Abstract

At early stages of visual processing, receptive fields are typically described as subtending local regions of space and thus performing computations on a narrow spatial scale. Nevertheless, stimulation well outside of the classical receptive field can exert clear and significant effects on visual processing. Given the distances over which they occur, the retinal mechanisms responsible for these long-range effects would certainly require signal propagation via active membrane properties. Here the physiology of a wide-field amacrine cell—the wiry cell—in macaque monkey retina is explored, revealing receptive fields that represent a striking departure from the classic structure. A single wiry cell integrates signals over wide regions of retina, 5–10 times larger than the classic receptive fields of most retinal ganglion cells. Wiry cells integrate signals over space much more effectively than predicted from passive signal propagation, and spatial integration is strongly attenuated during blockade of NMDA spikes but integration is insensitive to blockade of NaV channels with TTX. Thus these cells appear well suited for contributing to the long-range interactions of visual signals that characterize many aspects of visual perception.

Highlights

  • THE CANONICAL SUBUNIT for visual processing is the centersurround receptive field in which a narrow center lies in spatial antagonism to a weaker, more diffuse surround of opposite sign

  • Our findings provide the first study of the biophysical and light encoding properties of wiry amacrine cells in the macaque monkey retina

  • Further experimentation revealed that the response polarity of these cells shifted during object motion, from either ON or OFF to ON-OFF (Fig. 6), supporting a possible role in encoding of visual motion

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Summary

Introduction

THE CANONICAL SUBUNIT for visual processing is the centersurround receptive field in which a narrow center lies in spatial antagonism to a weaker, more diffuse surround of opposite sign. “Wiry” amacrine cells, studied here, have been anatomically identified in the macaque (Mariani 1990) and human (Kolb et al 1992) retina. They lack axons and exhibit long, straight dendrites emanating ϳ1 mm from the soma and stratifying narrowly within specific regions of the inner plexiform (i.e., synaptic) layer. The receptive fields of these widefield cells were large, radiating structures lacking classical center-surround antagonism. The width of these receptive fields subtended Ͼ5° of visual angle. Pharmacological blockade strongly attenuated signals from distal dendrites, consistent with signal propagation via active membrane processes

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