Retinal Ganglion Cells Can Rapidly Change Polarity from Off to On

Maria Neimark Geffen,Markus Meister,Saskia E J De Vries,Peter Sterling

doi:10.1371/journal.pbio.0050065

Abstract

Retinal ganglion cells are commonly classified as On-center or Off-center depending on whether they are excited predominantly by brightening or dimming within the receptive field. Here we report that many ganglion cells in the salamander retina can switch from one response type to the other, depending on stimulus events far from the receptive field. Specifically, a shift of the peripheral image—as produced by a rapid eye movement—causes a brief transition in visual sensitivity from Off-type to On-type for approximately 100 ms. We show that these ganglion cells receive inputs from both On and Off bipolar cells, and the Off inputs are normally dominant. The peripheral shift strongly modulates the strength of these two inputs in opposite directions, facilitating the On pathway and suppressing the Off pathway. Furthermore, we identify certain wide-field amacrine cells that contribute to this modulation. Depolarizing such an amacrine cell affects nearby ganglion cells in the same way as the peripheral image shift, facilitating the On inputs and suppressing the Off inputs. This study illustrates how inhibitory interneurons can rapidly gate the flow of information within a circuit, dramatically altering the behavior of the principal neurons in the course of a computation.

Highlights

In the retina, signals flow along parallel, spatially distributed pathways [1]
The eye communicates to the brain all the information needed for vision in the form of electrical pulses, or spikes, on optic nerve fibers. These spikes are produced by retinal ganglion cells, the output neurons of the retina
In a popular view of retinal function, each ganglion cell responds to a small region of interest in the visual image, known as its receptive field, and is specialized for certain image features within that window

Summary

Introduction

Signals flow along parallel, spatially distributed pathways [1]. A major split occurs at the very first synapse: On bipolar cells and Off bipolar cells respond to light with the opposite sign. Retinal ganglion cells receive excitatory input from On or Off bipolars within their dendritic field. On ganglion cells are excited by an increase of illumination in the receptive field center, and Off ganglion cells by a decrease. Certain ganglion cells draw on both bipolar cell types, and are excited transiently both at the onset and the offset of illumination [2,3]. Light falling on the receptive field surround generally antagonizes the action of light in the center: An On cell will be inhibited and an Off cell excited. Pure image motion in the periphery, without stimulation of the receptive field center, is often found to excite retinal ganglion cells [4,5,6,7], certain moving patterns produce inhibition [8,9,10]. When the receptive field center is stimulated as well, peripheral motion generally suppresses the cell’s sensitivity to the center [11,12,13,14], with the occasional differing report [6]

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