VOLTAGE-GATED POTASSIUM CHANNELS CONTROL THE GAIN OF ROD-DRIVEN LIGHT RESPONSES IN MIXED-INPUT ON BIPOLAR CELLS

Abstract

AbstractTo achieve high sensitivity at scotopic levels, vision sacrifices spatial and temporal resolution. The detection of dim light, however, depends crucially on the ability of the visual system to speed up rod signals as they advance towards the brain. At higher light levels, gain control mechanisms are necessary to prevent premature saturation of second-order neurons. We investigated how goldfish mixed-input ON bipolar cells (ON mBCs) manage to partially compensate for the intrinsically slow kinetics of rod signals in the dark-adapted state, and at the same time control the gain of rod signals. Rod-driven responses of axotomized ON mBCs become faster and more transient than those of rod horizontal cells as stimulus intensity increases. This transientness has a voltage-dependency consistent with the activation of a voltage-gated K+ conductance. Simulations with NEURON indicate that the voltage-gated K+ channels responsible for speeding up responses are concentrated at the distal tips of the bipolar cell dendrites, close to the glutamate receptors. These channels act as a gain control mechanism, by shunting the effect of tonically hyperpolarized rods onto the ON mBC. Further activation of K+ channels accelerates the ON mBC response by decreasing the membrane time constant as light levels increase. Therefore, the presence of voltage-gated K+ channels at the dendritic tips of ON mBCs extends the dynamic range of these neurons, and at the same time generates a transient signal already at the first visual synapse.Key Points SummaryHere we show that voltage-gated potassium channels can adjust the gain of the rod input to mixed-input ON bipolar cells and generate a transient signal already at the first visual synapse.These channels are activated during the light-induced depolarization, making bipolar cell light responses smaller, faster, and more transient, effects that can be abolished by the K+ channel blocker TEA.Mathematical simulations suggest that these channels are concentrated at the bipolar cell dendritic tips, close to the site of rod input.This kind of gain control happens at all levels in the retina and is especially important for cells that receive mixed input from rods and cones, in order to prevent premature saturation with increasing light levels and remove the temporal redundancy of the photoreceptor signal.