480
Braht Research, 83 (1975) 480-485 © Elsevier ScientificPublishing Company, Amsterdam - Printed in The Netherlands
Effects of neonatal cortical lesions upon the cat superior colliculus
BARRY E. STEIN AND BRAULIO MAGALHAES-CASTRO Department of Anatomy, UCLA School of Medicine, Los Angeles, Calif. 90024 (U.S.A.)
(Accepted October 7th, 1974)
During development the brain displays plasticity in that the response properties of visual cortex neurons are determined by early visual experience 2,4,5,15, and the functional anomalies produced by cortical lesions can be partially compensated for during a critical stage of infancy18,28. While the adaptive significance of this capacity is obvious, little information is available about the long-term effects of early cortical lesions upon structures ordinarily dependent upon cortical projections for normal function (e.g., the cat superior colliculus). In all species studied, movement has been found to be the most effective stimulus for the activation of superior colliculus neurons, with response magnitude dependent upon such stimulus parameters as direction and velocity a'6,s'9,11,17,19,21,25,27. Two primary sources of visual input may contribute to these properties, one directly from retina and one via ipsilateral visual cortex x4. In some species, neuronal response selectivity may be unaffected by removal of visual cortex, and this may be related to the selective response properties present in their retinal ganglion cells9,12. In the cat, however, removal of area 17 of visual cortex nearly eliminates binocularity and directional selectivity, and decreases the effectiveness of moving stimuli16,3°. The neonatal cat superior colliculus resembles that of the adult decorticate preparation. Neurons are monocularly driven, best activated by stationary light, poorly activated by moving stimuli and rarely display directional selectivity 23,'~4. Movement-related selectivity develops gradually over a 6-8 week period, apparently dependent upon corticotectal maturation. Although a similar distinction between adult and newborn rabbit exists, in this species mature colliculus properties develop within 9 days2°, preceding and apparently independent of visual cortex input 9,1°. The present experiments were performed to investigate the neurophysiological features determined by superior colliculus development in the absence of much of the corticotectal system in cat. Since the corticotectal pathway is retinotopically organized 7 a region can be removed during 'plastic' stages of development, prior to its complete development, and its collicular target area studied at maturity. Three reasonable consequences might be anticipated: (1) effects would be similar to those seen in adult decorticates; (2) a new pattern of superior colliculus organization would emerge; (3) movement-selective properties would develop 'normally', perhaps due to afferent reorganization. The results support the first of these alternatives.
481
SHORT COMMUNICATIONS
TABLE I NEURONAL PROPERTIES IN SUPERIOR COLLICULI W I T H AND W I T H O U T INTACT CORTICOTECTAL PROJECTIONS
Visual cortex lesions were made in 14 kittens 2.5 days-5 weeks of age and the response properties of superior colliculus neurons were studied following a 2-4 month recovery period. The percentages of neurons in the superior colliculus contralateral or ipsilateral to the cortical lesion evidencing; binocularity (Binoc.), directional selectivity (Direct.select.), 'preference' for a stimulus with a small edge (Pref.sm.edge), responsiveness to moving stimuli (M) only, stationary light (SL) only, or both stationary light and movement, are presented. Those cells responsive to both stationary and moving stimuli are further classified on the basis of whether they were, or were not, best activated by movement (M > SL). Numbers in parentheses refer to the sample of neurons tested and ~ to the total sample size. Comparative data from normal and cortically lesioned adults were taken from the studies of Rosenquist and Palmer*, is, Sterling and Wickelgren* *,25 and Wickelgren and Sterling* * *, s0. See text for a discussion, Binoc. (%)
Contralateral
Ipsilateral
74 (34) 80* 97** 35 (80) 29* 30***
Direct. Pref. sin. M only select.(%) edge (%) (%)
77 (26) 75* 75** 28 (54) 12" 7***
64 (14) 70* 90** 52 (21) 70*
SL only (%)
M and SL M > SL (%) (%)
47 (45) 75*
0 (45)
53 (45)
63 (24)
22 (55) 50* 23***
5 (55)
73 (55)
E=67 38 (40) X=108
Subtotal visual cortex lesions were produced by subpial aspiration in 14 kittens anesthetized with sodium pentobarbital and aged 2.5 days (5), 2-3 weeks (7) and 5 weeks (2). The border o f the lesion was to be at area 17 corresponding to approximately 30 ° d o w n in visual space1,31 and to extend caudally to include all o f area 17 on the dorsal and medial surfaces o f the right hemisphere. Thus, some o f 17 and most o f areas 18, 19 and the suprasylvian gyrus were to remain intact. In some cases, however, the splenial sulcus was spared, while in others area 17 and adjacent portions o f area 18 were removed. In no case, was the lesion of area 17 complete and in all animals the anterior aspect o f 17 (especially on the medial surface) remained intact as did m u c h of 18, 19 and all o f the suprasylvian gyrus. Following surgery, the animals were reared in c o m m u n a l cages for 2-4 months. Recording, testing and anesthesia methods have been described 23 and are only summarized here. A t r a c h e o t o m y and a craniotomy were performed using halothane anesthesia, after which the animal was paralyzed with gallamine triethiodide and o-tubocurarine and artificially respired. The eyes were focused on a transparent hemisphere positioned 45 cm f r o m the cornea and used for m a p p i n g the optic discs and receptive fields. The animal was then maintained on a mixture of 70 ~ nitrous oxide and 30 ~ oxygen for recording single unit activity. Electrolytic lesions made at strategic points facilitated the location o f recorded units. Recordings were obtained from cells located primarily in the upper collicular layers, contralateral as well as ipsilateral to the cortical lesion. A n attempt was made to record cells with visual fields located near the area centralis,
482
S H O R T C O M M U N I C A I IONS
but receptive field centers were often distributed as far as 5° dorsal, 20 c ventral, 5° medial, 20 ° lateral. At the end of each experiment the animal was anesthetized with sodium pentobarbital and perfused through the heart with I0'.'~o formalin. The brain was sectioned at 15 /~m and every third section was stained with cresyl violet for serial reconstruction of the cortical lesion and mapping of electrode tracks. Photographs of the dorsal surface of two brains (Fig. 1), in which much of the lateral gyrus was removed at 2.5 days of age, illustrate the characteristic shifting and expansion of the suprasylvian gyrus, after early lesions, to occupy the space previously occupied by the lateral gyrus. The response properties of 67 cells studied in the superior colliculus contralateral to the lesion 2-4 months postoperatively were indistinguishable from those of normal adults6, 21,25. Most were activated by stimuli delivered to either eye, were best driven by moving stimuli, and response magnitude (selectivity) was related to the direction and velocity of movement. The population of neurons recorded in the superior colliculus ipsilateral to the lesions and having receptive fields in retinotopic correspondence (n = 108) with the cortical tissue ablated 1,al was distinctly atypical regardless of the age at which the cortical lesion was made. Table I compares the response selectivity of neurons in these experiments with those in which data were obtained from normal and visual cortex lesioned adults ~6,a°. It is apparent that the response properties of colliculus neurons ipsilateral to the cortical ablation were significantly different from normal, and similar data are being obtained in another laboratory 13. There was a loss of stimulus specificity which was apparent not only in the severe reduction of directional selectivity (77-28~), but also as a relative increase in the effectiveness of stationary light. Nearly half of the cells in the normal (contralateral) colliculus were activated only by a moving stimulus, while 22 ~o~ of the cells studied on the lesion side were movement-specific. Of those cells in the normal colliculus responsive to both stationary and moving stimuli, 63 ~ were clearly most responsive to movement as compared with 38 ~ of ipsilateral colliculus cells, and the surround inhibition (pref. sm. edge) of a stimulus which overlapped the borders of the receptive field6,25 was less frequently observed in the ipsilateral colliculus. The percentage of binocular neurons was severely reduced in the ipsilateral colliculus as the input from the ipsilateral eye is derived, in large part, indirectly from visual cortex 14. Although these effects of cortical ablation were striking, some response properties appeared to be unaltered. The proportion of unresponsive cells and the proportions of on, off and on-off responses to stationary light were similar to those of mature animals2L Many neurons fired vigorously to a stimulus swept across the receptive field and their response selectivity to stimulus velocity appeared unchanged, with many cells responsive over a wide range of velocities. Optimum velocities differed significantly among neurons, as on the normal side, and no evidence was obtained for different optimum velocities between cells of the two colliculi. The effect of stimulus velocity upon the responsiveness of a cell from the ipsilateral superior colliculus is illustrated in Fig. 1. Retinotopic or functional reorganization of the superior colliculus was not evident in any experiment. Tests for responsiveness to somatic and acoustic stimuli
483
SHORT COMMUNICATIONS
At; I
Fig. 1. Visual cortex of the right hemisphere was ablated at 2.5 days of age. The area removed and the subsequent spatial reorganization of adjacent cortex can be seen in photographs of two brains which were made 3.5 months after surgery and are presented above. LG = lateral gyrus; SSG suprasylvian gyrus. The darkened oval represents the receptive field of a cell in the superior colliculus ipsilateral to the cortical lesion (from the brain on the left) and the broken rectangles represent the stimulus employed. Size and location can be seen in relation to the area centralis (AC) and the 5° scale provided. The stimulus was moved across the receptive field in 8 directions (45 ° disparity) and at 5 velocities. As was observed for most superior colliculus cells ipsilateral to the cortical lesion, directional selectivity was not apparent. Symmetrical movements along the horizontal axis (shown here) evoked approximately the same number of impulses as did similar movements in other axis tested, and maximal responses were obtained at low velocities regardless of direction of movement.
484
SHORT COMMUNICATIONS
(characteristic only o f lower layer neurons) were c o n d u c t e d in several p e n e t r a t i o n s a n d the l o c a t i o n a n d response p r o p e r t i e s o f activated neurons were not obviously different f r o m the n o r m a l adult2~,26, ~-9. These d a t a d o indicate that some m o v e m e n t selectivity does develop in the absence o f corticotectal afferents, b u t the selectivity present closely a p p r o x i m a t e s t h a t o b s e r v e d in a d u l t decorticate animals 16,30. It might have been expected, however, t h a t response selectivity w o u l d have developed m o r e like that o f the intact animal, due p e r h a p s to r e o r g a n i z a t i o n o f r e m a i n i n g visual cortex. R e o r g a n i z a t i o n o f corticotectal p r o j e c t i o n s could conceivably account for the small differences in the p r o p o r t i o n o f directionally selective neurons e n c o u n t e r e d here, as c o m p a r e d to d a t a f r o m a d u l t decorticates (Table 1), b u t it seems m o r e likely t h a t these discrepancies reflect differences in sampling, or criteria for classification. Thus, the presence o f visual cortex a p p e a r s to be as critical during d e v e l o p m e n t as in m a t u r i t y for m a i n t a i n i n g the f u n c t i o n a l integrity o f the superior colliculus.
1 BILGE, M., BINGLE, A., SENEVIRATNE, K. N., AND WHITTERIDGE, D., A map of the visual area of the cat, J. Physiol. (Lond.), 191 (1967) 116-118P. 2 BLAKEMORE, C., AND MITCHELL, D. M., Environmental modification of the visual cortex and the neural basis of learning and memory, Nature (Lond.), 241 (1973) 467-468. 3 GOLDaERG, M. E., AND WURTZ, R. H., Activity of superior colliculus in behaving monkey. 1. Visual receptive fields of single neurons, J. NeurophysioL, 35 (1972) 542-559. 4 HIRSCH, H. V. B., AND SPINELLI,D. N., Modification of the distribution of receptive field orientation in cats by selective visual exposure during development, Exp. Brain Res., 13 (1971) 509-527. 5 HUBEL, D. H., AND WIESEL,T. N., The period of susceptibility to the physiological effects of unilateral eye closure in kittens, J. Physiol. (Lond.), 206 (1970) 419-436. 6 MCILWAIN,J. T., AND BUSER, P., Receptive fields of single cells in the cat's superior colliculus, Exp. Brain Res., 5 (1968) 314-325. 7 MCILWAIN,J. T., Retinotopic fidelity of striate cortex-superior colliculus interactions in the cat, J. Neurophysiol., 36 (1973) 702-710. 8 MARCHIAFAVA,P. L., AND PEPEU, G., The responses of units in the superior colliculus of the cat to a moving visual stimulus, Experientia (Basel), 22 (1966) 51-55. 9 MASLANO,R. H., CHOW, K. L., AND STEWART,D. L., Receptive-field characteristics of superior colliculus neurons in the rabbit, J. NeurophysioL, 34 (1971) 148-156. 10 MATHERS,L. H., CHOW, K. L., SPEAR,P. D., AND GROBSTEIN,P., Ontogenesis of receptive fields in the rabbit striate cortex, Exp. Brain Res., 19 (1974) 20-35. 11 MICHAEL,C. R., Visual receptive fields of single neurons in superior colliculus of the ground squirrel, J. Neurophysiol., 35 (1972) 815-832. 12 MICHAEL,C. R., Functional organization of cells in superior colliculus of the ground squirrel, J. Neurophysiol., 35 (1972) 833-846. 13 MIZE, R., AND MURPHY, E. H., Receptive field characteristics in the superior colliculus following visual decortication in infant and adult cats, Paper presented at the American Psychological Association Conventional, Montreal, Canada, August 29, 1973. 14 PALMER, L. A., ROSENQUIST, A. C., AND SPRAGUE, J. M., Corticotectal systems in the cat: their structure and function. In T. FRIGYESI, E. RINVIK AND M. D. YAHR (Eds.), Corticothalamic
Projections and Sensorimotor Activities, Raven Press, New York, 1972, pp. 491-523. 15 PETTIGREW,J., OLSON, C., AND BARLOW, H. B., Kitten visual cortex:short-term, stimulus-induced
changes in connectivity, Science, 180 (1973) 1202-1203. 16 ROSENQUIST, A. C., AND PALMER, L. A., Visual receptive field properties of cells of the superior
colliculus after cortical lesions in the eat, Exp. Neurol., 33 (1971) 629-652. 17 SCHILLER,P. H., STRVKER, M,, CYNADER, M., AND BERMAN,N., Response characteristics of single cells in the monkey superior colliculus following ablation or cooling of visual cortex, J. Neurophysiol., 37 (1974) 181-194.
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485
18 SCHNEIDER, G. E., Mechanisms of functional recovery following lesions of visual cortex or superior colliculus in neonate and adult hamsters, Brain Behav. Evol., 3 (1970) 295-323. 19 SIMINOFF, R., SCHWASSMANN,H. O., AND KRUGER, L., An electrophysiological study of the visual projection to the superior colliculus of the rat, J. comp. Neurol., 127 (1966) 435-444. 20 SPEAR, P. D., CHOW, K. L., MASLAND, R. H., AND MURPHY, E. H., Ontogenesis of receptive field characteristics of superior colliculus neurons in the rabbit, Brain Research, 45 (1972) 67-86. 21 STERN,B. E., AND ARIGBEDE, M. O., A parametric study of movement detection properties of neurons in the cat's superior colliculus, Brain Research, 45 (1972) 437-454. 22 STEIN, B. E., AND ARIGBEDE, M. O., Unimodal and multimodal response properties of neurons in the cat's superior colliculus, Exp. Neurol., 36 (1972) 179-196. 23 STEIN,B. E., LABOS,E., AND KRUGER, L., Sequence of changes in properties of neurons of superior colliculus of the kitten during maturation, J. Neurophysiol., 36 (1973) 667-679. 24 STEIN,B. E., LABOS,E., AND KRUGER, L., Determinants of response latency in neurons of superior colliculus in kittens, J. Neurophysiol., 36 (1973) 680~89. 25 STERLING,P., AND WICKELGREN,B. G., Visual receptive fields in the superior colliculus of the cat, J. Neurophysiol., 32 (1969) 1-15. 26 STRASCHILL,H., AND HOFFMANN, K. P., Functional aspects of localization in the cat's tectum opticum, Brain Research, 13 (1969) 274-283. 27 STRASCHILL,H., AND HOFFMANN,K. P., Activity of movement sensitive neurons of the cat's tectum opticum during spontaneous eye movements, Exp. Brain Res., 11 (1970) 318-326. 28 WETZEL, A. B., THOMPSON, V. E., HOREL, J. A., AND MEYER, P. M., Some consequences of perinatal lesions of the visual cortex in the cat, Psychon. Sci., 3 (1965) 381-382. 29 WICKELGREN,B. G., Superior colliculus: some receptive field properties of bimodally responsive cells, Science, 173 (1971) 69-72. 30 WICKELGREN,B. G., AND STERLING,P., Influence of visual cortex on receptive fields in the superior colliculus of the cat, J. Neurophysiol., 32 (1969) 16-23. 31 WOOLSEY,C. N., Comparative studies on cortical representation of vision, Vision Res., 3 (1971) 365-382.
Braht Research, 83 (1975) 480-485 © Elsevier ScientificPublishing Company, Amsterdam - Printed in The Netherlands
Effects of neonatal cortical lesions upon the cat superior colliculus
BARRY E. STEIN AND BRAULIO MAGALHAES-CASTRO Department of Anatomy, UCLA School of Medicine, Los Angeles, Calif. 90024 (U.S.A.)
(Accepted October 7th, 1974)
During development the brain displays plasticity in that the response properties of visual cortex neurons are determined by early visual experience 2,4,5,15, and the functional anomalies produced by cortical lesions can be partially compensated for during a critical stage of infancy18,28. While the adaptive significance of this capacity is obvious, little information is available about the long-term effects of early cortical lesions upon structures ordinarily dependent upon cortical projections for normal function (e.g., the cat superior colliculus). In all species studied, movement has been found to be the most effective stimulus for the activation of superior colliculus neurons, with response magnitude dependent upon such stimulus parameters as direction and velocity a'6,s'9,11,17,19,21,25,27. Two primary sources of visual input may contribute to these properties, one directly from retina and one via ipsilateral visual cortex x4. In some species, neuronal response selectivity may be unaffected by removal of visual cortex, and this may be related to the selective response properties present in their retinal ganglion cells9,12. In the cat, however, removal of area 17 of visual cortex nearly eliminates binocularity and directional selectivity, and decreases the effectiveness of moving stimuli16,3°. The neonatal cat superior colliculus resembles that of the adult decorticate preparation. Neurons are monocularly driven, best activated by stationary light, poorly activated by moving stimuli and rarely display directional selectivity 23,'~4. Movement-related selectivity develops gradually over a 6-8 week period, apparently dependent upon corticotectal maturation. Although a similar distinction between adult and newborn rabbit exists, in this species mature colliculus properties develop within 9 days2°, preceding and apparently independent of visual cortex input 9,1°. The present experiments were performed to investigate the neurophysiological features determined by superior colliculus development in the absence of much of the corticotectal system in cat. Since the corticotectal pathway is retinotopically organized 7 a region can be removed during 'plastic' stages of development, prior to its complete development, and its collicular target area studied at maturity. Three reasonable consequences might be anticipated: (1) effects would be similar to those seen in adult decorticates; (2) a new pattern of superior colliculus organization would emerge; (3) movement-selective properties would develop 'normally', perhaps due to afferent reorganization. The results support the first of these alternatives.
481
SHORT COMMUNICATIONS
TABLE I NEURONAL PROPERTIES IN SUPERIOR COLLICULI W I T H AND W I T H O U T INTACT CORTICOTECTAL PROJECTIONS
Visual cortex lesions were made in 14 kittens 2.5 days-5 weeks of age and the response properties of superior colliculus neurons were studied following a 2-4 month recovery period. The percentages of neurons in the superior colliculus contralateral or ipsilateral to the cortical lesion evidencing; binocularity (Binoc.), directional selectivity (Direct.select.), 'preference' for a stimulus with a small edge (Pref.sm.edge), responsiveness to moving stimuli (M) only, stationary light (SL) only, or both stationary light and movement, are presented. Those cells responsive to both stationary and moving stimuli are further classified on the basis of whether they were, or were not, best activated by movement (M > SL). Numbers in parentheses refer to the sample of neurons tested and ~ to the total sample size. Comparative data from normal and cortically lesioned adults were taken from the studies of Rosenquist and Palmer*, is, Sterling and Wickelgren* *,25 and Wickelgren and Sterling* * *, s0. See text for a discussion, Binoc. (%)
Contralateral
Ipsilateral
74 (34) 80* 97** 35 (80) 29* 30***
Direct. Pref. sin. M only select.(%) edge (%) (%)
77 (26) 75* 75** 28 (54) 12" 7***
64 (14) 70* 90** 52 (21) 70*
SL only (%)
M and SL M > SL (%) (%)
47 (45) 75*
0 (45)
53 (45)
63 (24)
22 (55) 50* 23***
5 (55)
73 (55)
E=67 38 (40) X=108
Subtotal visual cortex lesions were produced by subpial aspiration in 14 kittens anesthetized with sodium pentobarbital and aged 2.5 days (5), 2-3 weeks (7) and 5 weeks (2). The border o f the lesion was to be at area 17 corresponding to approximately 30 ° d o w n in visual space1,31 and to extend caudally to include all o f area 17 on the dorsal and medial surfaces o f the right hemisphere. Thus, some o f 17 and most o f areas 18, 19 and the suprasylvian gyrus were to remain intact. In some cases, however, the splenial sulcus was spared, while in others area 17 and adjacent portions o f area 18 were removed. In no case, was the lesion of area 17 complete and in all animals the anterior aspect o f 17 (especially on the medial surface) remained intact as did m u c h of 18, 19 and all o f the suprasylvian gyrus. Following surgery, the animals were reared in c o m m u n a l cages for 2-4 months. Recording, testing and anesthesia methods have been described 23 and are only summarized here. A t r a c h e o t o m y and a craniotomy were performed using halothane anesthesia, after which the animal was paralyzed with gallamine triethiodide and o-tubocurarine and artificially respired. The eyes were focused on a transparent hemisphere positioned 45 cm f r o m the cornea and used for m a p p i n g the optic discs and receptive fields. The animal was then maintained on a mixture of 70 ~ nitrous oxide and 30 ~ oxygen for recording single unit activity. Electrolytic lesions made at strategic points facilitated the location o f recorded units. Recordings were obtained from cells located primarily in the upper collicular layers, contralateral as well as ipsilateral to the cortical lesion. A n attempt was made to record cells with visual fields located near the area centralis,
482
S H O R T C O M M U N I C A I IONS
but receptive field centers were often distributed as far as 5° dorsal, 20 c ventral, 5° medial, 20 ° lateral. At the end of each experiment the animal was anesthetized with sodium pentobarbital and perfused through the heart with I0'.'~o formalin. The brain was sectioned at 15 /~m and every third section was stained with cresyl violet for serial reconstruction of the cortical lesion and mapping of electrode tracks. Photographs of the dorsal surface of two brains (Fig. 1), in which much of the lateral gyrus was removed at 2.5 days of age, illustrate the characteristic shifting and expansion of the suprasylvian gyrus, after early lesions, to occupy the space previously occupied by the lateral gyrus. The response properties of 67 cells studied in the superior colliculus contralateral to the lesion 2-4 months postoperatively were indistinguishable from those of normal adults6, 21,25. Most were activated by stimuli delivered to either eye, were best driven by moving stimuli, and response magnitude (selectivity) was related to the direction and velocity of movement. The population of neurons recorded in the superior colliculus ipsilateral to the lesions and having receptive fields in retinotopic correspondence (n = 108) with the cortical tissue ablated 1,al was distinctly atypical regardless of the age at which the cortical lesion was made. Table I compares the response selectivity of neurons in these experiments with those in which data were obtained from normal and visual cortex lesioned adults ~6,a°. It is apparent that the response properties of colliculus neurons ipsilateral to the cortical ablation were significantly different from normal, and similar data are being obtained in another laboratory 13. There was a loss of stimulus specificity which was apparent not only in the severe reduction of directional selectivity (77-28~), but also as a relative increase in the effectiveness of stationary light. Nearly half of the cells in the normal (contralateral) colliculus were activated only by a moving stimulus, while 22 ~o~ of the cells studied on the lesion side were movement-specific. Of those cells in the normal colliculus responsive to both stationary and moving stimuli, 63 ~ were clearly most responsive to movement as compared with 38 ~ of ipsilateral colliculus cells, and the surround inhibition (pref. sm. edge) of a stimulus which overlapped the borders of the receptive field6,25 was less frequently observed in the ipsilateral colliculus. The percentage of binocular neurons was severely reduced in the ipsilateral colliculus as the input from the ipsilateral eye is derived, in large part, indirectly from visual cortex 14. Although these effects of cortical ablation were striking, some response properties appeared to be unaltered. The proportion of unresponsive cells and the proportions of on, off and on-off responses to stationary light were similar to those of mature animals2L Many neurons fired vigorously to a stimulus swept across the receptive field and their response selectivity to stimulus velocity appeared unchanged, with many cells responsive over a wide range of velocities. Optimum velocities differed significantly among neurons, as on the normal side, and no evidence was obtained for different optimum velocities between cells of the two colliculi. The effect of stimulus velocity upon the responsiveness of a cell from the ipsilateral superior colliculus is illustrated in Fig. 1. Retinotopic or functional reorganization of the superior colliculus was not evident in any experiment. Tests for responsiveness to somatic and acoustic stimuli
483
SHORT COMMUNICATIONS
At; I
Fig. 1. Visual cortex of the right hemisphere was ablated at 2.5 days of age. The area removed and the subsequent spatial reorganization of adjacent cortex can be seen in photographs of two brains which were made 3.5 months after surgery and are presented above. LG = lateral gyrus; SSG suprasylvian gyrus. The darkened oval represents the receptive field of a cell in the superior colliculus ipsilateral to the cortical lesion (from the brain on the left) and the broken rectangles represent the stimulus employed. Size and location can be seen in relation to the area centralis (AC) and the 5° scale provided. The stimulus was moved across the receptive field in 8 directions (45 ° disparity) and at 5 velocities. As was observed for most superior colliculus cells ipsilateral to the cortical lesion, directional selectivity was not apparent. Symmetrical movements along the horizontal axis (shown here) evoked approximately the same number of impulses as did similar movements in other axis tested, and maximal responses were obtained at low velocities regardless of direction of movement.
484
SHORT COMMUNICATIONS
(characteristic only o f lower layer neurons) were c o n d u c t e d in several p e n e t r a t i o n s a n d the l o c a t i o n a n d response p r o p e r t i e s o f activated neurons were not obviously different f r o m the n o r m a l adult2~,26, ~-9. These d a t a d o indicate that some m o v e m e n t selectivity does develop in the absence o f corticotectal afferents, b u t the selectivity present closely a p p r o x i m a t e s t h a t o b s e r v e d in a d u l t decorticate animals 16,30. It might have been expected, however, t h a t response selectivity w o u l d have developed m o r e like that o f the intact animal, due p e r h a p s to r e o r g a n i z a t i o n o f r e m a i n i n g visual cortex. R e o r g a n i z a t i o n o f corticotectal p r o j e c t i o n s could conceivably account for the small differences in the p r o p o r t i o n o f directionally selective neurons e n c o u n t e r e d here, as c o m p a r e d to d a t a f r o m a d u l t decorticates (Table 1), b u t it seems m o r e likely t h a t these discrepancies reflect differences in sampling, or criteria for classification. Thus, the presence o f visual cortex a p p e a r s to be as critical during d e v e l o p m e n t as in m a t u r i t y for m a i n t a i n i n g the f u n c t i o n a l integrity o f the superior colliculus.
1 BILGE, M., BINGLE, A., SENEVIRATNE, K. N., AND WHITTERIDGE, D., A map of the visual area of the cat, J. Physiol. (Lond.), 191 (1967) 116-118P. 2 BLAKEMORE, C., AND MITCHELL, D. M., Environmental modification of the visual cortex and the neural basis of learning and memory, Nature (Lond.), 241 (1973) 467-468. 3 GOLDaERG, M. E., AND WURTZ, R. H., Activity of superior colliculus in behaving monkey. 1. Visual receptive fields of single neurons, J. NeurophysioL, 35 (1972) 542-559. 4 HIRSCH, H. V. B., AND SPINELLI,D. N., Modification of the distribution of receptive field orientation in cats by selective visual exposure during development, Exp. Brain Res., 13 (1971) 509-527. 5 HUBEL, D. H., AND WIESEL,T. N., The period of susceptibility to the physiological effects of unilateral eye closure in kittens, J. Physiol. (Lond.), 206 (1970) 419-436. 6 MCILWAIN,J. T., AND BUSER, P., Receptive fields of single cells in the cat's superior colliculus, Exp. Brain Res., 5 (1968) 314-325. 7 MCILWAIN,J. T., Retinotopic fidelity of striate cortex-superior colliculus interactions in the cat, J. Neurophysiol., 36 (1973) 702-710. 8 MARCHIAFAVA,P. L., AND PEPEU, G., The responses of units in the superior colliculus of the cat to a moving visual stimulus, Experientia (Basel), 22 (1966) 51-55. 9 MASLANO,R. H., CHOW, K. L., AND STEWART,D. L., Receptive-field characteristics of superior colliculus neurons in the rabbit, J. NeurophysioL, 34 (1971) 148-156. 10 MATHERS,L. H., CHOW, K. L., SPEAR,P. D., AND GROBSTEIN,P., Ontogenesis of receptive fields in the rabbit striate cortex, Exp. Brain Res., 19 (1974) 20-35. 11 MICHAEL,C. R., Visual receptive fields of single neurons in superior colliculus of the ground squirrel, J. Neurophysiol., 35 (1972) 815-832. 12 MICHAEL,C. R., Functional organization of cells in superior colliculus of the ground squirrel, J. Neurophysiol., 35 (1972) 833-846. 13 MIZE, R., AND MURPHY, E. H., Receptive field characteristics in the superior colliculus following visual decortication in infant and adult cats, Paper presented at the American Psychological Association Conventional, Montreal, Canada, August 29, 1973. 14 PALMER, L. A., ROSENQUIST, A. C., AND SPRAGUE, J. M., Corticotectal systems in the cat: their structure and function. In T. FRIGYESI, E. RINVIK AND M. D. YAHR (Eds.), Corticothalamic
Projections and Sensorimotor Activities, Raven Press, New York, 1972, pp. 491-523. 15 PETTIGREW,J., OLSON, C., AND BARLOW, H. B., Kitten visual cortex:short-term, stimulus-induced
changes in connectivity, Science, 180 (1973) 1202-1203. 16 ROSENQUIST, A. C., AND PALMER, L. A., Visual receptive field properties of cells of the superior
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