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Y-type retinal ganglion cells show a pronounced, nonlinear, frequency-doubling behavior in response to modulated sinewave gratings. This is not observed in X-type cells. The source of this spatial nonlinear summation is still under debate. We have designed a realistic biophysical model of the cat retina to test the influence of different retinal cell classes and subcircuits on the linearity of ganglion cell responses. The intraretinal connectivity consists of the fundamental feedforward pathway via bipolar cells, lateral horizontal cell connectivity, and two amacrine circuits. The wiring diagram of X- and Y-cells is identical apart from two aspects: (1) Y-cells have a wider receptive field and (2) they receive input from a nested amacrine circuit consisting of narrow- and wide-field amacrine cells. The model was tested with contrast-reversed gratings. First and second harmonic response components were determined to estimate the degree of nonlinearity. By means of circuit dissection, we found that a high degree of the Y-cell nonlinear behavior arises from the spatial integration of temporal photoreceptor nonlinearities. Furthermore, we found a weaker and less uniform influence of the nested amacrine circuit. Different sources of nonlinearities interact in a multiplicative manner, and the influence of the amacrine circuit is ∼25% weaker than that of the photoreceptor. The model predicts that significant nonlinearities occur already at the level of horizontal cell responses. Pharmacological inactivation of the amacrine circuit is expected to exert a milder effect in reducing ganglion cell nonlinearity.

The Influence of Different Retinal Subcircuits on the Nonlinearity of Ganglion Cell Behavior