Necessity of acetylcholine for retinal directionally selective responses to drifting gratings in rabbit

A model for retinal directional selectivity postulates that GABAergic inhibition of responses to motions in the null (anti-preferred) direction underlies this selectivity. An alternative model postulates that besides this inhibition, there exists an asymmetric, nicotinic acetylcholine (ACh) input from starburst amacrine cells. It is possible for the latter but not the former model that stimuli could exist such that nicotinic blockade eliminates directional selectivity. Such stimuli would drive the cholinergic but not the GABAergic system well. So far, attempts to eliminate directional selectivity with nicotinic blockade have failed, but they always used isolated, moving bars as the stimulus. We confirmed this failure for On-Off directionally selective (DS) ganglion cells in our preparation of the rabbit's retina. However, while recording from these cells, we discovered that nicotinic blockade eliminated directional selectivity to drifting, low spatial frequency sine- and square-wave gratings. This effect was not just due to the smallness of the responses under nicotinic blockade. NMDA blockade caused even smaller responses, but no loss of directional selectivity. This result is consistent with a two-asymmetric-pathways model of directional selectivity, but inconsistent with an asymmetric-GABA-only model. We conclude that asymmetric nicotinic inputs extend the range of stimuli that can elicit directional selectivity to include moving textures, that is, those with multiple peaks in their spatial luminance profile.