Effects of visual cortex lesions upon the visual fields of monocularly deprived cats.

The visual fields of 16 cats raised with monocular eyelid suture were measured by means of a visual orienting test. We separately measured the fields of nondeprived and deprived eyes. Each cat was tested preoperatively, and 13 of the cats were tested following lesions of the visual cortex, superior colliculus, and/or optic chiasm. Preoperatively with the nondeprived eye, every cat had a normal monocular field extending roughly from 90" ipsilateral t o 45" contralateral to the eye being tested. Fields for the deprived eye seemed to depend upon the nature of the deprivation. Fourteen of the cats had complete lid fusions, and 13 of these had virtually identical deprived eye fields which essentially included only the monocular segment (i.e., roughly 45" to 90" ipsilateral). Only these 13 cats were tested postoperatively. The fourteenth cat with complete lid closure may have had a visual field for the deprived eye that included the entire ipsilateral hemifield, but its responses were extremely unreliable. Two of the cats had incomplete lid fusions which exposed the cornea and thus permitted some pattern vision during development. Their visual fields for the deprived eye included the entire hemifield. We conclude that rearing a cat with complete monocular lid occlusion produces for the deprived eye a field which is effectively limited to the monocular segment. Following postoperative testing, histological verification of neural lesions was obtained for every cat except one. An optic chiasm transection in one cat rendered its deprived eye totally blind on these tests, presumably because crossing nasal fibers which represent the monocular segment were cut. The chiasm transection also reduced the nondeprived eye's field to 0" to 45" contralateral. Cortical ablations in the other 12 cats were contralateral to the deprived eye or bilateral, and they ranged in size from lesions of areas 17 and 18 to total occipitotemporal ablations. (Cats with the latter ablations also had tectal lesions to counteract hemianopia due to large cortical lesions.) Each of these 12 cats showed a dramatic postoperative increase of the deprived eye's visual field to include most or all of the ipsilateral hemifield. The smallest lesion (involving areas 17 and 18 contralateral t o the deprived eye) produced such an expansion of the deprived eye's field. Collicular ablations in another cat suggest that these expanded fields following cortical lesions depend upon retinotectal pathways. Postoperative fields for the nondeprived eyes were more variable. Generally, smaller lesions caused little change in these fields from preoperative measurements; larger lesions tended to reduce the fields to include only the ipsilateral hemifield. Two cats with bilateral occipitotemporal cortical ablations and transections of the commissure of the superior colliculus exhibited no obvious behavioral differences between use of the nondeprived and deprived eyes, and the monocular fields included the ipsilateral hemifield for each eye. One interpretation of these results is based upon prior suggestions that retinotectal pathways develop fairly normally in monocularly deprived cats, while geniculocortical pathways do not. The animals' preoperatively tested visual behavior and collicular response properties tend to reflect the status of cortical pathways, but following cortical lesions, the orienting functions of retinotectal pathways are more fully expressed. Since these retinotectal pathways are dominated by nasal retina, the entire nasal retina of the deprived eye after appropriate cortical lesions is functional for visual orienting. I Address after July 1, 1979, for repnnt requests. Department of Anatomlcal Sclencea, State University of New York at Stony Brook, School of Basic Health Sciences, Health Sciences Center, Stony Brook, New York 11794 J. COMP. NEUR. (1979) 188: 291-312. 291 292 S. MURRAY SHERMAN A N D JAMES M. SPRAGUE A cat raised with monocular lid suture develops serious abnormalities in the central visual pathways related to its deprived eye, and it also exhibits marked deficits in visually guided behavior when forced to use that eye. The purpose of the present study was to explore further the relationship between these neural and behavioral deficits. In the lateral geniculate nucleus, cells in deprived laminae (i-e., those receiving direct retinal afferents from the deprived eye) are abnormally small (Wiesel and Hubel, '63a; Guillery and Stelzner, '70). Also, instead of the normal proportion of Xand Y-cells,2 deprived laminae appear to have few recordable Y-cells, while the X-cells are relatively unaffected (Sherman et al., '72; LeVay and Ferster, '77; Garey and Blakemore, '77; Lin and Sherman, '78; Lehmkuhle et al., '78). In the striate cortex of deprived cats, the cells are influenced almost exclusively by the nondeprived eye, in contrast to the normal pattern in which most cells are binocularly activated (Wiesel and Hubel, '63b; Wilson and Sherman, '77). However, all of these deficits related to the deprived eye are relatively more serious in the binocular segment of the geniculostriate pathways than in the deprived monocular ~ e g m e n t . ~ That is, lateral geniculate cell sizes and the proportion of recordable Y-cells are fairly normal in the deprived monocular segment (Guillery and Stelzner, '70; Guillery, '72; Sherman et al., '72, '75; Hickey et al., '77). In turn, the deprived eye activates in a normal fashion many cells located in the deprived monocular segment of striate cortex but very few located in the binocular segment (Sherman et al., '74; Wilson and Sherman, '77). These differential effects of monocular deprivation on the binocular and monocular segments of the geniculocortical pathways are taken as evidence for competitive interactions between central pathways from each eye during development (i.e., "binocular competition," see Sherman et al., '74). Since cells in the deprived monocular segment cannot be at stimuli in the visual field of the deprived monocular segment Le., 35-45' to 90" from the vertical meridian and ipsilateral to the deprived eye), but orients poorly or not a t all to stimuli in the binocular segment of visual field (i.e., within 45' of the vertical meridian, Sherman, '73, '74a; also see Sherman et al.,