Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex

Abstract

The input conductance of cells in the cat primary visual cortex (V1) has been shown recently to grow substantially during visual stimulation. Because increasing conductance can have a divisive effect on the synaptic input, theoretical proposals have ascribed to it specific functions. According to the veto model, conductance increases would serve to sharpen orientation tuning by increasing most at off-optimal orientations. According to the normalization model, conductance increases would control the cell's gain, by being independent of stimulus orientation and by growing with stimulus contrast. We set out to test these proposals and to determine the visual properties and possible synaptic origin of the conductance increases. We recorded the membrane potential of cat V1 cells while injecting steady currents and presenting drifting grating patterns of varying contrast and orientation. Input conductance grew with stimulus contrast by 20-300%, generally more in simple cells (40-300%) than in complex cells (20-120%), and in simple cells was strongly modulated in time. Conductance was invariably maximal for stimuli of the preferred orientation. Thus conductance changes contribute to a gain control mechanism, but the strength of this gain control does not depend uniquely on contrast. By assuming that the conductance changes are entirely synaptic, we further derived the excitatory and inhibitory synaptic conductances underlying the visual responses. In simple cells, these conductances were often arranged in push-pull: excitation increased when inhibition decreased and vice versa. Excitation and inhibition had similar preferred orientations and did not appear to differ in tuning width, suggesting that the intracortical synaptic inputs to simple cells of cat V1 originate from cells with similar orientation tuning. This finding is at odds with models where orientation tuning in simple cells is achieved by inhibition at off-optimal orientations or sharpened by inhibition that is more broadly tuned than excitation.