Mouse rods signal through gap junctions with cones

Abstract

Rod and cone photoreceptors are coupled by gap junctions (GJs), relatively large channels able to mediate both electrical and molecular communication. Despite their critical location in our visual system and evidence that they are dynamically gated for dark/light adaptation, the full impact that rod–cone GJs can have on cone function is not known. We recorded the photovoltage of mouse cones and found that the initial level of rod input increased spontaneously after obtaining intracellular access. This process allowed us to explore the underlying coupling capacity to rods, revealing that fully coupled cones acquire a striking rod-like phenotype. Calcium, a candidate mediator of the coupling process, does not appear to be involved on the cone side of the junctional channels. Our findings show that the anatomical substrate is adequate for rod–cone coupling to play an important role in vision and, possibly, in biochemical signaling among photoreceptors.DOI: http://dx.doi.org/10.7554/eLife.01386.001

Recruitment of Rod Photoreceptors from Short-Wavelength-Sensitive Cones during the Evolution of Nocturnal Vision in Mammals

“…In addition, rods may have additional functions beyond scotopic light detection. Chemical and electrical rod-cone coupling can mediate mesopic vision (Abd-El-Barr et al, 2009; Asteriti et al, 2014; Hornstein et al, 2005; Pang et al, 2012; Ribelayga and Mangel, 2010). Rods also drive circadian photoentrainment (Altimus et al, 2010) and horizontal cell-mediated surround inhibition of cone signal (Szikra et al, 2014).…”

Nonlinear Spatiotemporal Integration by Electrical and Chemical Synapses in the Retina

“…In the outer retina, gap junctions form electrical synapses among the axons of neighboring rods, between rods and cones, and among cones (Asteriti et al, 2014; DeVries et al, 2002; Tsukamoto et al, 2001). In the mammalian inner retina, the axon terminals of most or all subtypes of ON cone bipolar cells are coupled via gap junctions with the dendrites of AII amacrine cells (Cohen and Sterling, 1990; Marc et al, 2014; Veruki and Hartveit, 2002a) or via gap junctions directly between cone bipolar cells (Cohen and Sterling, 1990).…”

Slow light response kinetics in rods points towards a perturbation of the normal cellular milieu

“…), as well as rod–cone coupling (Asteriti et al . ). Jin and colleagues are aware of and rightfully concerned about these potential problems, as can be seen from their statement: “A recent study has reported that rod–cone coupling increases spontaneously after obtaining intracellular access in mouse cones and that rundown of kinetics with time are often observed in patched rods (Asteriti et al .…”

“…Jin and colleagues are aware of and rightfully concerned about these potential problems, as can be seen from their statement: “A recent study has reported that rod–cone coupling increases spontaneously after obtaining intracellular access in mouse cones and that rundown of kinetics with time are often observed in patched rods (Asteriti et al . ). In our conditions, we observed a rundown in rod kinetics following intracellular access in less than 10% of the rods.…”

“…), but that we later successfully circumvented this problem by recording from rods with a loose seal technique (Asteriti et al . ). Moreover, contrary to what is stated by Jin et al .…”