Temporally Diverse Excitation Generates Direction-Selective Responses in ON- and OFF-Type Retinal Starburst Amacrine Cells

Abstract

The complexity of sensory receptive fields increases from one synaptic stage to the next. In many cases, increased complexity is achieved through spatiotemporal interactions between convergent excitatory and inhibitory inputs. Here, we present evidence that direction selectivity (DS), a complex emergent receptive field property of retinal starburst amacrine cells (SACs), is generated by spatiotemporal interactions between functionally diverse excitatory inputs. Electrophysiological whole-cell recordings from ON and OFF SACs show distinct temporal differences in excitation following proximal compared with distal stimulation of their receptive fields. Distal excitation is both faster and more transient, ruling out passive filtering by the dendrites and indicating a task-specific specialization. Model simulations demonstrate that this specific organization of excitation generates robust DS responses in SACs, consistent with elementary motion detector models. These results indicate that selective integration of spatiotemporally patterned excitation is a computational mechanism for motion detection in the mammalian retina.

Keywords: NMDA receptor; bipolar cell; circular white noise; direction selectivity; mouse; retina; reverse correlation; starburst amacrine cell.