Stimulus-specific oscillations in a retinal model

Abstract

High-frequency oscillatory potentials (HFOPs) in the vertebrate retina are stimulus specific. The phases of HFOPs recorded at any given retinal location drift randomly over time, but regions activated by the same stimulus tend to remain phase locked with approximately zero lag, whereas regions activated by spatially separate stimuli are typically uncorrelated. Based on retinal anatomy, we previously postulated that HFOPs are mediated by feedback from a class of axon-bearing amacrine cells that receive excitation from neighboring ganglion cells-via gap junctions-and make inhibitory synapses back onto the surrounding ganglion cells. Using a computer model, we show here that such circuitry can account for the stimulus specificity of HFOPs in response to both high- and low-contrast features. Phase locking between pairs of model ganglion cells did not depend critically on their separation distance, but on whether the applied stimulus created a continuous path between them. The degree of phase locking between spatially separate stimuli was reduced by lateral inhibition, which created a buffer zone around strongly activated regions. Stimulating the inhibited region between spatially separate stimuli increased their degree of phase locking proportionately. Our results suggest several experimental strategies for testing the hypothesis that stimulus-specific HFOPs arise from axon-mediated feedback in the inner retina.