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Effects of visual cortical ablation on pattern discrimination in the ground squirrel (Citellus tridecemlineatus)
EXPERIMENTAL
NEUROLOGY
Effects
%,270-276
(1973)
of Visual Cortical Ablation on Pattern Discrimination the Ground Squirrel (Cite//us tridecemlineotus) N. H. LEVEY, J. HARRIS, Department
AND J. A. JANE’
of Neurological Surgery, University of Virginia Charlottesville, Virginia 22901 Received
October
in
Hospital,
25, 1972
Five ground squirrels (Citellus tridecemlineatus) were trained on various visual discrimination problems following large bilateral cortical ablations. With lesions resulting only in complete retrograde loss of latera geniculate, discriminations other than those based upon total luminous flux were made easily. With lesions large enough to result in extensive retrograde degeneration of the pulvinar, a more profound deficit resulted, but not one in which complete loss of pattern vision occurred. The ground squirrel, like the tree shrew, is thus able to solve visual discrimination tasks in the absence of striate cortex.
INTRODUCTION While considerable controversy exists over the exact nature of the visual deficit following visual cortical ablation, it seems fairly well established that this lesion performed in the Malayan tree shrew results in a deficit which is qualifiably different than is a similar lesion, for instance, in the rhesus monkey (5, 7). Snyder and Diamond (7) suggested that this difference might be due to the large tectum possessedby the tree shrew; this suggestion implies that a second visual pathway involving tectum, pulvinar, and peristriate cortex might well mediate pattern vision. Studies on ablation in the tectum of the tree shrew have been consistent with this view (2, 4). In order to elaborate this hypothesis further it was thought that another species which possessesa large tectum but whose geniculostriate system differed somewhat from the tree shrew, would serve as an interesting comparison. The ground squirrel (Citellus tridecemlineatus) appeared to fulfill these criteria and indeed ablation of the visual cortex did not result in loss of pattern vision (6). 1 Supported
by
EYOO1.51-OlAl
the
Lucille
from National
Sargeant
Sebrell
Eye Institute. 270
Copyrinht All rights
9
1973 by Academic Res, reproduction in any form
Inc. reserved.
Fund
for
Brain
Research
and
1 ROl
PATTERN
FIG.
1. Typical
large
bilateral
271
DISCRIMINATION
aspiration
lesion,
animal
G6. Note
the large
optic
tectl um.
R’IETHODS s Gx
ground squirrels were subjected to large Materal cortical aspirat: ion ons (Fig. 1) and then trained in a two-choice apparatus described in previous cotntnuniration (.5). TU.O types of prol)lems \\-ere used. 7 ‘lie t involved two arrays of four lights in \\hich various comlhations of lights lvere illuminated. These prolhls consisted of four lights ver! SLlS on one side versus a bottom light on the otl her non le (4 vs 0), a top light (2 vs 37 (1 77s l), two lights in a vertical line versus two lights horizontally
lesil our firs the
272
LEVEY,
HARRIS
AND
JANE
% CORRECT 100 . 90
/J
80
:$z:::. . ....A . . .:5. ..y$.
/
60
10 t
...>.:: .*,:.:n ‘.2*.:.:.&
STIMULI
:::: +-
OL’ SESSIONS 1
.000 00 0. + -
w-w
FIG. 2. Postoperative performance stimulus arrays. The dorsal aspect the upper right. There was complete geniculate nucleus.
l-13 days
.000 .o.. +-
.O 0. 0..0 +-
I-b days
1-12 days
of animal G5 on pattern problems with four-light of the cortical lesion is schematically represented in bilateral retrograde degeneration of the dorsal lateral
and diagonal lines (slant). In the same apparatus it was also possible to project patterns such as squares and circles of various sizes and to enclose these figures within an annulus. The problems are illustrated at the bottom of Fig. 4. One hundred to 150 trials were run daily. Reinforcement, stimulus programming, recording, and performance criteria were as previously reported (5). Following completion of the experiments the animals were perfused, the brains removed and imbedded in egg yolk (3) and sectioned at 33 pm for Nissl preparations. RESITLTS In every instance there was complete retrograde degeneration of the lateral geniculate nucleus. This alone did not result in an inability to perform any of the light problems or the simple projected pattern problems. Three animals are represented in this group, GS, G6, and GlO (Figs. 2-4).
PATTERK
DISCRIMINATION
273
Animal G6 performed all the discriminations quite readily except for the last one in which an annulus enclosed the figure. This is quite similar to the findings of Snyder and Diamond (7) in \\-hich tree shrews with bilateral ablations of striate cortex were easily able to solve a triangle orientation problem, but were unable to do so when the triangles were encircled. The other two animals, G8 and G9, had extremely large lesions which not only caused complete degeneration of the lateral geniculate, but virtually complete degeneration in the pulvinar. A few remaining cells lvere found in the pulvinar, and these animals’ lateral nuclear complex was for the most part destroyed. These tlvo animals were able to learn the 4 vs 0 and the 1 vs 1 problems (Figs. 5 and 6), but were unable to learn the diagonal problem, the problem where a cue such as local flux changes would be most difficult to use.
80
60 50
----------------------------
40 30 20
PROBLEM _ ClvsSTIMULI
IO
-
p-
0 SESSIONS
l-4 days
l-11 doyr
l-11 days
FIG. 3. Performance of animal GlO on a series of projected figure problems. The positive stimulus remained the same in the first two problems, and the negative stimulus was constant in the second and third problems, Cl vs -: clear illuminated screen vs dark screen, Cl vs SC: clear screen vs small circle, SSQ vs SC: small square vs small circle. In the SSQ vs SC problem, the stimuli were equated for luminous flux.
274
LEVEY,
HARRIS
AND
JANE
% CORRECT 100 90
.
80 JO
60
50
I
----------I-----
1
PROBLEM 4vrO
lvsl
_------------
/&--
-----
---------------
-__.
r
20
c
SIanI
CIVS.
CMX
ssovrx
SS’hSC/lBC
COMMON
FIG. 4. Record of animal G6 on a problem series of light and projected figure patterns. There was complete retrograde degeneration of the dorsal lateral geniculate bilaterally. All problems were easily solved except the last, in which the stimuli in the previous problem were surrounded by a darkened annulus with an illuminated border. Performance on this problem was at chance after 38 days.
DISCUSSION The findings shown above are quite consistent with previous observathat ablation of the visual cortex in tree shrews does not result in an inability to solve pattern discrimination problems. Some difficulty can arise in interpretation of the results in our experimental situation, since the animals were allowed to approach the pattern and could presumably discover areas of differing local flux by scanning eye movements. It might be argued that this sort of scanning is a simplification of the normal means by which areas of local flux are transformed into a pattern. We have not performed experiments in which the animals were forced to make decisions at a distance from the target such as was done in Ward and Masterton’s (9) study to minimize the animals’ utilization of scanning to detect areas of flux change. Obviously some sort of visual processing is going on in the cortex and the deficits demonstrated in animal G6 on concealed figures may be indicative of such processing. In both the tree shrew and ground tions
PATTERN
275
DISCRIMINATION
RECT
--
--_-----------___ -------------___ I”--------h+hbv@f f+-bfo
FIG. 5. Postoperative record of animal G9 with a very large lesion resulting in extensive retrograde degeneration of the dorsal lateral geniculate, lateral, and lateroposterior nuclei.
% CORRECT 100
r
30 20 t
PROBLEM 4r.O
.00. 0..0 +
SESSIONS I.4
days
FIG. 6. Performance of animal retrograde changes in the dorsal nuclear complex.
l-10 days
-
-
1.21 days
G8 with an extensive lesion resulting in widespread lateral geniculate, lateroposteroir nucleus and lateral
276
LEVEY,
HARRIS
AND
JANE
squirrel, an intact geniculostriate system is apparently necessary for the solution of problems involving the discrimination of stimulus arrays with identical external dimensions, lvhich may be learned only by the abstraction and differentiation of pertinent features \vitllin the arrays. A comparison can be made \vith the tree shrew in that the ground squirrel’s tectum is comparable to the tree shrew’s in volume and input from the retina (1, 8) but its cortex and lateral geniculate nucleus do not show the same degree of laminar differentiation. This might lead one to suspect that the tectum of the ground squirrel plays an even more important role in visual function than the same structure in the tree shrew. REFERENCES 1. CAMPBELL, C. B. G., J. A. JANE, and D. YASHON. 1967. The retinal projections of the tree shrew and hedgehog. Brain Res. 5: 406418. 2. CASAGRANDE, V. A., J. K. HARTING, W. C. HALL, I. T. DIAMOND, and G. F. MARTIN. 1972. Superior colliculus of the tree shrew: A structural and functional subdivision into superficial and deep layers. Science 177: 444447. 3. EBBESSON, S. 0. E. 1970. The selective silver impregnation of degenerating axons, pp. 132-166. In “Contemporary Research Methods in Neuroanatomy.” W. J. H. Nauta and S. 0. E. Ebbesson [Ed.], Springer Verlag, New York. 4. JANE, J. A., N. J. CARSLON, and N. LWEY. 1969 A comparison of the effects of lesions of striate cortex and superior colliculus on vision in the Malayan tree shrew (Tupaia glis). Anal. Rec. 163: 306-307. 5. JANE, J. A., N. LEVEY, and N. J. CARLSON. 1972. Tectal and cortical function in vision. Exp. Neural. 3.5: 61-77. 6. LEVEY, N., J. HARRIS, W. R. WINN, and J. A. JANE. 1971. Anatomical and behavioral study of the visual system of the ground squirrel. Amt. Rec. 169: 367-368. 7. SNYDER, M., and I. T. DIAYOND. 1968. The organization and function of the visual cortex in the tree shrew. Brain. Behav. Evol. 1: 244-288. 8. TIGGES, J. 1970. Retinal projections to subcortical optic nuclei in diurnal and nocturnal squirrels. Brain. Behau. Evol. 3: 121-134. 9. WARD, J. P., and B. MASTERTON. 1970. Encephalization and visual cortex in the tree shrew (Tupaia glis). Brain. Behav. Evol. 3: 421469.
NEUROLOGY
Effects
%,270-276
(1973)
of Visual Cortical Ablation on Pattern Discrimination the Ground Squirrel (Cite//us tridecemlineotus) N. H. LEVEY, J. HARRIS, Department
AND J. A. JANE’
of Neurological Surgery, University of Virginia Charlottesville, Virginia 22901 Received
October
in
Hospital,
25, 1972
Five ground squirrels (Citellus tridecemlineatus) were trained on various visual discrimination problems following large bilateral cortical ablations. With lesions resulting only in complete retrograde loss of latera geniculate, discriminations other than those based upon total luminous flux were made easily. With lesions large enough to result in extensive retrograde degeneration of the pulvinar, a more profound deficit resulted, but not one in which complete loss of pattern vision occurred. The ground squirrel, like the tree shrew, is thus able to solve visual discrimination tasks in the absence of striate cortex.
INTRODUCTION While considerable controversy exists over the exact nature of the visual deficit following visual cortical ablation, it seems fairly well established that this lesion performed in the Malayan tree shrew results in a deficit which is qualifiably different than is a similar lesion, for instance, in the rhesus monkey (5, 7). Snyder and Diamond (7) suggested that this difference might be due to the large tectum possessedby the tree shrew; this suggestion implies that a second visual pathway involving tectum, pulvinar, and peristriate cortex might well mediate pattern vision. Studies on ablation in the tectum of the tree shrew have been consistent with this view (2, 4). In order to elaborate this hypothesis further it was thought that another species which possessesa large tectum but whose geniculostriate system differed somewhat from the tree shrew, would serve as an interesting comparison. The ground squirrel (Citellus tridecemlineatus) appeared to fulfill these criteria and indeed ablation of the visual cortex did not result in loss of pattern vision (6). 1 Supported
by
EYOO1.51-OlAl
the
Lucille
from National
Sargeant
Sebrell
Eye Institute. 270
Copyrinht All rights
9
1973 by Academic Res, reproduction in any form
Inc. reserved.
Fund
for
Brain
Research
and
1 ROl
PATTERN
FIG.
1. Typical
large
bilateral
271
DISCRIMINATION
aspiration
lesion,
animal
G6. Note
the large
optic
tectl um.
R’IETHODS s Gx
ground squirrels were subjected to large Materal cortical aspirat: ion ons (Fig. 1) and then trained in a two-choice apparatus described in previous cotntnuniration (.5). TU.O types of prol)lems \\-ere used. 7 ‘lie t involved two arrays of four lights in \\hich various comlhations of lights lvere illuminated. These prolhls consisted of four lights ver! SLlS on one side versus a bottom light on the otl her non le (4 vs 0), a top light (2 vs 37 (1 77s l), two lights in a vertical line versus two lights horizontally
lesil our firs the
272
LEVEY,
HARRIS
AND
JANE
% CORRECT 100 . 90
/J
80
:$z:::. . ....A . . .:5. ..y$.
/
60
10 t
...>.:: .*,:.:n ‘.2*.:.:.&
STIMULI
:::: +-
OL’ SESSIONS 1
.000 00 0. + -
w-w
FIG. 2. Postoperative performance stimulus arrays. The dorsal aspect the upper right. There was complete geniculate nucleus.
l-13 days
.000 .o.. +-
.O 0. 0..0 +-
I-b days
1-12 days
of animal G5 on pattern problems with four-light of the cortical lesion is schematically represented in bilateral retrograde degeneration of the dorsal lateral
and diagonal lines (slant). In the same apparatus it was also possible to project patterns such as squares and circles of various sizes and to enclose these figures within an annulus. The problems are illustrated at the bottom of Fig. 4. One hundred to 150 trials were run daily. Reinforcement, stimulus programming, recording, and performance criteria were as previously reported (5). Following completion of the experiments the animals were perfused, the brains removed and imbedded in egg yolk (3) and sectioned at 33 pm for Nissl preparations. RESITLTS In every instance there was complete retrograde degeneration of the lateral geniculate nucleus. This alone did not result in an inability to perform any of the light problems or the simple projected pattern problems. Three animals are represented in this group, GS, G6, and GlO (Figs. 2-4).
PATTERK
DISCRIMINATION
273
Animal G6 performed all the discriminations quite readily except for the last one in which an annulus enclosed the figure. This is quite similar to the findings of Snyder and Diamond (7) in \\-hich tree shrews with bilateral ablations of striate cortex were easily able to solve a triangle orientation problem, but were unable to do so when the triangles were encircled. The other two animals, G8 and G9, had extremely large lesions which not only caused complete degeneration of the lateral geniculate, but virtually complete degeneration in the pulvinar. A few remaining cells lvere found in the pulvinar, and these animals’ lateral nuclear complex was for the most part destroyed. These tlvo animals were able to learn the 4 vs 0 and the 1 vs 1 problems (Figs. 5 and 6), but were unable to learn the diagonal problem, the problem where a cue such as local flux changes would be most difficult to use.
80
60 50
----------------------------
40 30 20
PROBLEM _ ClvsSTIMULI
IO
-
p-
0 SESSIONS
l-4 days
l-11 doyr
l-11 days
FIG. 3. Performance of animal GlO on a series of projected figure problems. The positive stimulus remained the same in the first two problems, and the negative stimulus was constant in the second and third problems, Cl vs -: clear illuminated screen vs dark screen, Cl vs SC: clear screen vs small circle, SSQ vs SC: small square vs small circle. In the SSQ vs SC problem, the stimuli were equated for luminous flux.
274
LEVEY,
HARRIS
AND
JANE
% CORRECT 100 90
.
80 JO
60
50
I
----------I-----
1
PROBLEM 4vrO
lvsl
_------------
/&--
-----
---------------
-__.
r
20
c
SIanI
CIVS.
CMX
ssovrx
SS’hSC/lBC
COMMON
FIG. 4. Record of animal G6 on a problem series of light and projected figure patterns. There was complete retrograde degeneration of the dorsal lateral geniculate bilaterally. All problems were easily solved except the last, in which the stimuli in the previous problem were surrounded by a darkened annulus with an illuminated border. Performance on this problem was at chance after 38 days.
DISCUSSION The findings shown above are quite consistent with previous observathat ablation of the visual cortex in tree shrews does not result in an inability to solve pattern discrimination problems. Some difficulty can arise in interpretation of the results in our experimental situation, since the animals were allowed to approach the pattern and could presumably discover areas of differing local flux by scanning eye movements. It might be argued that this sort of scanning is a simplification of the normal means by which areas of local flux are transformed into a pattern. We have not performed experiments in which the animals were forced to make decisions at a distance from the target such as was done in Ward and Masterton’s (9) study to minimize the animals’ utilization of scanning to detect areas of flux change. Obviously some sort of visual processing is going on in the cortex and the deficits demonstrated in animal G6 on concealed figures may be indicative of such processing. In both the tree shrew and ground tions
PATTERN
275
DISCRIMINATION
RECT
--
--_-----------___ -------------___ I”--------h+hbv@f f+-bfo
FIG. 5. Postoperative record of animal G9 with a very large lesion resulting in extensive retrograde degeneration of the dorsal lateral geniculate, lateral, and lateroposterior nuclei.
% CORRECT 100
r
30 20 t
PROBLEM 4r.O
.00. 0..0 +
SESSIONS I.4
days
FIG. 6. Performance of animal retrograde changes in the dorsal nuclear complex.
l-10 days
-
-
1.21 days
G8 with an extensive lesion resulting in widespread lateral geniculate, lateroposteroir nucleus and lateral
276
LEVEY,
HARRIS
AND
JANE
squirrel, an intact geniculostriate system is apparently necessary for the solution of problems involving the discrimination of stimulus arrays with identical external dimensions, lvhich may be learned only by the abstraction and differentiation of pertinent features \vitllin the arrays. A comparison can be made \vith the tree shrew in that the ground squirrel’s tectum is comparable to the tree shrew’s in volume and input from the retina (1, 8) but its cortex and lateral geniculate nucleus do not show the same degree of laminar differentiation. This might lead one to suspect that the tectum of the ground squirrel plays an even more important role in visual function than the same structure in the tree shrew. REFERENCES 1. CAMPBELL, C. B. G., J. A. JANE, and D. YASHON. 1967. The retinal projections of the tree shrew and hedgehog. Brain Res. 5: 406418. 2. CASAGRANDE, V. A., J. K. HARTING, W. C. HALL, I. T. DIAMOND, and G. F. MARTIN. 1972. Superior colliculus of the tree shrew: A structural and functional subdivision into superficial and deep layers. Science 177: 444447. 3. EBBESSON, S. 0. E. 1970. The selective silver impregnation of degenerating axons, pp. 132-166. In “Contemporary Research Methods in Neuroanatomy.” W. J. H. Nauta and S. 0. E. Ebbesson [Ed.], Springer Verlag, New York. 4. JANE, J. A., N. J. CARSLON, and N. LWEY. 1969 A comparison of the effects of lesions of striate cortex and superior colliculus on vision in the Malayan tree shrew (Tupaia glis). Anal. Rec. 163: 306-307. 5. JANE, J. A., N. LEVEY, and N. J. CARLSON. 1972. Tectal and cortical function in vision. Exp. Neural. 3.5: 61-77. 6. LEVEY, N., J. HARRIS, W. R. WINN, and J. A. JANE. 1971. Anatomical and behavioral study of the visual system of the ground squirrel. Amt. Rec. 169: 367-368. 7. SNYDER, M., and I. T. DIAYOND. 1968. The organization and function of the visual cortex in the tree shrew. Brain. Behav. Evol. 1: 244-288. 8. TIGGES, J. 1970. Retinal projections to subcortical optic nuclei in diurnal and nocturnal squirrels. Brain. Behau. Evol. 3: 121-134. 9. WARD, J. P., and B. MASTERTON. 1970. Encephalization and visual cortex in the tree shrew (Tupaia glis). Brain. Behav. Evol. 3: 421469.