Functional influence of areas 17, 18, and 19 on lateral suprasylvian cortex in kittens and adult cats: implications for compensation following early visual cortex damage

Abstract

The aim of the present study was to investigate the mechanisms of physiological compensation that is seen in the posteromedial lateral suprasylvian (PMLS) cortex of cats that received visual cortex (areas 17, 18, and 19) damage early in life. The strategy was to compare the response properties of PMLS neurons just after visual cortex damage (before any compensation has occurred) with the properties of PMLS neurons in normal cats and cats with long-standing visual cortex damage. Fourteen animals (aged 8 weeks, 18 wweks, 26 weeks, or adult) received a unilateral visual cortex lesion and recordings were made from ipsilateral PMLS cortex within about 24 h. An additional 4 adult cats were studied within either 24 or 3 h of a bilateral visual cortex lesion. Results from these animals were compared with results from normal cats and cats with long-standing visual cortex damage studied previously in this laboratory. At all ages studied, an acute visual cortex lesion reduced the percentage of direction-sensitive cells in PMLS cortex from nearly 80% in normal cats to about 20% after the lesion. In 8- and 18-week-old kittens, nearly all of the remaining PMLS cells responded best to stimulus movement but were not direction sensitive. In 26-week-old and adult cats, the remaining cells were divided between those that responded to movement without a directional preference and those that responded as well to stationary flashed stimuli as to moving stimuli. The presence of receptive-field surround inhibition was not affected significantly by an acute lesion at any age. In addition, few PMLS cells were orientation selective to elongated slits of light in cats with an acute lesion, just as in normal cats. The ocular dominance distributions of PMLS neurons also were normal following an acute visual cortex lesion at all ages studied. These results suggest that the influences of areas 17, 18, and 19 on the response properties of PMLS neurons are the same when the properties first reach maturity as in adult cats. The results also suggest that the mechanisms of physiological compensation for an early visual cortex lesion differ for different response properties. Compensation of direction sensitivity and orientation selectivity (an anomalous property) develops de novo after the early lesion. In contrast, compensation of ocular dominance appears to be due to the maintenance of a pre-existing property that is present immediately after the lesion. Thus, plasticity after early visual cortex damage represents multiple developmental changes in the remaining visual pathways.