Neuroplasticity in the cat's visual system: test of the role of the expanded retino-geniculo-parietal pathway in behavioral sparing following early lesions of visual cortex

Abstract

Sparing of the ability to redirect head and eyes to new stimuli and expansion of the retino-geniculo-parietal pathway are both robust aspects of the repercussions of early lesions of occipital visual areas in cats. The purpose of the present work was to test the proposition that the pathway expansions and spared behaviors are causally linked. The proposition was tested by deactivating either the dorsal lateral geniculate nucleus (dLGN) and thereby uncoupling the primary and secondary limbs of the retino-geniculo-parietal pathway, or silencing the terminus of the pathway, and then testing the ability of cats to detect and orient head and eyes to visual targets. Six cats sustained experimental unilateral lesions of occipital areas 17 and 18 and variable amounts of area 19 on postnatal days 1-2 or 26-30 to induce rewiring and expansion of visual pathways from retina through the dLGN onto a critical region of visuoparietal (VP) cortex. Unilateral lesions ensured that we could use the orienting performance of the intact hemisphere as a fiduciary marker of performance against which performance of the experimental hemisphere could be gauged. When the cats were adult, a secondary test lesion was made on the damaged side by injecting, under electrophysiological guidance, ibotenic acid into either dLGN of four cats or into VP cortex of two cats. Prior to injection of ibotenic acid, all cats oriented head and eyes with high proficiency throughout the contralesional field, and performance was indistinguishable from orienting to stimuli presented in the ipsilesional field; sparing of the orienting behavior was complete. Ibotenic acid lesions of both dLGN and VP cortex induced a profound neglect of stimuli introduced into the contralesional hemifield. Orienting into the ipsilesional field remained high throughout. Subsequently, there was restoration of orienting behavior over the next 4-6 (dLGN deactivation) and 9-12 (VP deactivation) days. The test results demonstrate the essential contribution made by the retino-geniculo-parietal pathway to the ability to detect and redirect head and eyes to look at visual stimuli following early lesions of occipital visual cortices. The subsequent post-test lesion restoration of high orienting proficiency shows that in the absence of dLGN, or the critical region of VP cortex, other regions of cerebral cortex, or other structures such as the superior colliculus, can emerge and make important contributions to orienting behavior. These results reveal a maintained residual, beneficial adaptive plasticity of mature neural circuits even in brains compromised by early lesions of occipital visual areas.