Direct Evidence for Daily Plasticity of Electrical Coupling between Rod Photoreceptors in the Mammalian Retina

Abstract

Rod photoreceptors are electrically coupled through gap junctions. Coupling is a key determinant of their light response properties, but whether rod electrical coupling is dynamically regulated remains elusive and controversial. Here, we have obtained direct measurements of the conductance between adjacent rods in mouse retina and present evidence that rod electrical coupling strength is dependent on the time of day, the lighting conditions, and the mouse strain. Specifically, we show in CBA/Ca mice that under circadian conditions, the rod junctional conductance has a median value of 98 pS during the subjective day and of 493 pS during the subjective night. In C57BL/6 mice, the median junctional conductance between dark-adapted rods is ϳ140 pS, regardless of the time in the circadian cycle. Adaptation to bright light decreases the rod junctional conductance to ϳ0 pS, regardless of the time of day or the mouse strain. Together, these results establish the high degree of plasticity of rod electrical coupling over the course of the day. Estimates of the rod coupling strength will provide a foundation for further investigations of rod interactions and the role of rod coupling in the ability of the visual system to anticipate, assimilate, and respond to the daily changes in ambient light intensity.

Temporal resolution of single-photon responses in primate rod photoreceptors and limits imposed by cellular noise

“…Rod outer segment currents are thought to be independent in nearby rods due to the lack of voltage dependence of the transduction current (Baylor and Nunn 1986). This is unlike rod voltages, which are correlated between rods due to electrical coupling (Jin and Ribelayga 2016;Li et al 2012); such correlations complicate characterization of rod noise. Furthermore, rod outer segment currents are amenable to quantitative experimental characterization and provide clear limits to the sensitivity of downstream signals and behavior.…”

A congenic line of the C57BL/6J mouse strain that is proficient in melatonin synthesis

“…3,4 In agreement with this, timed extra-ocular injections of melatonin in melatonin-deficient mice restore rhythms of DA release in the retina. 17 The absence of melatonin in the B6 strain and transgenic mouse lines with B6 background has long imposed limitations to the study of DA-dependent rhythmic processes in the retina, such as the strength of electrical coupling between photoreceptors 19,20 or gene expression. 3,4 One of the major goals of this project was to create a melatonin-proficient B6 congenic mouse line and test whether restoring a melatonin rhythm would restore a circadian rhythm of DA release in the retina.…”

Temporal resolution of single photon responses in primate rod photoreceptors and limits imposed by cellular noise

“…Rod outer segment currents are quite independent in nearby rods due to the lack of voltage dependence of the transduction current [19]. This is unlike rod voltages, which are correlated between rods due to electrical coupling [20,21]; such correlations complicate characterization of rod noise. Furthermore, rod outer segment currents are amenable to quantitative experimental characterization and provide clear limits to the sensitivity of downstream signals and behavior.…”

“…The pooling models considered, however, neglect several known features of retinal circuitry downstream of the rod outer segment that likely lower the sensitivity of the retinal output signals. For example, gap junctions between rod inner segments could hamper the ability to separate single photon responses from continuous noise [20,21,43]. Similarly, downstream cellular and synaptic processes will necessarily introduce noise as signals traverse the retina [3,39].…”