Spatially displaced excitation contributes to the encoding of interrupted motion by the retinal direction-selective circuit

Spatially distributed excitation and inhibition collectively shape a visual neuron9s receptive field (RF) properties. In the direction-selective circuit of the mammalian retina, the effects of strong null-direction inhibition of On-Off direction-selective ganglion cells (ON-OFF DSGCs) on their direction selectivity are well-studied. However, how excitatory inputs influence the On-Off DSGC;s visual response is underexplored. Here, we report that the glutamatergic excitation of On-Off DSGCs shows a spatial displacement to the side where preferred-direction motion stimuli approach the soma (the 9preferred side9). Underlying this displacement is a non-uniform distribution of excitatory conductance across the dendritic span of the DSGC on the preferred-null motion axis. The skewed excitatory RF contributes to robust null-direction spiking during RF activation limited to the preferred side, a potential ethologically relevant signal to encode interrupted or discontinuous motion trajectories abundant in natural scenes. Theoretical analysis indicates that such differential firing patterns of On-Off DSGCs to continuous and interrupted motion stimuli may help leverage synchronous firing to signal the spatial location of a novel moving object in complex, naturalistic visual environments. Our study highlights that visual circuitry, even the well-defined direction-selective circuit, exploits different sets of neural mechanisms under different stimulus conditions to generate context-dependent neural representations of visual features.