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Functional Circuitry for Peripheral Suppression in Mammalian Y-Type Retinal Ganglion Cells

¹Departments of Neuroscience and ²Bioengineering, University of Pennsylvania, Philadelphia, Pennsylvania; and ³Neuroscience Program and ⁴Departments of Ophthalmology and Visual Sciences and ⁵Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, Michigan

Submitted 11 October 2006; accepted in final form 22 April 2007

A retinal ganglion cell receptive field is made up of an excitatory center and an inhibitory surround. The surround has two components: one driven by horizontal cells at the first synaptic layer and one driven by amacrine cells at the second synaptic layer. Here we characterized how amacrine cells inhibit the center response of ON- and OFF-center Y-type ganglion cells in the in vitro guinea pig retina. A high spatial frequency grating (4–5 cyc/mm), beyond the spatial resolution of horizontal cells, drifted in the ganglion cell receptive field periphery to stimulate amacrine cells. The peripheral grating suppressed the ganglion cell spiking response to a central spot. Suppression of spiking was strongest and observed most consistently in OFF cells. In intracellular recordings, the grating suppressed the subthreshold membrane potential in two ways: a reduced slope (gain) of the stimulus-response curve by 20–30% and, in OFF cells, a tonic 1-mV hyperpolarization. In voltage clamp, the grating increased an inhibitory conductance in all cells and simultaneously decreased an excitatory conductance in OFF cells. To determine whether center response inhibition was presynaptic or postsynaptic (shunting), we measured center response gain under voltage-clamp and current-clamp conditions. Under both conditions, the peripheral grating reduced center response gain similarly. This result suggests that reduced gain in the ganglion cell subthreshold center response reflects inhibition of presynaptic bipolar terminals. Thus amacrine cells suppressed ganglion cell center response gain primarily by inhibiting bipolar cell glutamate release.

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