Conserved neural mechanisms for direction selectivity in the primate retina

Abstract

Purpose : Detection of motion direction is an essential visual function and a classic model for neural computation. This has been studied intensely in the non-primate retina where starburst amacrine cells (SACs) provide directionally-tuned inhibition to ON and ON-OFF direction-selective retinal ganglion cells (dsRGCs). While SACs are present in primates, their circuitry is largely unknown and the existence of dsRGCs remains an open question. Resolving the long-standing debate over primate retinal direction selectivity requires a detailed wiring diagram of SAC circuitry.

Methods : We reconstructed the structure, synapses and circuitry of ON SACs from a serial block-face scanning electron microscopy volume of macaque central retina. Postsynaptic RGC reconstructions were compared to RGCs labeled by injections of the retrograde tracer rhodamine dextran into the nucleus of the optic tract and dorsal terminal nucleus of the accessory optic system (NOT-DTN).

Results : First, we confirmed that the neural mechanisms supporting direction selectivity in mammalian SACs are conserved in primate. Mechanisms identified included a proximal-distal distribution of input-output synapses along each dendrite, reciprocal inhibition from other SACs and temporally-diverse bipolar cell input. Next, we reconstructed all postsynaptic RGCs. SACs targeted a single RGC type resembling some of the RGCs labeled from the NOT-DTN as well as the mammalian ON-sustained dsRGCs. These RGCs were rare (<1% of all RGCs) with large overlapping dendritic fields that cofasiculated with the SAC plexus. The overlapping RGCs may encode different directions as nearby dendrites rarely received input from the same SACs. The extensive SAC input to the RGCs was directionally tuned, as predicted from the angles of presynaptic SAC dendrites.

Conclusions : Here we show that the necessary machinery for direction selectivity exists within the primate retina, earlier in the primate visual system than classically thought, and implements many of the elementary motion detection strategies found across vertebrate species. Our results shed light on the nature of primate motion processing by identifying which aspects of the mammalian retinal direction selectivity circuit were conserved and which were not. For example, we did not find SAC input to an ON-OFF dsRGC homolog. The RGCs reported here are candidate homologs to the mammalian ON dsRGCs that contribute to optokinetic nystagmus.

This is a 2021 ARVO Annual Meeting abstract.