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Y. Cao, C. Ribelayga, S. C. Mangel; Light/Dark Adaptive Regulation of GABAA Receptor and Chloride Cotransporter Expression and Activity Modulates the ON-Pathway Surround. Invest. Ophthalmol. Vis. Sci. 2010;51(13):3289.
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Ganglion cells (GCs) display a center-surround receptive field (RF) following prolonged (>30 min) light adaptation, but lose their surround responses following prolonged dark adaptation (Barlow et al., 1957). Under light-adapted conditions, horizontal cells (HCs) contribute to ON-GC surround responses (Mangel, 1991) possibly by releasing GABA onto ON-bipolar cell (BC) dendrites, which express Cl-permeable GABAA receptor (GABAAR) channels and the Cl cotransporter NKCC. We thus tested whether light/dark adaptive regulation of GABAARs and NKCC mediates light/dark adaptive modulation of the ON-pathway surround.
Pigmented rabbits were bright light (photopic)- or dark (low scotopic)-adapted for 1 h or rabbit retinas were incubated in Ringer for 1 h under light-adapted conditions with or without test drugs. Retinal sections were processed in an identical manner for immunostaining with specific antibodies against the β2/3 subunit-containing, GABAAR (MAB341, Millipore) and NKCC (T4, DSHB). Following prolonged light adaptation, the effects of current injections into rabbit HCs on the activity of nearby ON-GCs were studied.
Intense GABAAR and NKCC antibody labeling were observed in ON-BC dendrites and HC somata under light-adapted control conditions, but both immunosignals were minimal in dark-adapted retinas or in light-adapted retinas pre-treated with the dopamine D1 antagonist SCH23390 or the nitric oxide (NO) synthase inhibitor L-NAME. Under light-adapted conditions, picrotoxin, a GABAA/C antagonist, and bumetanide, a specific NKCC inhibitor, blocked the effect of HC polarizations on ON-GC spike activity. Picrotoxin also eliminated the reduction in the ON-GC center response produced by hyperpolarizing nearby HCs.
These results suggest that prolonged light adaptation increases D1 receptor activation and NO synthesis so that GABAAR and NKCC expression and activity on the dendrites of ON-BCs are enhanced, producing the RF surrounds of ON-BCs (and ON-GCs). In contrast, following prolonged dark adaptation D1 receptor activation and NO synthesis are minimal so that GABAAR and NKCC expression and activity are substantially reduced, eliminating the RF surrounds of ON-BCs (and ON-GCs).
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