Rods in daylight act as relay cells for cone-driven horizontal cell–mediated surround inhibition

Abstract

Vertebrate vision relies on two types of photoreceptors, rods and cones, which signal increments in light intensity with graded hyperpolarizations. Rods operate in the lower range of light intensities while cones operate at brighter intensities. The receptive fields of both photoreceptors exhibit antagonistic center-surround organization. Here we show that at bright light levels, mouse rods act as relay cells for cone-driven horizontal cell-mediated surround inhibition. In response to large, bright stimuli that activate their surrounds, rods depolarize. Rod depolarization increases with stimulus size, and its action spectrum matches that of cones. Rod responses at high light levels are abolished in mice with nonfunctional cones and when horizontal cells are reversibly inactivated. Rod depolarization is conveyed to the inner retina via postsynaptic circuit elements, namely the rod bipolar cells. Our results show that the retinal circuitry repurposes rods, when they are not directly sensing light, to relay cone-driven surround inhibition.

Ambient illumination switches contrast preference of specific retinal processing streams

“…1) at five different mean light levels (1 R*·rod Ϫ1 ·s Ϫ1 , or 1 R* for short, 10 R*, 100 R*, 1,000 R*, 10,000 R*) and recorded responses of large ensembles of RGCs on MEAs. Stimulation at 1 R* and 10 R* activates only rod photoreceptors (scotopic light levels), with signals elicited at 1 R* being transmitted exclusively by RBCs; stimulation at 100 R* and 1,000 R* activates both rods and cones (mesopic light levels); and stimulation at 10,000 R* activates primarily cones (photopic light level) (Bloomfield and Dacheux 2001;Farrow et al 2013;Field et al 2009;Murphy and Rieke 2006;Naarendorp et al 2010;Szikra et al 2014;Tikidji-Hamburyan et al 2015).…”

“…Increases in ambient illumination have been shown to strengthen RGC receptive field surrounds in several species (Barlow et al 1957;Bisti et al 1977;Dedek et al 2008;Enroth-Cugell and Robson 1966;Farrow et al 2013) and can induce responses to nonpreferred contrasts for large (e.g., full field) stimuli (Creutzfeldt et al 1970;Sagdullaev and McCall 2005). Alternatively, in RGCs receiving convergent input from ON and OFF pathways, changes in the relative weights of these inputs in the receptive field center could alter contrast preference (Tikidji-Hamburyan et al 2015). To distinguish between these mechanisms, we characterized spatiotemporal receptive fields of RGCs at light levels from 1 R* to 10,000 R* using Gaussian white noise bar stimulation.…”

“…Rather than being turned on and off, it appears that the modus operandi of retinal neurons and pathways can change with ambient illumination. For example, in bright light cones can co-opt rods, inverting their responses via horizontal cells to mediate surround signals (Szikra et al 2014). Similarly, cones can function as relay cells of rod signals at dim light levels (Nelson 1977;Schneeweis and Schnapf 1995;Soucy et al 1998;Szikra et al 2014).…”

“…For example, in bright light cones can co-opt rods, inverting their responses via horizontal cells to mediate surround signals (Szikra et al 2014). Similarly, cones can function as relay cells of rod signals at dim light levels (Nelson 1977;Schneeweis and Schnapf 1995;Soucy et al 1998;Szikra et al 2014). AII amacrine cells switch their excitatory input from chemical synapses with rod bipolar cells (RBCs) to electrical synapses with ON cone bipolar cells (Manookin et al 2008;Munch et al 2009), whereas RBCs and some RGCs change the source of their inhibitory input (Farrow et al 2013;Ichinose and Lukasiewicz 2012).…”

“…By comparison, how contrast encoding and the detection of complex features depend on ambient illumination is not well studied. A recent study found that contrast responses of RGCs can change qualitatively as a function of ambient light levels (Tikidji-Hamburyan et al 2015). Whether such changes are restricted to specific RGC types that exhibit distinctive shifts in contrast encoding and how altered contrast responses affect the detection of more complex features remain unknown.…”