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O. N. Dumitrescu, F. G. Pucci, K. Y. Wong, D. M. Berson; ON Bipolar Cell Output to the OFF Sublamina of the Inner Plexiform Layer: Contacts With Melanopsin Ganglion Cells and Dopaminergic Amacrine Cells. Invest. Ophthalmol. Vis. Sci. 2009;50(13):5031.
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© ARVO (1962-2015); The Authors (2016-present)
Mammalian ON bipolar cells have been thought to synapse exclusively in the inner IPL (the ON sublamina) onto dendrites of ON-type amacrine and ganglion cells. However, two inner retinal cell types, M1 melanopsin-expressing ganglion cells and dopaminergic amacrine (DA) cells, apparently violate this dogma. Though both clearly receive excitatory synaptic input from ON bipolar cells, their dendrites stratify in the outer OFF sublayer. Here, we tested the hypothesis that the ON-channel input to these cells is mediated by ectopic ON bipolar synapses in the outermost IPL.
We used Grm6-EGFP mice (which express GFP only in ON bipolars) and immunostainings for ribbon markers, vesicles, glutamate receptors, M1 and DA cells, and various bipolar types, in confocal analysis of ON bipolar output synapses. We used FM4-64 imaging in dissociated rat bipolar cells to assess vesicular uptake and release.
ON bipolar cells do make ectopic ribbon synaptic contacts in the OFF IPL. These occur either as overt terminals or en passant contacts from smooth axonal shafts. They are highly concentrated in the outermost sublamina of the OFF sublayer. There they make close contacts with dendrites of both M1 and DA cells at far beyond chance levels, suggesting the presence of synapses between them. We estimate that each M1 cell receives more than 40 such ON bipolar contacts, seemingly enough to account for their synaptically driven ON responses. Live cell imaging demonstrates uptake and release of synaptic vesicles at ectopically located ribbons in ON bipolar cell axons. The ectopic ribbon synapses appear to derive from an ON cone bipolar cell of unknown type. They were not associated with the axons of rod bipolar cells, nor with those of the Type 1 or 2 OFF cone bipolars terminating in the outermost IPL.
ON cone bipolar cells make functional ectopic synapses in the outermost OFF sublayer of the IPL. These are probably the source of the previously unexplained ON channel input to M1 melanopsin ganglion cells and DA amacrine cells.
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