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The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell

Abstract

Directional selectivity is a response that is greater for a visual stimulus moving in one (PREF) direction than for the opposite (NULL) direction, and its computation in the vertebrate retina is a classical issue in functional neurophysiology. To date, most quantitative experimental studies have relied on extracellular responses for identifying properties of the directionally selective circuit. Here I describe an intracellular analysis using whole-cell patch recordings of the synaptic events underlying the spike response in directionally selective ganglion cells of the turtle retina. These quantitative measurements allowed me to distinguish among various explicit classes of circuit models that can, in principle, account for ganglion cell directional selectivity. I found that ganglion cell directional selectivity is due to an excitatory input that itself is directionally selective, and that the crucial shunting inhibition implicated in this computation must act on cells presynaptic to the ganglion cell.

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Figure 1: Three basic combinations of excitatory () and inhibitory () synaptic input onto a directionally selective neuron can account for the neuron's response properties.
Figure 2: Compartmental model simulation of postsynaptically generated directional selectivity based on excitatory–inhibitory synaptic correlation at the ganglion cell (c, circuit nodes marked by circles).
Figure 3: Electrophysiological recordings of visual responses of a directionally selective ganglion cell (B25) in the turtle retina.
Figure 4: Population measures for synaptic inputs to directionally selective ganglion cells in the turtle.
Figure 5: Electrophysiological recordings of visual responses of a directionally selective ganglion cell (A46) in turtle retina.

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Acknowledgements

I thank T. Poggio for support and inspiration for this project, and for providing his laboratory for the experiments (Department of Brain and Cognitive Science at the Massachusetts Institute of Technology). I also thank L. Menendez de la Prida for comments on the manuscript, N. Grzywacz and R. Smith for technical assistance and discussions at an early stage of the work, and J. Lisman, E. Fernandez, J. Ammermuller, Y. Frégnac, C. Monier, V. Bringuier and I. Segev for discussions. Part of this work was supported by grants from the Fondation Fyssen, Fondation Phillipe, and a CNRS ATIPE Fellowship.

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Correspondence to Lyle J. Borg-Graham.

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Borg-Graham, L. The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell. Nat Neurosci 4, 176–183 (2001). https://doi.org/10.1038/84007

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