Exp. Brain Res. 25, 131-137 (1976)
Experimental Brain Research 9 by Springer-Verl~g 1976
Early Versus Late Visual Cortex Lesions: Effects on Receptive Fields in Cat Superior Colliculus* N. B e r m a n a Department of Anatomy and Neurobiology, Washington University School of Medicine, Saint Louis, Missouri 63110 (USA) M. Cynader Department of Psychology,Dalhousie University, Halifax, Nova Scotia B3H 4J2 (Canada)
Summary. Cats that sustain lesions of the visual cortex early in life appear to p e r f o r m certain visual discrimination tasks better than those operated as adults. This study sought to determine whether this recovery of visual capacities was accompanied by reorganization of single cell responses at the level of the superior colliculus. Areas 17 and 18 were ablated in adult cats and in kittens at various times during the neonatal period. Responses of units in superior colliculus ipsilateral to the lesion were recorded following a prolonged recovery period. Following cortical lesions, collicular units rarely exhibited direction selectivity, binocularity was reduced in the majority of animals, and the ocular dominance distribution was biased toward the contralateral eye. The reduction of direction selectivity and binocularity were unrelated to the animal's age at operation. Key words: Early lesions - Superior colliculus - Visual System - Receptive fields.
Introduction Clinical observations have frequently suggested that patients who sustain cortical injury at an early age are less severely impaired than those who suffer similar injury as adults (Kennard, 1940; see also Teuber, 1966, 1970). Several investigators have demonstrated that cats that sustain lesions of the visual cortex at an early age are superior to cats that sustain similar lesions as adults in discrimination of flicker (Tucker et al., 1968) and in pattern discrimination * This research was supported by M.R.C. Grant No. MA 5201 and NRC Grant No. A9939 (to M.C.) and Grants from NIH (postdoctoral fellowshop to N.B.). 1 Present address: Department of Physiologyand Biochemistry, Medical College of Pennsylvania, Philadelphia, Pa. 19129 (USA).
132
N. Berman and M. Cynader
(Wetzel et al., 1965; for further ref. see Doty, 1973). It has also been shown that in several situations anatomical reorganization occurs more readily following early lesions than after later lesions (Lund and Lund, 1973; Schneider, 1970; Guillery, 1972; Kalil, 1972). This study sought to determine whether early lesions result in changes at the single unit level which could be correlated with these behavioral and anatomical changes. In the normal cat, the superior colliculus receives major projections from contralateral retina and from areas 17 and 18 of ipsilateral cortex, and projects to other areas of the cortex with known visual functions (area 19 and the ClareBishop area) via posterior thalamic nuclei (Graybiel, 1972). In normal adult cats most units in superior coUiculus are binocularly driven and about two-thirds are direction selective (Straschill and Hoffmann, 1969; sterling and Wickelgren, 1969; Berman and Cynader, 1972). Following ablation of ipsilateral areas 17 and 18 most units are driven more strongly by the contralateral eye and direction selectivity is virtually absent (Wickelgren and Sterling, 1969; Rosenquist and Palmer, 1971; Berman and Cynader, 1972). A property not shown by collicular units in the intact animal, inhibition by diffuse flashes in the visual background, is observed following the lesion (Berman and Cynader, 1975). If reorganization at the collicular level plays a part in recovery of visual function, recovery from cortical lesions may be associated with normalization of the receptive-field properties of collicular units. An increase in binocularity and in direction selectivity, as well as a decrease in inhibition by background flicker would be expected.
Methods Operates Unilateral ablation of visual cortex including all of areas 17 and 18 was carried out under aseptic conditions by subpial aspiration. Surgery was performed on kittens at ages 1, 4, 6, 10, 14 and 120 days, and on adult cats. Kittens were anesthetized with methoxyflurane (Metofane, Pitman-Moore), adults with intravenous Nembutal with 4 gin. Mannitol in 20 cc water i.v. to prevent edema. With the exception of the animal operated at 120 days, all of the kittens were permitted 6-10 months of exposure in a normal visual environment after surgery and prior to electrophysiological study. The adult operates comprised two groups: 8 animals were permitted 1-15 days postoperative exposure in a normal environment prior to recording (Short postoperative group) and 3 cats were exposed for 6-10 months postoperatively in a normal environment prior to recording (Long postoperative group). Thus, one group of adult operates was permitted as long a period of exposure following surgery and before single unit recording as the group of kittens operated during the neonatal period.
Single Unit Recording The cat was anesthetized initially with intravenous sodium pentothal, then intubated by mouth and paralyzed with Flaxedil. Pentothal was discontinued and the animal respirated with a mixture of 70 % nitrous oxide and 30 % oxygen. Glass-coated platinum-iridium microelectrodes were used to record single units extracellularly in the superficial layerS of the superior colliculus ipsilateral to the lesion. Sterile conditions were maintained and at the end of each recording session the animal was permitted to recover from paralysis and returned to its home cage. In this way recordings could be taken more than once from the same cat. After the final session the operated cats were reauesthetized with Nembutal and peffused through the heart with saline followed by 10 % formalin. Celloidon-embeddedsec-
Early VS. Late Lesions
133
tions were cut at 30 ~ and stained with cresylviolet. The lesions were reconstructed using cytoarchitectonic criteria for cortical areas and retrograde changes in the lateral geniculate nucleus. Data from animals found to have incomplete lesions were eliminated from the results. Further details of the procedures used in preparing the animals, presenting stimuli, recording single unit responses and reconstructing lesions along with the criteria used for assessing receptive-field properties are presented in Cynader and Berman (1972), and Berman and Cynader (1972). We concentrated on determining the ocular dominance, preferred direction, and extent of inhibition by background flicker for the collicular units, but all three properties were not determined for every unit.
Results
Reconstruction of Lesions After unilateral early lesions of areas 17 and 18 the cortical gyral pattern was abnormal an the lesion side; in most cases the suprasylvian gyrus was enlarged and in all cases the lateral geniculate nucleus showed severe retrograde changes.
Receptive-Field Properties Figure 1 shows the ocular dominance distribution of collicular units in the early lesion group, adult lesion long survival group, adult lesion short survival group, and normal adult controls ( B e r m a n and Cynader, unpublished observations). R e gardless of the age at which the lesion was sustained or the interval between surgery and recording, the ocular dominance distribution of the operates shows a reduction in the n u m b e r of units equally responsive to input to both eyes (category 4) and a trend toward increased responsiveness to input via the contralateral eye. The decrement in the per cent of units equally responsive to input to both eyes appears m o r e p r o n o u n c e d in the adult lesion animals recorded within 15 days of surgery than in both groups of cats recorded 6 - 1 0 months after surgery, but the differences a m o n g groups of operates fail to reach statistical significance (Kolmogorov-Smirnoff test, two-tailed). Table 1 presents the ocular dominance distributions and percent of direction selctive units for all the operated animals. All operated animals show a loss of direction selectivity when c o m p a r e d with the intact animal. This decrement is greater in the adult operates recorded within 15 days of operation than-in the animals recorded 6 - 1 0 months after surgery (Chi-square test, p < 0.01). The age at which the lesion was sustained does not appear to influence the per cent of direction selective units. In all three groups of operates, about 80 % of collieular units were strongly inhibited by background flicker, as previously reported following lesions of ipsilateral cortical areas 17 and 18 ( B e r m a n and Cynader, 1975). Figure 2 summarizes the results in the operated group by showing the average ocular dominance (top) and per cent of direction selectivity (bottom) in collicular cells versus the animal's age when the cortical lesion was made. The average ocular dominance of the units did not change systematically with the animal's age at the time of the lesion and was lower in all cases than that of the intact adult.
134
N. Berman and M. Cynader
1009080" ~ 7 0 Early Lesion
100902 80~
.~ 6o,
6o "5 5O "E 415 8 30. 79
u~
Adult Lesion Long Survival
50'
~
82
2o. 10-
4oJ
32
30 215 10
234567
234567 contralateral equal ipsilateral
contralateral equal ipsilateral
I00, 90. 80.
100 9080. N70. Normally Reared ~6O. Intact Adult 93 50. 40~30. 0-20. 10-
70" Adult Lesion ~ 60- Short Survival
50.
~4o30-
~2o- ?8 34 2838 10234567
1 2 3 4 5 6 7
contralateral equal ipsilateral
,,wcontralateral equal ipsiJateral ID-
Fig. 1. Ocular dominance distributions of units recorded in the superior colliculus of the four groups of cats. The categories correspond to those defined by Hubel and Wiesel (1962). The groups 1-7 represent a contralateral to ipsilateral trend in ocular dominance with units in group 1 driven only by the contralateral eye, units in group 4 driven equally by both eyes and units in group 7 driven only by the ipsilateral eye. The numbers at the top of each bar represent the number of units in that group
Table 1
Group
Normal Adults Intact Light-Reared Adults Adults Short Post-Op Adults Long Post-Op Neonates, Age: 1 day 4 days 6 days 10 days 14 days Total neonates 120 days
Ocular Dominance Distribution 1 2 3 4 5
6
7
Direction Selectivity No. Units % of total Yes No
11 38 23
17 34 12
37 28 15
93 38 32
18 10 6
6 8 3
7 7 8
154 10 16
84 243 108
65 4 13
9 9 7 8 46 79 5
2 10 5 8 12 37 5
5 7 5 2 11 30 3
18 15 16 12 21 82 2
7 1 3 6 5 22 5
3 0 1 2 1 7 4
3 0 1 5 6 15 1
0 5 8 12 16 45 2
53 45 35 30 99 272 27
0 10 19 28 14 14 7
Early VS. Late Lesions
135
*adult
intact
c-
9
short survival
o 1-
4'
~
10'
1~
/"11o /~ul
t
Age at lesion (days) .~
100-
_~9o$18o}7o-
adult 9 infect
u 60"0 5040-
10" 9 1
4
6
10
14
120
adult short survival
adult
Age at lesion (days) Fig. 2. (Top) The average ocular dominance of collicular units versus the age at which the visual cortex was removed. T h e values for n o r m a l adult cats and adult cats which were allowed to survive 15 clays or less after the lesion are shown for comparison on the right side of the figure. A n average ocular dominance of 4 would m e a n that the two eyes had equalinfluence on collicular units, and any average lower than 4 would m e a n that the contralateral eye was m o r e effective in driving collicular units than the ipsilateral eye. (Bottom) T h e percent of direction selective collicular units versus the age at which the visual cortex was removed. T h e values for normal adult cats and the adult short survival group are shown for comparison on the right side of the figure
There is considerable variability in the per cent of direction selective units after the early lesions, but most animals, including the long survival adults, showed a slightly higher per cent of direction selective collicular units than the short survival adults. The positions of the areae centrales on the tangent screen in the operated animals were not different from those found in normal animals; indicating that neither early nor late lesions produce a strong divergence or convergence. Discussion
Several studies have shown that kittens show substantially more recovery of visual discriminations (Wetzel et al., 1965; Doty, 1961; Tucker et al., 1968) following
136
N. Berman and M. Cynader
visual cortex lesions than do adult cats sustaining similar lesions. The superior colliculus, which provides a pathway from retina to cortical areas such as the ClareBishop area, might be expected to participate in any functional reorganization following the early lesions which underlies the increased recovery. Our data indicate, however, that the receptive-field properties of single neurons in the superficial layers of the superior colliculus of cats sustaining visual cortex lesions neonatally are not different from those of cats which sustained the lesions as adults and were allowed similar survival times. In both cases, reduced direction selectivity and binocularity were observed following the lesion and the inhibitory effects of flickering the visual background increased. One possible explanation for our failure to find special changes in collicular receptive field properties following early or late cortical lesions is that the physiologic reorganization which underlies behavioral recovery of function occurs in other brain structures. The pretectum and ventral lateral geniculate nucleus both receive extensive retinal inputs (Laties and Sprague, 1966) and it is possible that receptive-field properties in these structures have been altered following early lesions. It is further possible that reorganization has taken place at later points in the pathway from colliculus to posterior thalamus to suprasylvian cortex. Further experiments comparing the consequences of visual cortex lesions in adulthood vs. infancy on the responses of neurons in the other visual structures noted above would be most welcome. An alternative possibility is that the behavioral studies which led us to look for these physiologic changes were based on incomplete early lesions. It is possible, for example, that a small zone of area 17 or 18 remaining following an early lesion is able to mediate the behavioral recovery. Doty (1971) re-examined his earlier data on kittens and found that the animals which had pattern vision despite removal of area 17 also had significant sparing of areas 18 or 19. He concluded that "comparison of the effects of removing striate cortex in adult versus neonatal cats does not now encourage the belief that any extensive neural reorganization accrues to the advantage of the neonatal subject." This conclusion is supported by our data. It may be that recovery after neonatal visual cortex lesions is more extensive than the recovery following lesions in adults only in animals in which the retinotectal projection is not complete at birth, such as the hamster (Schneider, 1970).
Comparison with Other Studies Stein and Magalhfies-Castro (1975) studied superior collicular units in cats which had sustained incomplete lesions of area 17 at 2.5 to 35 days of age and allowed 2-4 months recovery. They report reduction in direction selectivity and in binocularity following these lesions. Although their lesions were smaller than ours and survival times shorter, their results are similar to the present results.
Acknowledgements. We wouldliketo thankIngoWinzerfor preparing the histologicalmaterial.
Early VS. Late Lesions
137
References Berman, N., Cynader, M.: Comparison of receptive-field organization in the superior colliculus of Siamese and normal cats. J. Physiol. (Lond.) 224, 363-389 (1972) Berman, N., Cynader, M.: Receptive fields in cat superior colliculus after visual cortex lesions. J. Physiol. (Lond.) 245, 261-270 (1975) Cynader, M., Berman, N.: Receptive-field organization of the monkey superior colliculus. J. Neurophysiol. 35, 187-201 (1972) Doty, R. W.: Ablation of visual areas in the central nervous system. In: Handbook of Sensory Physiology, Vol. VII/3. pp. 483-541. Berlin-Heidelberg-New York: Springer 1973 Doty, R.W.: Functional significance of the topographical aspects of the retinocortical projection. In: The Visual System: Neurophysiology and Psycbophysics. (Ed.R. Jung and H. Kornhuber), pp. 228-245. Berlin-Heidelberg-New York: Springer 1961 Doty, R.W.: Survival of pattern vision after removal of striate cortex in the adult cat. J. comp. Neurol. 143, 341-370 (1971) Graybiel, A.M.: Some extrageniculate visual pathways in the cat. Invest. Ophthal. 5, 322-332 (1972) Guillery, R.W.: Experiments to determine whether retinogeniculate axons can form translaminar collateral sprouts in the dorsal lateral geniculate nucleus of the cat. J. comp. Neurol. 146, 407-420 (1972) Hubel, D.H., Wiesel, T.N.: Receptive fields, binocular interaction and functional architecture in the cat's striate cortex. J. Physiol. (Lond.) 168, 106-154 (1962) Kalil, R.E.: Formation of new retino-geniculate connections in kittens: effects of age and visual experience. Anat. Rec. 175, 353 (1972) Kennard, M.A.: Relation of age to motor impairment in man and in subhuman primates. Arch. Neurol. Psychiat. (Chic.) 44, 377-397 (1940) Laties, A.M., Sprague, J.M.: The projection of optic fibers to the visual centers in the cat. J. comp. Neurol. 91, 369-408 (1966) Lund, R.D., Lurid, J.S.: Reordered growth patterns of the rat's retinotectal pathway after neonatal retinal lesions. Anat. Rec. 175, 376 (Abstract) (1973) Rosenquist, A.C., Palmer, L.: Visual receptive field properties of cells in the superior colliculus after cortical lesions in the cat. Exp. Neurol. 33, 629-652 (1971) Schneider, G.E.: Mechanisms of functional recovery following lesions of visual cortex or superior colliculus in neonate and adult hamsters. Brain Behav. Evol. 3, 295-323 (1970) Stein, B. E., Magalhfies-Castro, B.: Effects of neonatal cortical lesions upon the cat superior colliculus. Brain Res. 83, 480-485 (1975) Sterling, P., Wickelgren, B.G.: Visual receptive fields in the superior colliculus of the cat. J. Neurophysiol. 32, 1-15 (1969) Sterling, P., Wickelgren, B.G.: Function of the projection from the visual cortex to the superior colliculus. Brain Behav. Evol. 3, 210-218 (1970) Straschill, M., Hoffmann, K.P.: Functional aspects of localization in the cat's tectum opticum. Brain Res. 13, 274-283 (1969) Teuber, H.L.: Alterations of perception after brain injury. In: Brain and Conscious Experience. (Ed. John C. Eccles), pp. 182-216. Berlin-Heidelberg-New York: Springer 1966 Teuber, H.L.: Mental retardation after early trauma to the brain: some issues in search of facts. In: Physical Trauma as an Etiological Agent in Mental Retardation. (Ed. C.R. Angle and E.A. Bering, Jr.), pp. 7-28. Bethesda, Md.: National Institutes of Health 1970 Tucker, T.J., Kling, A., Sharlock, D.P.: Sparing of photic frequency and brightness discriminations after striatectomy in neonatal cats. J. Neurophysiol. 31, 818-832 (1968) Wetzel, A.B., Thompson, V.E., Horel, J.A., Meyer, P.M.: Some consequences of perinatal lesions of the visual cortex in the cat. Psychon. Sci. 3, 381-382 (1965) Wickelgren, B.G., Sterling, P.: Influence of visual cortex on receptive fields in the superior colliculus of the cat. J. Neurophysiol. 32, 16-23 (1969)
Received August 25, 1975
Experimental Brain Research 9 by Springer-Verl~g 1976
Early Versus Late Visual Cortex Lesions: Effects on Receptive Fields in Cat Superior Colliculus* N. B e r m a n a Department of Anatomy and Neurobiology, Washington University School of Medicine, Saint Louis, Missouri 63110 (USA) M. Cynader Department of Psychology,Dalhousie University, Halifax, Nova Scotia B3H 4J2 (Canada)
Summary. Cats that sustain lesions of the visual cortex early in life appear to p e r f o r m certain visual discrimination tasks better than those operated as adults. This study sought to determine whether this recovery of visual capacities was accompanied by reorganization of single cell responses at the level of the superior colliculus. Areas 17 and 18 were ablated in adult cats and in kittens at various times during the neonatal period. Responses of units in superior colliculus ipsilateral to the lesion were recorded following a prolonged recovery period. Following cortical lesions, collicular units rarely exhibited direction selectivity, binocularity was reduced in the majority of animals, and the ocular dominance distribution was biased toward the contralateral eye. The reduction of direction selectivity and binocularity were unrelated to the animal's age at operation. Key words: Early lesions - Superior colliculus - Visual System - Receptive fields.
Introduction Clinical observations have frequently suggested that patients who sustain cortical injury at an early age are less severely impaired than those who suffer similar injury as adults (Kennard, 1940; see also Teuber, 1966, 1970). Several investigators have demonstrated that cats that sustain lesions of the visual cortex at an early age are superior to cats that sustain similar lesions as adults in discrimination of flicker (Tucker et al., 1968) and in pattern discrimination * This research was supported by M.R.C. Grant No. MA 5201 and NRC Grant No. A9939 (to M.C.) and Grants from NIH (postdoctoral fellowshop to N.B.). 1 Present address: Department of Physiologyand Biochemistry, Medical College of Pennsylvania, Philadelphia, Pa. 19129 (USA).
132
N. Berman and M. Cynader
(Wetzel et al., 1965; for further ref. see Doty, 1973). It has also been shown that in several situations anatomical reorganization occurs more readily following early lesions than after later lesions (Lund and Lund, 1973; Schneider, 1970; Guillery, 1972; Kalil, 1972). This study sought to determine whether early lesions result in changes at the single unit level which could be correlated with these behavioral and anatomical changes. In the normal cat, the superior colliculus receives major projections from contralateral retina and from areas 17 and 18 of ipsilateral cortex, and projects to other areas of the cortex with known visual functions (area 19 and the ClareBishop area) via posterior thalamic nuclei (Graybiel, 1972). In normal adult cats most units in superior coUiculus are binocularly driven and about two-thirds are direction selective (Straschill and Hoffmann, 1969; sterling and Wickelgren, 1969; Berman and Cynader, 1972). Following ablation of ipsilateral areas 17 and 18 most units are driven more strongly by the contralateral eye and direction selectivity is virtually absent (Wickelgren and Sterling, 1969; Rosenquist and Palmer, 1971; Berman and Cynader, 1972). A property not shown by collicular units in the intact animal, inhibition by diffuse flashes in the visual background, is observed following the lesion (Berman and Cynader, 1975). If reorganization at the collicular level plays a part in recovery of visual function, recovery from cortical lesions may be associated with normalization of the receptive-field properties of collicular units. An increase in binocularity and in direction selectivity, as well as a decrease in inhibition by background flicker would be expected.
Methods Operates Unilateral ablation of visual cortex including all of areas 17 and 18 was carried out under aseptic conditions by subpial aspiration. Surgery was performed on kittens at ages 1, 4, 6, 10, 14 and 120 days, and on adult cats. Kittens were anesthetized with methoxyflurane (Metofane, Pitman-Moore), adults with intravenous Nembutal with 4 gin. Mannitol in 20 cc water i.v. to prevent edema. With the exception of the animal operated at 120 days, all of the kittens were permitted 6-10 months of exposure in a normal visual environment after surgery and prior to electrophysiological study. The adult operates comprised two groups: 8 animals were permitted 1-15 days postoperative exposure in a normal environment prior to recording (Short postoperative group) and 3 cats were exposed for 6-10 months postoperatively in a normal environment prior to recording (Long postoperative group). Thus, one group of adult operates was permitted as long a period of exposure following surgery and before single unit recording as the group of kittens operated during the neonatal period.
Single Unit Recording The cat was anesthetized initially with intravenous sodium pentothal, then intubated by mouth and paralyzed with Flaxedil. Pentothal was discontinued and the animal respirated with a mixture of 70 % nitrous oxide and 30 % oxygen. Glass-coated platinum-iridium microelectrodes were used to record single units extracellularly in the superficial layerS of the superior colliculus ipsilateral to the lesion. Sterile conditions were maintained and at the end of each recording session the animal was permitted to recover from paralysis and returned to its home cage. In this way recordings could be taken more than once from the same cat. After the final session the operated cats were reauesthetized with Nembutal and peffused through the heart with saline followed by 10 % formalin. Celloidon-embeddedsec-
Early VS. Late Lesions
133
tions were cut at 30 ~ and stained with cresylviolet. The lesions were reconstructed using cytoarchitectonic criteria for cortical areas and retrograde changes in the lateral geniculate nucleus. Data from animals found to have incomplete lesions were eliminated from the results. Further details of the procedures used in preparing the animals, presenting stimuli, recording single unit responses and reconstructing lesions along with the criteria used for assessing receptive-field properties are presented in Cynader and Berman (1972), and Berman and Cynader (1972). We concentrated on determining the ocular dominance, preferred direction, and extent of inhibition by background flicker for the collicular units, but all three properties were not determined for every unit.
Results
Reconstruction of Lesions After unilateral early lesions of areas 17 and 18 the cortical gyral pattern was abnormal an the lesion side; in most cases the suprasylvian gyrus was enlarged and in all cases the lateral geniculate nucleus showed severe retrograde changes.
Receptive-Field Properties Figure 1 shows the ocular dominance distribution of collicular units in the early lesion group, adult lesion long survival group, adult lesion short survival group, and normal adult controls ( B e r m a n and Cynader, unpublished observations). R e gardless of the age at which the lesion was sustained or the interval between surgery and recording, the ocular dominance distribution of the operates shows a reduction in the n u m b e r of units equally responsive to input to both eyes (category 4) and a trend toward increased responsiveness to input via the contralateral eye. The decrement in the per cent of units equally responsive to input to both eyes appears m o r e p r o n o u n c e d in the adult lesion animals recorded within 15 days of surgery than in both groups of cats recorded 6 - 1 0 months after surgery, but the differences a m o n g groups of operates fail to reach statistical significance (Kolmogorov-Smirnoff test, two-tailed). Table 1 presents the ocular dominance distributions and percent of direction selctive units for all the operated animals. All operated animals show a loss of direction selectivity when c o m p a r e d with the intact animal. This decrement is greater in the adult operates recorded within 15 days of operation than-in the animals recorded 6 - 1 0 months after surgery (Chi-square test, p < 0.01). The age at which the lesion was sustained does not appear to influence the per cent of direction selective units. In all three groups of operates, about 80 % of collieular units were strongly inhibited by background flicker, as previously reported following lesions of ipsilateral cortical areas 17 and 18 ( B e r m a n and Cynader, 1975). Figure 2 summarizes the results in the operated group by showing the average ocular dominance (top) and per cent of direction selectivity (bottom) in collicular cells versus the animal's age when the cortical lesion was made. The average ocular dominance of the units did not change systematically with the animal's age at the time of the lesion and was lower in all cases than that of the intact adult.
134
N. Berman and M. Cynader
1009080" ~ 7 0 Early Lesion
100902 80~
.~ 6o,
6o "5 5O "E 415 8 30. 79
u~
Adult Lesion Long Survival
50'
~
82
2o. 10-
4oJ
32
30 215 10
234567
234567 contralateral equal ipsilateral
contralateral equal ipsilateral
I00, 90. 80.
100 9080. N70. Normally Reared ~6O. Intact Adult 93 50. 40~30. 0-20. 10-
70" Adult Lesion ~ 60- Short Survival
50.
~4o30-
~2o- ?8 34 2838 10234567
1 2 3 4 5 6 7
contralateral equal ipsilateral
,,wcontralateral equal ipsiJateral ID-
Fig. 1. Ocular dominance distributions of units recorded in the superior colliculus of the four groups of cats. The categories correspond to those defined by Hubel and Wiesel (1962). The groups 1-7 represent a contralateral to ipsilateral trend in ocular dominance with units in group 1 driven only by the contralateral eye, units in group 4 driven equally by both eyes and units in group 7 driven only by the ipsilateral eye. The numbers at the top of each bar represent the number of units in that group
Table 1
Group
Normal Adults Intact Light-Reared Adults Adults Short Post-Op Adults Long Post-Op Neonates, Age: 1 day 4 days 6 days 10 days 14 days Total neonates 120 days
Ocular Dominance Distribution 1 2 3 4 5
6
7
Direction Selectivity No. Units % of total Yes No
11 38 23
17 34 12
37 28 15
93 38 32
18 10 6
6 8 3
7 7 8
154 10 16
84 243 108
65 4 13
9 9 7 8 46 79 5
2 10 5 8 12 37 5
5 7 5 2 11 30 3
18 15 16 12 21 82 2
7 1 3 6 5 22 5
3 0 1 2 1 7 4
3 0 1 5 6 15 1
0 5 8 12 16 45 2
53 45 35 30 99 272 27
0 10 19 28 14 14 7
Early VS. Late Lesions
135
*adult
intact
c-
9
short survival
o 1-
4'
~
10'
1~
/"11o /~ul
t
Age at lesion (days) .~
100-
_~9o$18o}7o-
adult 9 infect
u 60"0 5040-
10" 9 1
4
6
10
14
120
adult short survival
adult
Age at lesion (days) Fig. 2. (Top) The average ocular dominance of collicular units versus the age at which the visual cortex was removed. T h e values for n o r m a l adult cats and adult cats which were allowed to survive 15 clays or less after the lesion are shown for comparison on the right side of the figure. A n average ocular dominance of 4 would m e a n that the two eyes had equalinfluence on collicular units, and any average lower than 4 would m e a n that the contralateral eye was m o r e effective in driving collicular units than the ipsilateral eye. (Bottom) T h e percent of direction selective collicular units versus the age at which the visual cortex was removed. T h e values for normal adult cats and the adult short survival group are shown for comparison on the right side of the figure
There is considerable variability in the per cent of direction selective units after the early lesions, but most animals, including the long survival adults, showed a slightly higher per cent of direction selective collicular units than the short survival adults. The positions of the areae centrales on the tangent screen in the operated animals were not different from those found in normal animals; indicating that neither early nor late lesions produce a strong divergence or convergence. Discussion
Several studies have shown that kittens show substantially more recovery of visual discriminations (Wetzel et al., 1965; Doty, 1961; Tucker et al., 1968) following
136
N. Berman and M. Cynader
visual cortex lesions than do adult cats sustaining similar lesions. The superior colliculus, which provides a pathway from retina to cortical areas such as the ClareBishop area, might be expected to participate in any functional reorganization following the early lesions which underlies the increased recovery. Our data indicate, however, that the receptive-field properties of single neurons in the superficial layers of the superior colliculus of cats sustaining visual cortex lesions neonatally are not different from those of cats which sustained the lesions as adults and were allowed similar survival times. In both cases, reduced direction selectivity and binocularity were observed following the lesion and the inhibitory effects of flickering the visual background increased. One possible explanation for our failure to find special changes in collicular receptive field properties following early or late cortical lesions is that the physiologic reorganization which underlies behavioral recovery of function occurs in other brain structures. The pretectum and ventral lateral geniculate nucleus both receive extensive retinal inputs (Laties and Sprague, 1966) and it is possible that receptive-field properties in these structures have been altered following early lesions. It is further possible that reorganization has taken place at later points in the pathway from colliculus to posterior thalamus to suprasylvian cortex. Further experiments comparing the consequences of visual cortex lesions in adulthood vs. infancy on the responses of neurons in the other visual structures noted above would be most welcome. An alternative possibility is that the behavioral studies which led us to look for these physiologic changes were based on incomplete early lesions. It is possible, for example, that a small zone of area 17 or 18 remaining following an early lesion is able to mediate the behavioral recovery. Doty (1971) re-examined his earlier data on kittens and found that the animals which had pattern vision despite removal of area 17 also had significant sparing of areas 18 or 19. He concluded that "comparison of the effects of removing striate cortex in adult versus neonatal cats does not now encourage the belief that any extensive neural reorganization accrues to the advantage of the neonatal subject." This conclusion is supported by our data. It may be that recovery after neonatal visual cortex lesions is more extensive than the recovery following lesions in adults only in animals in which the retinotectal projection is not complete at birth, such as the hamster (Schneider, 1970).
Comparison with Other Studies Stein and Magalhfies-Castro (1975) studied superior collicular units in cats which had sustained incomplete lesions of area 17 at 2.5 to 35 days of age and allowed 2-4 months recovery. They report reduction in direction selectivity and in binocularity following these lesions. Although their lesions were smaller than ours and survival times shorter, their results are similar to the present results.
Acknowledgements. We wouldliketo thankIngoWinzerfor preparing the histologicalmaterial.
Early VS. Late Lesions
137
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Received August 25, 1975
