Spatial Asymmetry and Temporal Delay of Inhibitory Amacrine Cells Produce Directional Selectivity in Retina

Abstract

Directional selectivity is a unique function relating to agility that some portion of ganglion cells in the retina fire only for moving light signals with specific direction and speed [1]. Taylor et al. [2] showed that inhibitory synaptic outputs from inhibitory amacrine cells to directional selective ganglion cells are playing a critical role in directional selectivity in the rabbit retina. We previously reported that dendrites of inhibitory amacrine cells have active regenerative properties to propagate action potentials [3]. γ-Aminobutyric acid releases from the dendrites were driven by action potential propagation into the dendrites. The speed of action potential propagation in dendrites of amacrine cells was approximately 10 m/s, which is one tenth slower than that of an axon. Thus, initiation and propagation of action potentials on amacrine cell dendrites cause a temporal delay in synaptic outputs to ganglion cells. In addition, asymmetric expansion of dendrites of amacrine cells causes asymmetric synaptic outputs to ganglion cells. Here, we established a novel hypothesis that these features of inhibitory amacrine cells might play an important role in forming directional selectivity. In order to clarify the mechanism of directional selectivity, we numerically analyzed the whole retina activity using a recently developed neural-network simulation powered by NEURON, which models each cell’s electrophysiological activity. All known experimental facts reported to date are explained in a consistent manner by our hypothesis on the connection of cells that direction-selective ganglion cells are receiving inhibitory synaptic inputs from amacrine cell dendrites with a random spatial asymmetry and a temporal delay.