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J Neurophysiol 93: 3479-3488, 2005. First published December 15, 2004; doi:10.1152/jn.00839.2004
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Light Signaling in Scotopic Conditions in the Rabbit, Mouse and Rat Retina: A Physiological and Anatomical Study

Dario A. Protti1,2, Nicolas Flores-Herr2, Wei Li3, Stephen C. Massey3 and Heinz Wässle2

1Discipline of Physiology, School of Medical Sciences and Institute for Biomedical Research, The University of Sydney, Australia; 2Department of Neuroanatomy, Max Planck Institute for Brain Research, Frankfurt am Main, Germany; and 3Ophthalmology and Visual Science, University of Texas Medical School at Houston, Houston, Texas

Submitted 16 August 2004; accepted in final form 7 December 2004

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.

Address for reprint requests and other correspondence: D. A. Protti, Discipline of Physiology, School of Medical Sciences and Inst. for Biomedical Research (F13), The Univ. of Sydney, NSW 2006, Australia (E-mail: dariop{at}physiol.usyd.edu.au)




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