Light Adaptation of Retinal Rod Bipolar Cells

Abstract

The sensitivity of retinal cells is altered in background light to optimize the detection of contrast. For scotopic (rod) vision, substantial adaptation occurs in the first two cells, the rods and rod bipolar cells (RBCs), through sensitivity adjustments in rods and postsynaptic modulation of the transduction cascade in RBCs. To study the mechanisms mediating these components of adaptation, we made whole-cell, voltage-clamp recordings from retinal slices of mice from both sexes. Adaptation was assessed by fitting the Hill equation to response-intensity relationships with the parameters of half-maximal response (I1/2), Hill coefficient (n), and maximum response amplitude (Rmax). We show that rod sensitivity decreases in backgrounds according to the Weber–Fechner relation with anI1/2of ∼50 R* s−1. The sensitivity of RBCs follows a near-identical function, indicating that changes in RBC sensitivity in backgrounds bright enough to adapt the rods are mostly derived from the rods themselves. Backgrounds too dim to adapt the rods can however altern, relieving a synaptic nonlinearity likely through entry of Ca2+into the RBCs. There is also a surprising decrease ofRmax, indicating that a step in RBC synaptic transduction is desensitized or that the transduction channels became reluctant to open. This effect is greatly reduced after dialysis of BAPTA at a membrane potential of +50 mV to impede Ca2+entry. Thus the effects of background illumination in RBCs are in part the result of processes intrinsic to the photoreceptors and in part derive from additional Ca2+-dependent processes at the first synapse of vision.SIGNIFICANCE STATEMENTLight adaptation adjusts the sensitivity of vision as ambient illumination changes. Adaptation for scotopic (rod) vision is known to occur partly in the rods and partly in the rest of the retina from presynaptic and postsynaptic mechanisms. We recorded light responses of rods and rod bipolar cells to identify different components of adaptation and study their mechanisms. We show that bipolar-cell sensitivity largely follows adaptation of the rods but that light too dim to adapt the rods produces a linearization of the bipolar-cell response and a surprising decrease in maximum response amplitude, both mediated by a change in intracellular Ca2+. These findings provide a new understanding of how the retina responds to changing illumination.