Adaptation to background light permits contrast coding at rod bipolar cell synapses

Abstract

Purpose: Rod photoreceptors contribute to vision across ~6 log units of light intensity. This wide dynamic range is postulated to depend on light-dependent switching between two parallel pathways linking rods to ganglion cells: rods signal through the rod bipolar (RB) pathway at dim backgrounds, whereas rods signal through cones and cone bipolar cell pathways at brighter backgrounds. We evaluated this conventional model of the retinal circuitry by assessing RB output at circuit and synaptic levels.

Methods: Retinas were isolated from c57bl/6 mice, and retinal slices and whole-mount preparatons were prepared as described in published work (Jarsky et al. 2011; Wang et al. 2011). RB-mediated light responses were recorded in ganglion cells and RB-mediated synaptic currents in AII amacrine cells in the mouse retina. Experimental observations were probed using a phenomenological model of the RB-AII synapse (Jarsky et al. 2011) in which transmission is described as a function of vesicle cycling.

Results: 1) Background light eliminates event detection in the rod bipolar pathway; 2) Signal-to-noise ratio at the rod bipolar synapse depends on presynaptic V_M; 3) The rod bipolar circuit encodes contrast in the presence of background light; 4) The rod bipolar’s contrast response is enabled by temporary suppression of ongoing synaptic release; 5) In the presence of background light the rod bipolar circuit shows high contrast sensitivity and band-pass temporal filtering; 6) Vesicle pool dynamics limit the frequency response.

Conclusions: As background luminance increases, the RB’s role transitions from event detection to contrast coding. This transition is predicted by the intrinsic properties of the synapse: specifically, by the effect that sustained depolarization of presynaptic V_M has on the cycling of the readily-releasable vesicle pool.

Keywords: 693 retinal connections, networks, circuitry • 691 retina: proximal (bipolar, amacrine, and ganglion cells) • 478 contrast sensitivity