteristics of, 56
Eye(s); see also Fixation movements; Sac-
cadic movements; Tracking move-
ments; etc.
"floating" movements of, 65
muscles of, see Eye muscles
Eye-centering system, fIXation and, 66
Eye displacement, "memory" and "effort"
in correction of, 6Hi2
Eye movements
in behavioral arousal reaction, 5
INDEX
Eye movements (cont'd)
cerebellar "holding lines" and, 14
cerebral cortex and, 9-10, 13
convergent, see Convergent eye movements
Helmholtz's theory of, 141-150
and higher cortical functions, 109-162
horizontal, 4-7
local cerebral blood flow and, 114-141
nervous system changes and, 87
opticomotor area and, 110
programmingin,81-87, 103,149, 164,170
rapidity of, 8
repetitive, 169
saccadic, see Saccadic eye movements
system controlling, 166
tracking, see Tracking eye movements
vertical, 7-8
visual perception constancy and, 141-162
Eye muscles
activity of motor units of, 167-169
electrical activity of during saccadic eye
movements, 92-96
electrical activity of during tracking move-
ments, 72-78
electrical discharges in, 2
innervation mechanisms of, 1-21
interaction in during convergence, 100-107
motoneuron activity in, 2, 74-78
nystagmus and, 72-75
peripheral innervation of, 1-3
"phasic" vs. "tonic" fibers in, 93
proprioceptors and, 16-18,59-62
regulating mechanisms of, 3
separate fibers, 1
supranuclear innervation mechanisms of, 3-
16
Eye muscle tonus, afferent regulation of, 16-21
Fixation
cortical mechanisms of, 11
eye-centering system and, 66
optical axis displacement during, 64
psychic disturbance of, 109
Fixation micro movements
control mechanism in, 45-64
in darkness, 60-61
orientation of, 46, 54-60
Fixation movements, 23-66; see also Fixation
micromovements; Microtremor;
Tremor
INDEX
Fixation movements (cant 'd)
different types of, 53
"motor image" concept of, 62
optical axis displacement during, 64
stabilization in, 64-66
visual perception and, 23-24
Frontal optomotor area
descending fibers from, 12
stimulation of, 10-11
topographical arrangement of, 11
Gasserian ganglion, 17
Goal-director behavior, v, vii
Graphemes, "recording" of, 133
Hemorrhage
microtremor and, 35-40
tremor and, 28-29
Holding lines, in cerebellar cortex, 14
Homatropine, accommodative convergence
and, 102
~;V.l.:~.:.::!.::! ?:rt~ Tnnvp.ments .. control of, 4-6
Hypermetropia, 105
Images
moving, see Moving images
perception of, 67-69,141-162
"Inflexible" connection, in stimulus-response "Motor image" concept, of fixation move-
relationship, 163
Innervation mechanisms
structure and functional organization in,
1-21
vertical organization of, 165
"Least interaction" principle, 165
Local cerebral blood flow; see also Blood;
Cerebral blood flow
dynamics of, 114-116
eye movements and, 114-141
in left cerebellar hemisphere, 157
in left parietotemporooccipital region,
127-128,149-150
in medial zones of right parietal region,
131-132
neuronal group functioning and, 129
in nystagmus, 133-139
in right occipitallobe, 139-140
in right parietal lobe, 147, 153-155
in right precentral gyrus, 134-137
in right premotor region, 143-145
187
Mesencephalon, in stereoscopic vision, 108
Micromovements, see Fixation micromove-
ments
Micronystagmus, 62
visual perception and, 24
Microsaccades, illumination and 59; see also
Saccade(s)
Microtremor; see also Tremor
bursts of, 39
fatal implication of, 28-29,35,37,40
hemorrhages and, 35
as indicator of motor unit and ocular mus-
cle activity, 15-45
motoneuron pool and, 42
motor unit activity and, 44
provocation and, 39
in unconsciousness, 29-36
Midbrain lesions, vertical eye movements
and, 7; see also Brain; Brainstem
Motoneuron pool, microtremor and, 42
Motoneurons
firing rate of, 2
IUnCtIoJl(1~ ~~~'" v!", ;~
proprioceptors and, 17
saccade and, 168
in tracking, 165
as velocity detectors, 78
ments,62
Motor unit, of eye muscles, 72
Movement, eye, see Eye movement; see also
Convergent eye movements; Fixation
movements; Saccadic eye movements
Movement perception, psychophysiological
tests of, 67 -69; see also Visual perception
Moving images, 67-69
Multilevel adjustments, leading level in, 164
Muscles, eye, see Eye muscles
Neuron(s)
activity of in saccades, 111-113
as direction detectors, 68
as velocity detectors, 68
Nucleus prepositus hypoglossi, role of in eye
movements, 8
Nystagmus
blood flow changes and, 169
brainstem and, 62-63
electrical activity of eye muscles during,
73-76,94
188 INDEX

Nystagmus (conI 'd) Relative accommodation, range of, 100; see

floating movement and, 65 also Accommodation
local cerebral blood now in, 133-139 Resting cerebral blood flow, spatial organiza-
neuron activity in, 110 tion in, 116; see also Local cerebral
spontaneous, 160 blood flow
stretch receptors and, 75 Reticular formation, neurons of, 66
vestibular, vs. optokinetic, 160 Retina, direction detectors in, 68
Retinal images, disparity of in asymmetrical
Occipital optomotor area convergence, 104
descending fibers from, 12
stimulation of, 11 Saccade(s); see also Fixation micromovements
Ocular muscles, see Eye muscles amplitude of, 49-51, 93
Ocular tremor, see Tremor change in direction of, 48
Oculomotor mechanism components of, 47
vestibular system and, 19-21 darkness and, 59
visual system and, 18-19 deimed,24
synapses and, 19-20 drift and, 4749
Ophthalmoplegia, saccadic eye movements quantitative characteristics of, 63
in,82 neuron activity and, 111-113
Opticokinetic nystagmus, see Nystagmus thalamus firing pattern and, 9
Opticomotor area, eye movements in, 110 Saccade development, basic stimulus for,
Optic radiation fibers, corticotectal tract 45
and,12 Saccadic eye movements, 79-96; see also
Optomotor areas, eye movements in, 10-13 Saccade(s)
acceleration and retardation in, 84
Paraabducens nucleus, in eye muscle control, "anticipation" at beginning of, 96
4 as ballistic movements, 81
Peristriate cortex, in stereoscopic vision, 108 brain and, 82
Perlia's nucleus, 8 "braking system" in, 83-87
Phasic fibers, in eye muscles, 93-94 control mechanisms in, 81-92
Photokymograph, 46 correction for stimulus displacement in,
Physiology of activity, 163 70
Posterior longitudinal bundle, role of, 4 electrical activity of eye muscles during,
Programming 92-96
of accommodative convergence, 103 eye muscles in, 167-168
in saccadic eye movements, 81-87 ilXation points and, 86
in visual perception, 149, 164, 170 inhibition of, 6-7
ProprioceptoIS "motor pretuning" in, 88
eye muscle tonus and, 16-18 perception decrease in, 79
motoneurons and, 17 "programming" of, 81-82,87,96
role of, 18,59-61 pupil reaction in, 81
in visual perception constancy, 141-143 "rigid program" for, 86-87
Psychic disturbance of fixation, 109 tracking and, 69
Purkinje cells, fast eye movements and, 13- triggering of, 84-85
14,88,168 Saccadic suppression, 80,160-161
Saccadic tonicity, 80
Rabbit visual cortex, unit activity in, 112- Sarcoplasm, of thin muscle fibers, 1
113 Scotoma
Refraction disturbances, in convergent eye artificial, 158
movements, 105-106 movement of, 158-159
INDEX 189

Semicircular canals Tremor (cont'd)

eye muscles and, 19
stimulation of, 20-21
Sense organs, in goal-directed behavior,
v, vii
Static hysteresis, 96
Stereoscopic vision
and convergent eye movements, 97-98
eye muscle reflexes in, 105
integrative mechanisms in, 107
mesencephalon in, 108
psychophysiological methods of investigat-
ing,98
Stimulus-response relationship, "inflexible"
connection in, 163
Strychnine, in brainstem, 5
Subdural hematoma, ocular tremor and, 36-
37
Superior colliculus, 18
Suprasylvian gyrus, eye movements and, 109
Thalamus
eye movements and, 88
firin" nattern in. 9
Tonic fibers, in eye muscles, 93
Tonus, afferent regulation of, 16-21
TOTE scheme, 163
Tracking movements
activation of fresh motor units in, 76
electrical activity in ocular muscles during,
72-78
extrapolation in control of, 69-72
eye muscles and, 72-78,167
motoneurons in, 165
neuron activity in, 110-111
smooth character of, 69
Tremor; see also Microtremor
aneurysm and, 36
in bulbar encephalitis, 28
characteristics of, 25
hemorrhage and, 28-29, 37-39
in infectious hepatitis, 43
jaundice and, 42
normal and pathological forms of, 27-28
"pathological bursts" of, 25-26,45
subdural hematoma operation and, 36-37
in unconsciousness, 29-34
Tremorogram, 25-27,4445
Trigeminal nerve, eye muscle and, 17
Unconsciousness
degree of, 30
microtremor and, 29-36
Velocity detection, neurons in, 68
Vertical eye movements
optomotor areas in, 12-13
paralysis of, 7
Vestibular nerve, sectioning of, 4
Vestibular system, oculomotor system and,
19-21
Vestibulooculomotor reflexes, 13
Visual functions, saccadic eye movements
and, 79-81
Visual perception
COIl~LaIlt.,;y u; ~1l .l'V~~~V.l1 ~v "'J':' ~~~.:.-::::::::~::~
141-162
"discrepancy" in, 149
fixation movements in, 23-24
Helmholtz's hypothesis of, 159
"matching" of information in, 150
"programming" in, 149
"volitional messages" in, 141-143
Visual system, oculomotor system and, 18-
19
Voluntary eye movements
afferentation and,151-159
oculomotor innervation and, 159
Writing disturbances, dynamic localization
and, 133
Yarbus cap, 64,158