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Journal of Neuroscience, Vol 12, 4911-4922, Copyright © 1992 by Society for Neuroscience
Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina
EC Hampson, DI Vaney and R Weiler
Department of Physiology and Pharmacology, University of Queensland, Brisbane, Australia.
In mammalian retina, the rod bipolar cells synapse on the AII amacrine
cells, which are therefore the third-order neurons in the rod-signal
pathway. The AII amacrine cells are connected by gap junctions, both to
each other and to fourth-order, On-center cone bipolar cells. They also
receive synaptic input from the dopaminergic amacrine cells, and in this
study, we investigated whether dopamine modulates the permeability of the
gap junctions between AII amacrine cells in the isolated rabbit retina. The
small biotinylated tracer Neurobiotin was injected into nuclear
yellow-labeled AII cells under direct microscopic control. The extent of
tracer coupling to neighboring AII cells, 40-60 min after Neurobiotin
injection (0.5 nA for 60 sec), provided a standard measure of the
permeability of the homologous gap junctions. Under control conditions,
individual AII amacrine cells were coupled to 73 +/- 15 neighboring cells,
and this was unaffected by changes in pH from 6.6 to 7.8. Exogenous
dopamine significantly reduced the tracer coupling at concentrations as low
as 10 nM (26 +/- 16 cells), with the effect increasing with dopamine
concentration up to 10 microM (6 +/- 4 cells). The uncoupling effect of
dopamine was both blocked by the selective D1 antagonist SCH-23390 (10
microM) and mimicked by the specific D1 agonist SKF-38393 (500 microM).
Moreover, the AII amacrine cells were also uncoupled when the retina was
incubated in forskolin (60 microM) and isobutylmethylxanthine (200 microM).
Taken together, these results indicated that the uncoupling was mediated by
a D1-like receptor that stimulates cAMP production. Although the selective
D1 antagonist on its own did not increase tracer coupling, suggesting that
there was little release of endogenous dopamine in the superfused
photo-bleached retina, veratridine-evoked release of endogenous
transmitters did uncouple the AII amacrine cells, and this effect was
blocked by the specific D1 antagonist.
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