Topographical Aspects of Intracortical Excitation and Inhibition Contributing to Orientation Specificity in Area 17 of the Cat Visual Cortex

Abstract

Intracortical mechanisms contributing to orientation and direction specificity were investigated with a method of local cortical inactivation. Single-unit activity was recorded in area 17 of the anaesthetized cat while a small volume of cortical tissue 400 - 2900 microm lateral to the recorded cell was inactivated by gamma-aminobutyric acid (GABA) microiontophoresis. Cells were stimulated with moving bars of variable orientation and changes of the response were monitored. Recording and inactivation sites were histologically verified. Statistically significant changes in orientation tuning during GABA-induced remote inactivation were observed in 80 of 145 cells (55%), and consisted in a reduced orientation specificity due to either increased (36%) or decreased (19%) responses. Increases of responses were more pronounced for the non-optimal orientations. This effect mainly occurred with GABA application at distances around 500 microm and is interpreted as loss of inhibition. Reduced orientation specificity as a result of decreasing response mainly to the optimal orientation was interpreted as loss of excitation. This effect most frequently occurred with inactivation at distances around 1000 microm. Loss of inhibition was also elicited from a distance of 1000 microm; such inhibition, however, affected only directionality, without inducing changes in orientation tuning. For several cells at distances >1000 microm from the inactivation site a temporal sequence consisting of a change in direction specificity followed by a reduction of orientation specificity, and finally by direct GABAergic inhibition of the cell under study, could be induced with gradually increasing ejecting currents. The results indicate that excitation and inhibition originating from populations of neurons at different horizontal distances differentially contribute to direction and orientation specificity of a given visual cortical cell.