Selectivity to approaching motion in retinal inputs to the dorsal visual pathway.

Todd R Appleby,Michael B Manookin

doi:10.7554/elife.51144

Abstract

To efficiently navigate through the environment and avoid potential threats, an animal must quickly detect the motion of approaching objects. Current models of primate vision place the origins of this complex computation in the visual cortex. Here, we report that detection of approaching motion begins in the retina. Several ganglion cell types, the retinal output neurons, show selectivity to approaching motion. Synaptic current recordings from these cells further reveal that this preference for approaching motion arises in the interplay between presynaptic excitatory and inhibitory circuit elements. These findings demonstrate how excitatory and inhibitory circuits interact to mediate an ethologically relevant neural function. Moreover, the elementary computations that detect approaching motion begin early in the visual stream of primates.

Highlights

As an object approaches, the image of that object becomes larger on the surface of an observer’s retina
Several ganglion cell types found in the retinas of humans and non-human primates project to the dorsal visual pathway, including parasol cells (Rodieck and Watanabe, 1993)
We recorded the spike responses of five ganglion cell types—broad thorny, On and Off smooth monostratified, and On and Off parasol ganglion cells—in an in vitro preparation of the macaque monkey retina to determine whether these cells showed preference for approaching or receding

Summary

Introduction

The image of that object becomes larger on the surface of an observer’s retina. Many animals use these size changes to estimate whether and when an object will collide with the animal (Schiff and Detwiler, 1979; Lee, 1976; Kaiser and Hecht, 1995) and to estimate the animal’s own motion through the environment (Clifford et al, 1999; Schrater et al, 2001) Neurons with such selectivity for approaching motion have been found in the dorsal visual pathway of primates (Orban et al, 1992; Duffy and Wurtz, 1991; Wang and Yao, 2011). Less is known about how motion affects the response properties of these cells (Chichilnisky and Kalmar, 2003; Frechette et al, 2005; Manookin et al, 2018)

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Results

Conclusion