Download Anatomic Studies on the Superior Colliculus

Investigative Ophthalmology
June 1972
434 Gouras
turtle cones until it was specifically looked for.
HUBEL: Isn't it more striking in ganglion cells
and couldn't this be accounted for by allowing
some of the horizontal cell connections to go on to
bipolars as well as on to receptors?
GOURAS : I agree, there must be strong opponent
interaction after the receptor level but some of
this antagonism may also begin in the receptors.
Anatomic studies on the superior colliculus
R. D. Lund
The superior colliculus is organized into a superficial zone which is directly connected with
other parts of the visual system and a deep zone which is not directly connected toith other
visual centers. Within the superficial zone, there is a convergence of retinal and visual cortical
afferents. The size, distribution, and synoptic patterns formed varies between animals. Removal of an eye in neonatal rats, at a time when there are few synapses formed in the colliculus, causes a great increase in the area of distribution of the uncrossed pathway of the remaining eye. At least some of the increased pathway arises from areas of retina which
normally would have projected only contralaterally. Removal of an eye at later developmental
stages results in no such abnormal projection, although there is evidence that synoptic sites
formerly occupied by optic terminals became taken over by other neurons.
Key words: superior colliculus, superficial layers, corticotectal pathway, retinotectal pathway,
plasticity of connections
T_l_he superior colliculi, paired hillocks on
the dorsal surface of the midbrain, are
concerned with aspects of visual attention
and centering of the visual image on the
retina and as such are of considerable importance in normal visual function.1"5 Of
particular interest is how the processing of
visual information through these structures
compared with that through the geniculocortical system and to what degree the
From the Departments of Biological Structure
and Neurological Surgery, University of Washington School of Medicine, Seattle, Wash.
98195.
The original work described in this report was
supported by United States Public Health Service Grants EY-00491, EY-00596, and NB04053 from the National Institutes of Health.
Some facilities were supported by United States
Public Health Service Grant HD-02274.
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colliculi function independently of the geniculocortical system.
Each colliculus is a laminated structure,
consisting of seven layers, each defined by
the presence or absence of tangentially
oriented fiber bundles.0 The layers can be
grouped into two major laminar divisions
—superficial and deep. The superficial division receives inputs from contralateral
and ipsilateral retinas and from visual areas
of the ipsilateral cortex and sends fibers
to the thalamic nuclei, lateralis posterior
and ventral lateral geniculate body,7 and
to the deeper laminar division. The deep
division, in addition to the input from the
superficial layer, receives inputs from
somatosensory and auditory systems, from
nonvisual cortical areas, and from the contralateral colliculus.810 Its major outputs
are to the brainstem, particularly to nuclei
involved in coordination of head and eye
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movements,8'a1"13 and there is also an ascending projection to the posterior region
of the thalamus.7'8
In this review attention is restricted to
the superficial laminar division. It is composed of two tangential fiber layers—the
stratum zonale (at the surface) and the
stratum opticum (lying deep)—and between them a complex layer of neurons
and neuropil—the stratum griseum superficiale. The majority of the visual afferents
to the colliculus enter via the stratum opticum and terminate principally in the stratum griseum superficiale. A small number
of afferents distribute in the stratum zonale
which also contains the axons of intrinsic
neurons. It is not known whether the afferents running in this layer are different
in function from those entering via the
stratum opticum, or whether they are a
remnant homologue of the superficial optic
layer found in nonmammalian vertebrates.6
The stratum zonale varies in its degree of
development between animals, being 10
to 15 fi thick in the monkey,14 an animal
in which it is well developed, and completely absent in the ground squirrel.15
A topographic retinal projection can be
mapped on the surface of the colliculus
such that the more central part of each
half visual field lies anteriorly, and the
more peripheral part, posteriorly in the contralateral colliculus. However, in some animals (e.g., rat,1(i cat,17 squirrel, tree shrewis)
the map continues anteriorly beyond the
vertical midline of the visual field so that
the most anterior point on the colliculus
is about 15 degrees nasal of the midline.
Such an overlap does not occur in the
retinal projection to the lateral geniculate
nucleus.18"20
The topographic map can be determined
physiologically or by anatomical degeneration studies after small retinal lesions. In
both cases, the optic projection appears as
columns tangential to the surface.21- 22 Small
lesions of visual cortical areas also cause
small patches or columns of degeneration23
in the superficial laminar division of the
superior colliculus. The corticotectal map
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Superior colliculus 435
is topographically arranged such that an
area of cortex receiving from one retinal
area projects to an area of the colliculus receiving from the same retinal
area.23 There are two interesting problems
related to this matching topography, which
holds good for rat,23'24 rabbit,25'2G cat,9'27
tree shrew,2S) 29 and monkey.30 In the monkey, the central seven degrees of the retina
does not project to the superior colliculus.30
After removal of one eye, no obvious degeneration can be found in the anterior
part of the colliculus either by light14-30
or electron microscopy,14 nor can significant autoradiographic label be detected in
the same area after injection of the eye
with tritiated leucine.31 However, the macular area of the visual cortex does project
to this anterior region. The second problem concerns the projection of the corticotectal pathway to the anterior region of
the colliculus in the cat. Since the retina
temporal to the midline representation projects to the anterior part of the colliculus
but not to the lateral geniculate nucleus
and hence visual cortex, one might expect
on the basis of matching topography that
there should be no corticotectal pathway
to this region. This is not the case,9 suggesting either that the corticotectal map
is less discrete than the retinotectal map
or that a special relationship occurs in
this region.
Despite the correspondence of the retinotectal and corticotectal field maps in a
variety of animals, there are some notable
differences in the extent of termination of
each pathway between animals. Two extremes are shown in Fig. 1. In the rat
the retinotectal pathway projects heavily
throughout the strata griseum superficiale
and zonale, with a higher density of terminals in the more superficial half, while in
the monkey retinotectal terminals are restricted to the superficial half of the stratum griseum superficiale.14' 32 In contrast,
the corticotectal pathway of the rat terminates sparsely mainly in the deeper half
of the stratum griseum superficiale, but in
the monkey terminates heavily throughout
436 Lund
Investigative Ophthalmology
June 1972
35
Vl'H
.V. A*
I'l't
Fig. 1. Diagrammatic cross-section of the left
superior colliculus. Details of the rectangle are
shown for rat and monkey. In Column 1, fiber
patterns are indicated; in Columns 2 and 3, the
distribution of crossed and uncrossed optic pathways respectively are shown; and Column 4
shows the distribution of the corticotectal pathway, sz = stratum zonale; sgs = stratum griseum
superficiale; so = stratum opticum.
the whole depth of the layer. Ground
squirrel15 and tree shrew33 both show a pattern similar to the rat, although the corticotectal pathway has a heavier density of
termination in the deep half of the stratum
griseum superficiale. The retinotectal pathway of the cat resembles that of the rat
in its distribution pattern, but the corticotectal pathway more closely resembles
that of the monkey, although its density
of termination becomes reduced closer to
the surface.3'1'35
By the electron microscope, the same
general terminal types are recognized as in
the lateral geniculate nucleus.30 There are
two main differences. First, no obvious
encapsulated synaptic zones are seen, although it is apparent in some animals at
least that there are zones of complex synaptic formations, albeit poorly delineated
from adjacent areas. Second, there are
many more clearly identifiable presynaptic
dendrites. In rat,32 ground squirrel,15 cat,34'
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and monkey,14 the only animals yet
studied with the electron microscope, the
optic terminals contain spheroidal vesicles
and pale mitochondria and are presynaptic
to dendrites or dendritic spines, terminals
containing flattened vesicles (some of
which are presynaptic dendrites), and occasionally to cell bodies. In rat and cat
they undergo both primary dense and
neurofilamentous reactions in degeneration, while in the monkey the neurofilamentous reaction is very uncommon. The
corticotectal pathway in rat synapses only
with small dendrites and dendritic spines,
but in both cat and monkey it also forms
serial synapses. In degeneration it undergoes the primary dense reaction only in
rat, ground squirrel, and cat, but in monkey
it also undergoes the neurofilamentous reaction.
These results indicate that the relative
size, distribution, and synaptic relations of
retinotectal and corticotectal pathways vary
between animals, and on this basis the
effect of cortical lesions on tectal function
should also vary. This seems to be the
case when comparing the collicular physiological response patterns after cortical lesions in ground squirrel37 and rat3S with
those of cat.39'40 It is not known whether
the variable projections are due to an
over-all change in each pathway or to the
addition or loss of particular axon populations, in the case of the retinotectal
pathway, for example, involving one ganglion cell type. It has been suggested14 that
the two major degenerative reactions may
differentiate two axon populations in the
optic nerve, each of which projects both
to the lateral geniculate nucleus and superior colliculus in the rat, and one of
which in the monkey projects to the lateral
geniculate nucleus and the other to the
superior colliculus.
In contrast to the crossed optic pathway, which distributes above the stratum
opticum, the uncrossed retinotectal pathway terminates within the stratum opticum
in many mammals (rat,41 rabbit,42 ground
squirrel,15'43 tree shrew), although in cat44
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and monkey30 it appears to be distributed
within the same zone as the crossed pathway. The uncrossed pathway relates to the
visual field map in that it is always found
anteriorly, but its posterior extent varies
between and within animal groups. It is
less extensive, for example, in albino than
pigmented animals as well as in Siamese
compared with regular cats, in which in
addition the terminal zone appears restricted to the more posterior part of the
colliculus.45
It is of considerable interest to know
what factors guide some axons from the
retina to join the optic tract of the same
side and end in ipsilateral visual centers,
while others cross at the chiasma and
terminate contralaterally. Studies on Siamese cats indicate that this process may
be disturbed, presumably as a result of
a genetic defect, such that axons from
areas of retina which should have ended
in the contralateral lateral geniculate body
end instead in the ipsilateral nucleus, although still maintaining the correct topographical distribution.'10
A study we47 undertook on rats has
shown that the distribution of the uncrossed pathway can be modified experimentally by removing the opposite eye
early in development. In normal albino
rats, the uncrossed pathway is extremely
small and distributed in the anteromedial
region of the stratum opticum (Fig. 2). If
one eye is removed at birth, at a time
when very few synapses of any kind are
found in the colliculus, an uncrossed pathway from the other eye, as charted by
degeneration studies at 3 months or more
of age, comes to occupy most of the area
of the ipsilateral colliculus, terminating
mainly in the strata griseum superficiale
and zonale. If the first eye is removed
from an animal 12 days or older, the uncrossed degeneration due to removal of
the other eye at a later time is exactly as
in a normal animal. If the first eye is removed at the fifth postnatal day, there is
partially increased distribution of the uncrossed pathway of the other eye. A simi-
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Superior colliculus 437
Right eye
removed
at birth
Right eye
removed
at 5 days
Right eye
removed
at I2'days
Fig. 2. Diagram of distribution of the left eye
of a rat on the superior colliculi when viewed
from above. The anterior borders of the colliculi
lie uppermost on the page. The solid hatched
line indicates the heavy crossed pathway and the
fine hatched line indicates the less densely distributed uncrossed pathway.
lar pattern of results has been found in
the lateral geniculate body.4S There are a
number of possible explanations for these
results:
1. The apparent degeneration from removal of the second eye is really residual
degeneration remaining from removal of
the first eye. Control studies show that
degeneration can persist for one and onehalf years after a lesion in an adult rat,
although for no more than two weeks in
a newborn animal. Care has been taken
to account for this factor.
2. The increased area of projection may
be a sprouting of the regular uncrossed
pathway from its normal area of distribution. This is the explanation suggested in
previous studies.47'50 It has a major drawback and that is that, by comparison with
Amphibia,49 one might expect at birth that
the topographic map between retina and
tectum is already established and that this
438 Lund
map could not be subsequently upset even
by experimental lesions. Such sprouting
would seem unlikely as a major cause of
the increased pathway, since the regular
uncrossed pathway is so small compared
with the sprouted pathway and the amount
of axonal branching required would be
enormous. There is no indication of such
an involved pattern of branching of degenerating axons, nor is there indication
of a major spread of axons from the anteromedial zone to cover the whole colliculus.
In addition, the further experiment described below offers evidence of an alternative explanation.
3. Each ganglion cell at birth sends
axons to both colliculi, and, as synapses
form, one of these atrophies. This proposition cannot be born out by degeneration
studies after short-term survivals following unilateral enucleation at birth.
4. Not all the axons have grown past
the chiasm at birth. If an eye is removed
at birth and the optic nerve degenerates,
axons which normally would have crossed
the axons in that nerve may not be able
to cross them either because of an unbalanced field effect or because they are
degenerating. Therefore, they may reroute
and end in the ipsilateral tectum instead.
There is no clear evidence as to whether
all optic nerves have grown past the
chiasm at birth, but it is apparent that
retinal cell division, possibly involving the
ganglion cell layer, continues for a week
after birth. One expectation of this hypothesis would be that small lesions in parts
of the retina of the intact eye which would
normally not be expected to project ipsilaterally should cause ipsilateral degeneration. A subsequent series of experiments
has shown this to be the case, both for
the superior colliculus and lateral geniculate body.48
5. One final possibility, which would also
be compatible with the experiment described above, is that there may after optic
degeneration at birth be collateral branching of the remaining optic nerve to supply
ipsilateral as well as contralateral colliculi.
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Investigative Ophthalmology
June 1972
The type of reorganization shown here
seems to be in part at least one of redistribution of axons to the side of the
brain opposite to that of which they normally project. Another type of reorganization is evident if an eye is removed at
any time after synapses are formed and
an appropriate minimum survival time allowed (three to five days in animals up
to three weeks of age and seven to 14
days in adults).47'50 Under these conditions, there is indication with the electron
microscope that the degenerating optic
terminals become removed from their postsynaptic sites and replaced by other axon
terminals or by neuroglia. The other terminals may contain spheroidal vesicles like
the optic terminals, but many contain flattened vesicles. Whether these new connections are functional is not clear. A considerable percentage of them show aggregation of synaptic vesicles along at least
part of the membrane. There is reasonable
evidence that the presence of synaptic
vesicles indicates the potential for transmission at the synapse, and as such allows
the possibility for considerable reorganization of functional connections within a deafferented region. Any such reorganization
must always be taken into account when
assessing the behavioral and physiologic
changes caused in response to specific
lesions.
The author wishes to thank Dr. Jennifer S.
Lund for helpful criticism, Mrs. E. Merrick and
Mr. R. Cole for technical assistance, and Mrs.
C. Lade for valuable secretarial help.
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Volume 11
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18. Lane, R. H., Allman, J. M., and Kaas, J.
H.: Representation of the visual field in the
superior colliculus of the grey squirrel
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19. Montero, V. M., Brugge, J. F., and Beitel,
R. E.: Relation of the visual field to the
lateral geniculate body of the albino rat, J.
Neurophysiol. 31: 221, 1968.
20. Sanderson, K. J.: The projection of the visual
field to the' lateral geniculate and medial
interlaminar nuclei in the cat, J. Comp.
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21. Mcllwain, J. T., and Buser, P.: Receptive
fields of single cells in the cat's superior
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colliculus, Exp. Brain Res. 5: 314, 1968.
22. Lund, J. S., and Lund, R. D.: Unpublished
results.
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superior colliculus of fibers originating in the
visual cortex, Nature (Lond.) 204: 1283,
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24. Lund, R. D.: The occipitotectal pathway of
the rat, J. Anat. (Lond.) 100: 51, 1966.
25. Giolli, R. A., and Guthrie, M. D.: Organization of projections of visual areas I and II
upon the superior colliculus and pretectal
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26. Giolli, R. A., and Guthrie, M. D.: Organization of subcortical projections of visual
areas I and II in the rabbit. An experimental
degeneration study, J. Comp. Neurol. 142:
351, 1971.
27. Garey, L. J.: Interrelationships of the visual
cortex and superior colliculus in the cat, Nature (Lond.) 207: 1410, 1965.
28. Abplanalp, P.: Some subcortical connections
of the visual system in Tree Shrews and
Squirrels, Brain Behav. Evol. 3: 155, 1970.
29. Harting, J. K., and Noback, C. R.: Subcortical projections from the visual cortex
in the tree shrew (Tupaia glis), Brain Res.
25: 21, 1971.
30. Wilson, M. E., and Toyne, M. J.: Retinotectal
and corticotectal projections in Macaca mulatta, Brain Res. 24: 395, 1970.
31. Hendrickson, A., Wilson, M. E., and Toyne,
M. J.: The distribution of optic nerve fibers
in Macaca mulatto, Brain Res. 23: 425, 1970.
32. Lund, R. D.: Synaptic patterns of the superficial layers of the superior colliculus of the
rat, J. Comp. Neurol. 135: 179, 1969.
33. Abplanalp, P.: The neuroanatomical organization of the visual system in the tree shrew,
Folia Primatol. 16: 1, 1971.
34. Sterling, P.: Receptive fields and synaptic
organization of the superficial gray layer of
the cat superior colliculus, Vision Res. 11:
(Suppl. 3) 309, 1971.
35. Lund, R. D.: Structural organization of the
superior colliculus and dorsal lateral geniculate body of the rat, J. Physiol. Soc. Jap.
32: 555, 1970.
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of the mammalian lateral geniculate body,
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37. Michael, C. R.: Units in superior colliculus
of ground squirrel, J. Gen. Physiol. 10: 2485,
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and monkeys, Exp. Neurol. 20: 312, 1968.
39. Wickelgren, B. G., and Sterling, P.: Influence of visual cortex on receptive fields
440 Lund
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in the superior colliculus of the cat, J. Neurophysiol. 32: 1, 1969.
Rosenquist, A. C , and Palmer, L. A.: Responses of single cells in the cat superior
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169: 414, 1971.
Lund, R. D.: Uncrossed visual pathways of
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1965.
Giolli, R. A., and Guthrie, M. D.: The primary optic projections in the rabbit. An experimental degeneration study, J. Comp.
Neurol. 136: 99, 1969.
Tigges, J.: Retinal projections to subcortical
optic nuclei in diurnal and nocturnal squirrels,
Brain Behav. Evol. 3: 121, 1970.
Laties, A. M., and Sprague, J. M.: The projection of optic fibers to the visual centers
in the cat, J. Comp. Neurol. 127: 35, 1966.
Kalil, R. E., Jhaveri, S. R., and Richards,
W.: Anomalous retinal pathways in the Siamese cat: An inadequate substrate for normal binocular vision, Science 174: 302, 1971.
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Discussion
SPRAGUE: IS the synaptic takeover you described
age dependent? Is it specific for S or F type terminals or is it nonspecific?
LUND: Both S or F type terminals are involved
in the takeover. It appears nonspecific within the
limits of our technique, but this may only say that
our technique is nonspecific. We have found the
takeover in all animals in which there are formed
synapses at the time of the lesion. In animals
lesioned at the time when there is a massive formation of optic synapses (15 to 25 days postnatal),
there are always a higher percentage of abnormal
synapses than at subsequent survival times.
BURKE: IS there competition between nerve and
glial cells in this?
LUND: It appears that both neuronal and neu-
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Investigative Ophthalmology
June 1972
roglial processes (astrocytes and oligodendrocytes)
can come to occupy postsynaptic sites as they
become vacated by degenerating optic terminals.
Whether they compete and the process is nonspecific (perhaps just to block off hyperactive
receptor sites) or whether certain neuronal processes may subsequently come to occupy sites initially covered by glial processes is unclear. So far
we have defined the system. The next step would
appear, to be to investigate this problem of specificity both between neurons and between neurons
and neuroglia.
WURTZ: Is there any Golgi material in monkey
comparable to what you showed in rat?
LUND: T. Langer and I have spent some time
looking at Golgi preparations of the monkey colliculus. All the cell types seen in the rat can be
found in the monkey. There are a number of differences: (1) There is always a preponderance of
pyriform cells staining (these are also shown by
Sterling in the cat [Vision Res. 11: Suppl. 3]). (2)
The clear lamination in rat of upper and lower
stratum griseum superficiale is not obvious. (3)
The horizontal cells impregnated so far do not
have long processes as have been found in the
rat. (4) There are some cells with dendrites which
pass through the stratum opticum into the stratum
griseum intermedium. This means that units recorded in the stratum griseum superficiale may be
activated directly by pathways terminating in the
deeper layers.
HUBEL: In the cat it is said that there is about
20 degrees or so of ipsilateral field projection which
is a puzzle, since it's hard to think of it coming
from 17, 18, or 19. Presumably this may come
via the optic nerve but then you'd wonder whether
the receptive fields would be the same. Is there
any evidence for an ipsilateral projection in the
monkey?
LUND: Neither Schiller and Koerner (J. Neurophysiol. 34: 920, 1971) nor Kadoya et al. (J.
Comp. Neurol. 142: 495, 1971) found units in
the rostral part of monkey colliculi crossing the
midline to any degree, as they do in cat and some
other animals.
MARK: Have you considered the possibility of
axonal sprouting at the chiasm?
LUND: This is, of course, one possibility which
must be considered. It could perhaps be eliminated
by firing optic terminals in the ipsilateral colliculus
antidromically and seeing whether a response could
be recorded in the other colliculus.
SCHILLER: One of my greatest puzzles with respect to the colliculus has to do with retinal versus
cortical contributions to cell function. I am particularly puzzled in monkey with the reports you
just gave as well as those of Wilson and Toyne.
We have found in recording from monkeys after
ablations of visual cortex that the receptive field
characteristics in these superficial layers do not
Superior colliculus 441
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Number 6
seem to be affected very dramatically and can
subserve foveal vision as well. Have you any ideas
on what this cortical input is doing as well as on
the anatomy of the lower layers of the colliculus
about which you haven't talked but which may
clarify some things?
LUND: That really is puzzling. I think it highly
unlikely that there is a major direct optic projection to the rostral colliculus. It cannot be demonstrated by light or electron microscope degenerative methods, nor can it be shown by autoradiographic labeling methods. Assuming that your
cortical lesions are complete and that your electrodes really are in the superior colliculus and not
in adjacent .pretectal nuclei, one has to postulate
that there may be indirect optic influences via
possible pretectum-collicular or geniculate-collicular
pathways. Alternatively, there could be a very
small number of direct optic terminals to the region
which are below the resolution of detection by the
anatomical methods used but which, are sufficient
to produce unit activity.
Your comments regarding the relatively normal
response patterns in the colliculus after cortical
lesions suggest to me two possibilities—either your
experimental situation does not exploit the normal
activity parameters of the corticotectal pathway,
or the widely assumed anatomical dogma that the
size of a pathway bears a direct relation to its
magnitude of influence is mistaken. With regard to
the last, I think it would be very valuable to test
the effects of cortical lesions in monkeys and rats
(or ground squirrels) under absolutely identical experimental conditions. As is described here, these
animals show marked differences in the relative
sizes of the two pathways (retinotectal and corticotectal) and one might expect that this should
be reflected in functional differences.
The deep layers with the possible exception of
part of the stratum griseum intermedium do not
receive a projection from visual cortical areas. This
does not, of course, mean that they do not respond
to more indirect visual influences.
The.primate superior colliculus and the
shift of visual attention
Robert H. Wurtz and Michael E. Goldberg
.he primate oculomotor system can generate eye movements in response to visual
stimuli. The superior colliculus, long
thought to be a component of that system,
occupies a transitional point in the oculomotor system. It receives input directly from
the retina and indirectly from the visual
cortex,9-22 and many investigators have
demonstrated cells with visual receptive
fields in the superior colliculus of monkeys
and other mammals.17 In the primate, the
anatomic connections to the motor nuclei
of the extraocular muscles are not direct.11
However, stimulating the colliculus results
in eye movements14 and single cells in the
From the Laboratory of Neurobiology, National
Institute of Mental Health, Bethesda, Md.
Downloaded From: http://iovs.arvojournals.org/ on 06/16/2017
colliculus discharge before voluntary eye
movements.15'20> 23
Although it is clear that the superior
colliculus is in the pathway between the
visual stimulus and the eye movement, the
role played by the colliculus in the process
of generating a visually guided eye movement is not at all clear. One view of colliculus function is that it provides the target
information necessary for the accurate
guidance of eye movements.13"15 However,
two different lines of evidence are highly
dissonant with this view. The first is that
monkeys without superior colliculi show no
gross deficit in visually guided eye movements.1' 12 The second is that the functional
properties of the cells in the monkey superior colliculus, which have large receptive fields or respond before eye move-