Spatiotemporally Asymmetric Excitation Supports Mammalian Retinal Motion Sensitivity

Abstract

The detection of visual motion is a fundamental function of the visual system. How motion speed and direction are computed together at the cellular level, however, remains largely unknown. Here, we suggest a circuit mechanism by which excitatory inputs to direction-selective ganglion cells in the mouse retina become sensitive to the motion speed and direction of image motion. Electrophysiological, imaging, and connectomic analyses provide evidence that the dendrites of ON direction-selective cells receive spatially offset and asymmetrically filtered glutamatergic inputs along motion-preference axis from asymmetrically wired bipolar and amacrine cell types with distinct release dynamics. A computational model shows that, with this spatiotemporal structure, the input amplitude becomes sensitive to speed and direction by a preferred direction enhancement mechanism. Our results highlight the role of an excitatory mechanism in retinal motion computation by which feature selectivity emerges from non-selective inputs.

Keywords: bipolar cells; dendritic computation; direction selectivity; direction-selective ganglion cells; glutamatergic inputs; motion processing; retina; spatially asymmetric wiring; speed tuning; temporal dynamics.