Blockade of intracortical inhibition in kitten striate cortex: effects on receptive field properties and associated loss of ocular dominance plasticity

Abstract

We have investigated the importance of GABAergic inhibition for the receptive field properties and plasticity of cells in the visual cortex of kittens. Osmotic minipumps were used to continuously infuse the GABA-antagonist, bicuculline methiodide (BIC), into striate cortex. Extracellular recordings were made during BIC infusion to assess neuronal response properties during the blockade of inhibition. Recordings were also made from other kittens after concurrent monocular deprivation and BIC infusion to investigate the importance of response selectivity for ocular dominance plasticity. The minipump delivery technique was used to produce a large volume of cortex presumably free of GABA-ergic inhibition. Compared to recordings in saline-infused control hemispheres, about half of the cells in bicuculline-infused hemispheres had abnormally low orientation selectivity. The low selectivity was generally accompanied by marked anomalies in several other receptive field properties. Particularly striking was the large size of the receptive fields. At eccentricities less than 10 deg many receptive fields subtended from 10 to over 30 deg of arc. The less selective neurons also had abnormal responses to flashed stimuli, giving strong transient responses to the onset and offset of large stationary stimuli which filled their receptive fields. These results imply that intracortical inhibition normally suppresses responses to stimuli within a large excitatory zone beyond the classical receptive field. Inhibition is necessary for the normal orientation selectivity of many cells, although the selectivity may be partially established by the cell's excitatory input. Additionally, intracortical inhibition appears to be necessary for the antagonism and segregation of ON and OFF receptive field subregions. In our study of plasticity, we exploited the fact that BIC treatment greatly increases the range of stimuli that activate cortical neurons. Kittens were monocularly deprived for 7 days concurrently with cortical infusion of BIC. After cessation of the drug treatment, physiological recordings were made. Response properties had returned to normal but neurons in BIC-infused hemispheres had a significantly reduced ocular dominance shift compared to neurons in control hemispheres. This is probably related to the reduced selectivity of cells during BIC infusion. The suggestion here is that there is diminished ocular dominance plasticity in BIC-infused hemispheres because of an increased probability of correlated activity between spontaneous discharge from the closed eye and the cortical activity evoked by the open eye afferents.