Paired Recording to Study Electrical Coupling Between Photoreceptors in Mouse Retina

In the dark, light signals are conventionally routed through the following circuit: rods synapse onto rod bipolar (RB) cells, which in turn contact AII amacrine cells. AII cells segregate the light signal into the on and off pathways by making electrical synapses with on cone bipolar (CB) cells and glycinergic inhibitory chemical synapses with off CB cells. These bipolar cells synapse onto their respective ganglion cells, which transfer on and off signals to the visual centers of the brain. Two alternative pathways have recently been postulated for the signal transfer in scotopic conditions: 1) electrical coupling between rods and cones, and 2) a circuit independent of cone photoreceptors, implying direct contacts between rods and off CB cells. Anatomical evidence supports the existence of both these circuits. To investigate the contribution of these alternative pathways to scotopic vision in the mammalian retina, we have performed patch-clamp recordings from ganglion cells in the dark-adapted retina of the rabbit, mouse, and rat. Approximately one-half of the ganglion cells in the rabbit retina received off signals through a circuit that was independent of RB cells. This was shown by their persistence in the presence of the glutamate agonist 2-amino-4-phosphonobutyric acid (APB), which blocks rod→RB cell signaling. Consistent with this result, strychnine, a glycine receptor antagonist, was unable to abolish these off responses. In addition, we were able to show that some off cone bipolar dendrites terminate at rod spherules and make potential contacts. In the mouse retina, however, there seems to be a very low proportion of off signals carried by an APB-resistant pathway. No ganglion cells in the rat retina displayed APB- and strychnine-resistant responses. Our data support signaling through flat contacts between rods and off CB cells as the alternative route, but suggest that the significance of this pathway differs between species.

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Rod electrical coupling is controlled by a circadian clock and dopamine in mouse retina

The Journal of Physiology ◽

10.1113/jphysiol.2014.284919 ◽

2015 ◽

Vol 593 (7) ◽

pp. 1597-1631 ◽

Cited By ~ 32

Author(s):

Nan Ge Jin ◽

Alice Z. Chuang ◽

Philippe J. Masson ◽

Christophe P. Ribelayga

Keyword(s):

Circadian Clock ◽

Electrical Coupling ◽

Mouse Retina

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Circadian clock and dopamine control of rod photoreceptor electrical coupling in mouse retina

Journal of Vision ◽

10.1167/13.15.42 ◽

2013 ◽

Vol 13 (15) ◽

pp. P7-P7

Author(s):

C. Ribelayga ◽

N. Jin

Keyword(s):

Circadian Clock ◽

Electrical Coupling ◽

Mouse Retina ◽

Rod Photoreceptor

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Expression and modulation of connexin30.2, a novel gap junction protein in the mouse retina

Visual Neuroscience ◽

10.1017/s0952523810000131 ◽

2010 ◽

Vol 27 (3-4) ◽

pp. 91-101 ◽

Cited By ~ 29

Author(s):

LUIS PÉREZ DE SEVILLA MÜLLER ◽

KARIN DEDEK ◽

ULRIKE JANSSEN-BIENHOLD ◽

ARNDT MEYER ◽

MARIA M. KREUZBERG ◽

...

Keyword(s):

Protein Kinase ◽

Gap Junction ◽

Ganglion Cells ◽

Electrical Coupling ◽

Amacrine Cells ◽

Mouse Retina ◽

Coding Region ◽

Transgenic Mouse Line ◽

Junction Protein ◽

Displaced Amacrine Cells

AbstractMammalian retinae express multiple connexins that mediate the metabolic and electrical coupling of various cell types. In retinal neurons, only connexin36, connexin45, connexin50, and connexin57 have been described so far. Here, we present an analysis of a novel retinal connexin, connexin30.2 (Cx30.2), and its regulation in the mouse retina. To analyze the expression of Cx30.2, we used a transgenic mouse line in which the coding region of Cx30.2 was replaced by lacZ reporter DNA. We detected the lacZ signal in the nuclei of neurons located in the inner nuclear layer and the ganglion cell layer (GCL). In this study, we focused on the GCL and characterized the morphology of the Cx30.2-expressing cells. Using immunocytochemistry and intracellular dye injections, we found six different types of Cx30.2-expressing ganglion cells: one type of ON-OFF, three types of OFF, and two types of ON ganglion cells; among the latter was the RGA1 type. We show that RGA1 cells were heterologously coupled to numerous displaced amacrine cells. Our results suggest that these gap junction channels may be heterotypic, involving Cx30.2 and a connexin yet unidentified in the mouse retina. Gap junction coupling can be modulated by protein kinases, a process that plays a major role in retinal adaptation. Therefore, we studied the protein kinase–induced modulation of coupling between RGA1 and displaced amacrine cells. Our data provide evidence that coupling of RGA1 cells to displaced amacrine cells is mediated by Cx30.2 and that the extent of this coupling is modulated by protein kinase C.

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Gap junctional coupling between retinal amacrine and ganglion cells underlies coherent activity integral to global object perception

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1708261114 ◽

2017 ◽

Vol 114 (48) ◽

pp. E10484-E10493 ◽

Cited By ~ 20

Author(s):

Kaushambi Roy ◽

Sandeep Kumar ◽

Stewart A. Bloomfield

Keyword(s):

Gap Junctions ◽

Long Range ◽

Ganglion Cells ◽

Electrical Coupling ◽

Amacrine Cells ◽

Spatial Separation ◽

Object Perception ◽

Mouse Retina ◽

Genetic Ablation ◽

Connexin 36

Coherent spike activity occurs between widely separated retinal ganglion cells (RGCs) in response to a large, contiguous object, but not to disjointed objects. Since the large spatial separation between the RGCs precludes common excitatory inputs from bipolar cells, the mechanism underlying this long-range coherence remains unclear. Here, we show that electrical coupling between RGCs and polyaxonal amacrine cells in mouse retina forms the synaptic mechanism responsible for long-range coherent activity in the retina. Pharmacological blockade of gap junctions or genetic ablation of connexin 36 (Cx36) subunits eliminates the long-range correlated spiking between RGCs. Moreover, we find that blockade of gap junctions or ablation of Cx36 significantly reduces the ability of mice to discriminate large, global objects from small, disjointed stimuli. Our results indicate that synchronous activity of RGCs, derived from electrical coupling with amacrine cells, encodes information critical to global object perception.

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