Nonlinear transfer and temporal gain control in ON bipolar cells

Abstract

The separation of visual input into discrete channels begins at the photoreceptor to bipolar cell synapse. Current models of the ON pathway describe the time-varying membrane voltage of ON bipolar cells as a linear function of light fluctuations. While this linearity holds under some visual conditions, stimulating the retina with full-field, high contrast flashes reveals a number of nonlinearities already present in the input current of ON bipolar cells. First, we show that the synaptic input to ON bipolar cells is asymmetric in response to equal flashes of opposite polarity. Next, we show that this asymmetry emerges because the responses to dark flashes increase linearly with contrast, whereas responses to bright flashes are highly rectified. We also describe how the outward current saturates in response to dark flashes of increasing duration. Furthermore, varying the inter-flash interval between a pair of high contrast flashes reveals a rapid, transient form of gain control that modulates both the amplitude and time course of the flash response. We develop a phenomenological model that captures the primary features of the ON bipolar cell response at high contrast. Finally, we discuss the implications of these nonlinearities in our understanding of how retinal circuitry shapes the visual signal.