Information Processing Underlying Gaze Control

437 Pages·1994·12.96 MB·English

by  J. M. Delgado-García

Pergamon Studies in Neuroscience No 12
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Information Processing
Underlying Gaze Control
Edited by
J. M. Delgado-Garcia, E. Godaux and P.-P. Vidal
PERGAMON
UK Elsevier Science Ltd, The Boulevard, Langford Lane,
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First edition 1994
Library of Congress Cataloging in Publication Data
Information processing underlying gaze control/ [edited
by] J.M. Delgado-Garcia, E. Godaux, and P.-P. Vidal. --
1sted.
p. cm. -- (Pergamon studies in neuroscience; no. 12)
Includes indexes.
1. Gaze-Regulation. 2. Eye-Movements--Regulation.
I. Delgado-Garcia, J. M. II. Godaux, E. III. Vidal, Pierre
Paul.
IV. Series.
QP477.5.I54 1994
612.8'46--dc20 94-19381
British Library Cataloguing in Publication Data
A catalogue record for this book is available from the
British Library.
ISBN 0 08 042506 2
Printed in Great Britain byAlden Press, Oxford
Preface
THIS volume represents the published proceedings of a Satellite Workshop to the
16th European Neuroscience Association meeting held from September 22 to 24,
1993, at the Colegio Hernando Colon of the University of Sevilla, Spain.
The goal of the workshop was to bring together researchers to exchange
information on the computational properties of neuronal circuits underlying gaze
control. The relative ease with which the appropriate sensory stimuli and the
resulting behavioral responses could be defined and measured has resulted in a
great amount of information on the neuronal network that generate and control
eye and head movements. However, if clear definitions for the different steps of
this computational processing have emerged, the neuronal and molecular
mechanisms at play are far from being elucidated. Furthermore, the relatively
recent discovery that neurons have complex intrinsic membrane mechanisms
which endow them with non-linear integrative properties has opened a new
branch of gaze physiology, but has also further complicated the issue.
Hence, in the organization of the workshop as well as in the edition of this
book, the main objective was to summarize some of the recent advances in our
fast growing field. Special emphasis was given to relatively new research areas,
ranging from the neurochemistry of the oculomotor system to the psychophysics
of gaze control. Finally, we wanted to include recent results from experiments and
descriptions of ongoing research programmes as well as brief reviews on each
topic under consideration in the different chapters. Thanks to the effort of the
authors, we believe that these objectives have been fulfilled at least in part. For
the sake of clarity, the contributions have been gathered in seven sections: (I)
morphology and physiology of extraocular motor nuclei, (II) anatomo-functional
organization of the saccadic system, (III) vestibular and otolithic systems, (IV)
optokinetic and smooth pursuit systems, (V) other sensory systems involved in the
control of the oculomotor function, (VI) role of the cerebellum in the genesis and
control of eye movements, (VII) coordination of eye, head and body movements.
Each of these sections has been organized by ranking each chapter according to
the following order: anatomy, electrophysiology, behavior and modelling.
It is our hope that this volume will not only be useful for those already interested
in gaze control, but that it will also help to bring new investigators into the field
and provide examples and useful discussions to other related areas of research.
XI
xii Preface
For the organizers, a very important outcome of the workshop was the
confirmation that gaze control is, more than ever, a valuable model in which basic
questions on the functional properties of the central nervous system (such as the
neural mechanisms subserving the acquisition of new motor skills or its post-
lesional plasticity) can be addressed with the most recent and advanced
techniques on anatomy, electrophysiology and molecular biology.
The workshop and the edition of this book were made possible mostly by the
altruistic and enthusiastic cooperation of M. Escudero, R.R. de la Cruz, A.
Gruart, R. Jimenez, A. Pastor and C. Zamora, to all of whom were are very
grateful.
THE EDITORS
1
The Anatomy of the Vestibulo-Ocular
System in Lampreys
M. A. POMBAL, M. C. RODICIO and R. ANADON
Department of Fundamental Biology, Faculty of Biology, University of Santiago de
Compostela, Santiago de Compostela, Spain
Studies of sensorimotor integration in lampreys are of particular interest because these
animals belong to the most ancient group of living vertebrates, the Agnatha. Lampreys
have a complex life cycle that comprises a very long larval phase, a first metamor-
phosis lasting several months, an adult phase and a prespawning second metamorpho-
sis. The oculomotor and visual systems develop over a very long period which spans
the embryonic, larval and first metamorphic phases (see Rubinson, 1990, for review);
the vestibular system, on the other hand, appears to acquire its basic pattern in early
larvae (Thornhill, 1972; Gonzalez, 1990).
The vestibulo-oculomotor pathways play an important role in controlling different
types of eye movement, but their most prominent function is to mediate the vestibu-
lo-ocular reflex to ensure stabilization of vision when the head is moving (Highstein
and McCrea, 1988). The last two decades have seen experimental anatomical studies
on the central projections of the eighth cranial nerve and higher-order octaval path-
ways in anamniotes. However, little is known about the organization of higher-order
octaval centres in fishes. From what is known, it is clear that the vestibulo-oculomo-
tor projections in lampreys differ in several respects from those in gnathostomes.
Labyrinth organs, primary octaval projections and octavomotor nuclei
The labyrinth of lampreys contains cristae with hair cells that respond to rotations of
1
2 Information Processing Underlying Gaze Control
the head, and maculae that respond to vibrations and tilt (supplying data for the control
of balance and position; Rovainen, 1979). The lamprey labyrinth is peculiar in that it
has no horizontal canal and in that the vestibular region forms a single cavity
(Lowenstein et αί, 1968); however, it responds to rotation movements in the three spa-
tial planes (Lowenstein et al, 1968; Lowenstein, 1970; Thornhill, 1972), because the
ampullary cristae of the anterior and posterior semicircular canals are orthogonally
arranged. A single ventral macular area, differentiated into horizontal and vertical por-
tions, occupies the ventral vestibular region. Both the dorsal position and the pattern
of innervation of the small dorsal macular area (macula neglecta) are unique in verte-
brates. In addition, the vestibular cavity of adult lampreys is partially divided by a cil-
iated septum into anterior and posterior ciliated chambers which are lined with a deep
epithelium bearing long, powerful cilia (Lowenstein et al, 1968). These ciliated cham-
bers are present exclusively in lampreys. The sensory areas are innervated by octaval
nerve branches containing afferent and efferent fibres. On the basis of size,
Lowenstein et al. (1968) distinguished two types of ganglion cell in the octaval gan-
glion of Lampetra fluviatilis: small cells that mainly innervate the maculae, and large
cells with long dendrites innervating only the ampullary cristae. Inputs from sensory
organs are carried by the dorsal and ventral roots of the octaval nerve, and both roots
are excited by rotations in any of the three spatial planes, as was demonstrated
electrophysiologically by Lowenstein (1970). Fibres of the dorsal root innervate the
crista of the posterior semicircular canal, dorsal macular area and caudal and medial
parts of the ventral macular area, while fibres of the ventral root innervate the crista of
the anterior semicircular canal and the rostral part of the ventral macular area
(Lowenstein et al., 1968).
Primary octaval afferents enter the octavolateral area (Pearson, 1936; Larsell, 1967;
Rubinson, 1974; Northcutt, 1979; Koyama et al., 1989; Gonzalez, 1990; Gonzalez and
Anadon, 1994), which extends in the dorsolateral wall of the medulla oblongata from
the "cerebellar plate" to the first roots of the vagal nerve (near the obex region). There
are three nuclei in the octavolateral area of lampreys (the dorsal, medial and ventral
nuclei); these form longitudinal columns constituted by cells of different sizes
(Johnston, 1902; Pearson, 1936; Larsell, 1967; Northcutt, 1979, 1980). The medial
and dorsal nuclei receive projections from the mechanoreceptors and electroreceptors,
respectively, of the lateral line nerves (Kappers et al., 1936; Bodznick and Northcutt,
1981; Boord and McCormick, 1984; Ronan and Northcutt, 1987; Gonzalez and
Anadon, 1992), while the ventral octavolateral nucleus receives ascending and
descending branches of ipsilateral octaval fibres (Stefanelli, 1937; Larsell, 1967;
Rubinson, 1974; Northcutt, 1979; Koyama et al., 1989; Gonzalez and Anadon, 1994).
Some ascending octaval fibres enter the "cerebellar plate" to terminate dorsolaterally
either ipsilaterally or contralaterally, after crossing in the octaval commissure (Heier,
1948; Larsell, 1967; Koyama et al., 1989; Gonzalez, 1990; Gonzalez and Anadon,
1994). Koyama et al. (1989) suggested that cristal and macular afferents terminate
ventrally and dorsally, respectively, in the ventral nucleus of the octavolateral area.
However, the precise pattern of termination of primary octaval afferents on the octavo-
motor nuclei and adjacent neurons of the ventral octavolateral nucleus is not known.
Several authors (Johnston, 1902; Larsell, 1967; Northcutt, 1979, 1980; Gonzalez,
1990) have described three groups of large neurons in the ventral octavolateral nucle-
us; these are known as the octavomotor nuclei (the anterior, intermediate and posteri-
The Anatomy of the Vestibulo-Ocular System in Lampreys 3
or octavomotor nuclei; Tretjakoff, 1909; Stefanelli, 1934; Larsell, 1947). Some
authors have also found a fourth nucleus (the "tangential nucleus", which may corre-
spond to the tangential nucleus of teleosts and birds) just at the entrance of the octaval
nerve (Kappers et al 1936; Stefanelli, 1937; Gonzalez and Anadon, 1994). This pat-
y
tern of distribution of octaval nuclei, in a single octaval column, is the simplest of the
three distinct patterns found among living anamniotes (the "agnathan", "gnathostome
fish" and "amphibian" patterns; Northcutt 1981), and there is clearly no one-to-one
correspondence between the different octaval nuclei of these different groups of anam-
niotes. In addition to ascending and descending octaval fibres, some unbranched pri-
mary octaval fibres appear to terminate on the neurons of the "tangential nucleus"
(Gonzalez, 1990; Gonzalez and Anadon, 1994).
It is of interest that the octaval nerve contains a number of coarse fibres which
establish conspicuous synaptic contacts with the cells of the octavomotor nuclei
(Stefanelli, 1937; Heier, 1948; Stefanelli and Caravita, 1970; Gonzalez, 1990;
Gonzalez and Anadon, 1994). These authors described large swellings on octaval
fibres in the area of contact with the large octavomotor neurons. Using electron
microscopy, Stefanelli and Caravita (1970) demonstrated that these swellings are not
terminal boutons but instead form en-passant mixed (electrical and chemical) synaps-
es with octavomotor neurons. In addition to the coarse fibres, Heier (1948) also report-
ed the existence of thin octaval fibres that appear to terminate around small and medi-
um-sized neurons adjacent to the octavomotor nuclei.
Visual system
Adult lampreys have well-developed eyes (Rochon-Duvigneaud, 1958; Kleerekoper,
1972). During the larval period, however, the eyes are subcutaneous and poorly devel-
oped (Rochon-Duvigneaud, 1958; Kleerekoper, 1972), apparently not becoming func-
tional until the first metamorphosis. The retina of the adult has two types of photore-
ceptor cell, as well as horizontal cells, bipolar cells, amacrine cells and ganglion cells
(Kleerekoper, 1972; De Miguel, 1989; Rubinson, 1990). In addition, biplexiform gan-
glion cells which contact the terminals of photoreceptors have been found in larval
lampreys (De Miguel et al, 1989). Unlike in other vertebrates, a ganglion cell layer is
not apparent in the retina, and the fibres of the optic nerve course towards the head of
the optic nerve in the inner plexiform layer near the inner nuclear layer (De Miguel et
al, 1989). The presence of two optic tracts, axial and lateral, and the distribution of
centrifugal fibres to optic centres in the thalamus, optic tectum and mesencephalic
tegmentum, as well as the presence in the lamprey retina of centripetal fibres arising
from neurons of two mesencephalic areas (the M5 nucleus and the reticular mesen-
cephalic area), have been demonstrated experimentally in adults (Reperant et al,
1980; Vesselkin et al, 1980, 1984; see Rubinson, 1990 for review). Two phases have
been distinguished in the development of the retina and the retinofugal optic pathways
in larval lampreys. The first phase occurs during the embryonic and early larval stages,
and comprises the development of the central retina and its photoreceptors (Studnicka,
1912; Keibel, 1928) and of the axial optic tract (De Miguel et al, 1990; Pombal et al,
unpublished observations). The second phase occurs in larvae longer than 60 mm, and
is characterized by the growth of a peripheral retina around the central retina (Keibel,
1928; Dickson and Collard, 1979; De Miguel and Anadon, 1987; Rubinson and Cain,
4 Information Processing Underlying Gaze Control
1989) and by the differentiation of the lateral optic tract (De Miguel et al., 1990).
Photoreceptors do not differentiate in the peripheral retina until the first metamorpho-
sis (De Miguel and Anadon, 1987; De Miguel, 1989). Several other changes occur in
both the retina (Dickson and Collard, 1979; Dickson and Graves, 1981; De Miguel and
Anadon, 1987; Rubinson and Cain, 1989) and the optic tectum (Rubinson and
Kennedy, 1979; De Miguel and Anadon, 1987) during the first metamorphosis. The
retinopetal system, on the other hand, is well developed in all larvae (De Miguel et al,
1990) and does not appear to undergo any changes during the late larval period.
It is interesting that lampreys have direct retinal projections to the oculomotor
nucleus (Fritzsch et al, 1990; Pombal et al, 1994), in addition to higher-order optic
projections from optic centres. In lamprey, visual and vestibular inputs to the motor
system in the brainstem and spinal cord are the most important inputs for controlling
the upright position of the body (Deliagina et al, 1992a,b; Orlovsky et al, 1992; Ullen
et al, 1993). In higher vertebrates, visual information is important for controlling
complex eye movements, but whether patterned vision has a role in the control of eye
movements in lampreys has not been investigated (Rovainen, 1982).
Oculomotor system
Lampreys possess six extraocular muscles: four rectus and two oblique. The four rec-
tus muscles are similar in position and function to those of higher vertebrates. The the-
oretical homologue of the superior oblique, the caudal oblique, is situated behind the
eye, while the rostral oblique is considered to be synergistic with the inferior rectus
(Rovainen, 1976). Although the extraocular muscle fibres of larval lampreys appear
tiny and are not differentiated into two types (Pombal et al, 1993), unlike those of
adults (Nakao and Aoki, 1982; Witalinski and Labuda, 1982), they are already inner-
vated (Pombal et al, 1993).
The topographic organization of the ocular motoneurons in adult lampreys has been
studied recently by Fritzsch et al (1990) by application of horseradish peroxidase
(HRP) to individual eye muscles. The muscles are innervated by three ocular motor
nuclei. Unlike in other vertebrates, the rostral and dorsal rectus and rostral oblique are
innervated by the oculomotor nucleus, the caudal oblique by the trochlear nucleus and
the caudal and ventral rectus by the abducens nucleus (Fritzsch et al, 1990). Studies
of the development of these nuclei carried out in our laboratory show that they are well
developed, with their motoneurons presenting an adult-like appearance, by the middle
of the larval period (Pombal et al, 1994). Afferents to the three ocular motor nuclei of
larvae (Pombal et al, 1994) appear to be similar to those described in adults (Fritzsch
and Sonntag, 1988; Fritzsch et al, 1990), and the presence of mature synaptic contacts
on oculomotor cells during the larval period has also been confirmed with electron
microscopy (Pombal et al, 1989).
Vestibulo-ocular connections
During vestibulo-ocular reflexes, each eye is turned by coordinated contractions of the
six extraocular muscles, and the head is moved in the complementary direction by
contraction of the rostral myotomes (De Burlet and Versteegh, 1930; Rovainen, 1979).
The Anatomy of the Vestibulo-Ocular System in Lampreys 5
The first experiments on eye-head movements were carried out by Kubo (1906) and
De Burlet and Versteegh (1930) in intact animals. Rovainen (1976) investigated the
effects of mechanical and electrical stimulation of the labyrinth organs in isolated
preparations from adult sea lampreys, and described stereotyped conjugated eye
movements and corresponding electrical activities in individual extraocular muscles.
The eye movements of the lamprey differ from those of other vertebrates because they
have only a slow phase of nystagmus and not a rapid phase in the opposite direction
to reset the position of the eye (Rovainen, 1982). In mammals the vestibulo-ocular
reflexes are disynaptic (see Highstein and McCrea, 1988, for a review), but in lam-
preys the number of synapses involved in these reflexes is still unknown.
Electrophysiological data, however, suggest that they are disynaptic (Rovainen, 1976).
The anatomical pathways involved in these reflexes were not studied experimental-
ly until very recently (Pombal, 1993). With general staining methods, Heier (1948)
described three tractus octavomotorius {anterior, medius and posterior) which are in
close contact with different groups of oculomotor cells. Other early studies (Stefanelli,
1937; Heier, 1948; Larsell, 1967) suggested that secondary vestibular projections in
lamprey coursed mainly in these tracts but also in the medial longitudinal fascicle and
the lemniscus vestibulo-lateralis or lemniscus bulbaris. The secondary octaval projec-
tions of larval lampreys have also been studied with silver staining methods by
Gonzalez (1990). The following description of octaval projections to ocular motor
nuclei is based mainly on our own observations of material from larval sea lampreys
(Petromyzon marinus L.) after in vivo and in vitro application of HRP to either the ocu-
lomotor nucleus or to one of the anterior, intermediate and posterior octavomotor
nuclei, as well as after HRP injection in the labyrinth (Pombal, 1993).
Connections between the anterior octavomotor nucleus and the oculomotor
nucleus
Previous studies with general and silver staining techniques (Heier, 1948; Gonzalez,
1990, respectively) have indicated that a tract of coarse fibres arises in the anterior
octavomotor nucleus and courses rostroventrally towards the ventral tegmental com-
missure. These fibres decussate ventral to the oculomotor nucleus, where most appear
to terminate. We have tested these findings by HRP labelling of either the oculomotor
nucleus or the anterior octavomotor nucleus. After HRP labelling of the oculomotor
nucleus, a group of cells was retrogradely labelled in the rostral part of the octavolat-
eral area, in the region of the anterior octavomotor nucleus (Pombal, 1993). Most
labelled cells were contralateral to the injection site, and were either large bipolar neu-
rons (20x13 μπι) of the anterior octavomotor nucleus or the small neurons (5-7 μιη in
diameter) considered by Larsell (1947) to constitute the primitive nucleus cerebelli.
All cell measurements were taken in transverse sections and are therefore of minimum
diameters, in view of the characteristic arrangement of octavomotor cells along the
ascending and descending fibres of the octaval nerve (Stefanelli, 1937; Heier, 1948;
Stefanelli and Caravita, 1970; Gonzalez, 1990).
Cross sections through the anterior octavomotor nucleus show that labelled cells
have short dendrites directed towards the ventral and medial nuclei of the octavolater-
al area, where they may be contacted by primary afferents from the labyrinth (ventral
nucleus; Heier, 1948; Larsell, 1967; Northcutt, 1979; Koyama et al, 1989) and from