Light increases the gap junctional coupling of retinal ganglion cells

Edward H. Hu, Feng Pan, Béla Völgyi, Stewart A. Bloomfield

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50 Citations (Scopus)

Abstract

We examined the effect of light adaptation on the gap junctional coupling of α-ganglion cells (α-GCs) in rabbit and mouse retinas. We assayed changes in coupling by measuring parameters of tracer coupling following injection of α-GCs with Neurobiotin and the concerted spike activity of α-GC neighbours under dark- and light-adapted conditions. We found that light adaptation using mesopic or photopic background lights resulted in a dramatic increase in the labelling intensity, number, and spatial extent of ganglion and amacrine cells coupled to OFF α-GCs when compared to levels seen under dark adaptation. While this augmentation of coupling by light did not produce an increase in the concerted spontaneous activity of OFF α-GC neighbours, it did significantly increase correlated light-evoked spiking. This was seen as an increase in the number of correlated spikes for α-GC neighbours and an extension of correlations to second-tier neighbours that was not seen under dark-adapted conditions. Pharmacological studies in the rabbit retina indicated that dopamine mediates the observed changes in coupling by differentially activating D1 and D2 receptors under different adaptation states. In this scheme, activation of dopamine D1 receptors following light exposure triggers cAMP-mediated intracellular pathways resulting in an increase in gap junctional conductance. Overall, our results indicate that as we move from night to day there is an enhanced electrical coupling between α-GCs, thereby increasing the concerted activity believed to strengthen the capacity and efficiency of information flow across the optic nerve.In addition to chemical synapses, neurons within the retina communicate via interconnecting channels called gap junctions that allow for rapid propagation of visual signals. The conductance of gap junctions is regulated by neuromodulators, such as dopamine, which can thereby reroute visual information depending on stimulus conditions. We show that brightening of ambient light increases the conductance of gap junctions expressed by ganglion cells, which coordinates the output signals of the retina. These results suggest a mechanism for strengthening the capacity and efficiency of information flow across the optic nerve to the brain during daylight conditions. Journal compilation
Original languageEnglish
Pages (from-to)4145-4163
Number of pages19
JournalJournal of Physiology
Volume588
Issue number21
DOIs
Publication statusPublished - 1 Nov 2010
Externally publishedYes

ASJC Scopus subject areas

  • Physiology

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