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Y. Cao, C. Ribelayga, S. C. Mangel; The Horizontal Cell Contribution to the Receptive Field Surround of the ON Pathway in Light-Adapted Rabbit Retinas is GABA- and NKCC-Dependent. Invest. Ophthalmol. Vis. Sci. 2009;50(13):5178.
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Ganglion cells (GCs) display a center-surround receptive field (RF) organization under light-adapted conditions, but lose their surround responses following 30 min of dark adaptation (Barlow et al., 1957). Under light-adapted conditions, horizontal cells (HCs) contribute to GC surround responses (Mangel, 1991) possibly by releasing GABA onto bipolar cells (BCs), which express chloride (Cl)-permeable GABA-A receptor channels. If GABA-A receptors mediate the surround responses of ON-BCs (and ON-GCs), then GABA should depolarize ON-BCs via the Cl cotransporter Na-K-2Cl (NKCC), which accumulates intracellular Cl and is localized to ON-BC dendrites (Vardi et al., 2000). However, the roles of GABA and NKCC in the HC contribution to the ON pathway surround remain unclear.
Pigmented rabbits were light (photopic)- or dark (low scotopic)-adapted for 1 hr or rabbit retinas were incubated in Ringer for 1 hr under light-adapted conditions with or without test drugs. Retinal sections were processed in an identical manner for immunostaining with a specific NKCC (T4, DSHB) antibody. In addition, following at least 30 min light adaptation, the effects of current injections into rabbit HCs on the extracellular spike activity of nearby ON-center GCs were studied.
Intense NKCC antibody labeling was observed in the OPL under light-adapted control conditions, but NKCC immunoreactivity was much less intense 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. In the rabbit retina under light-adapted conditions, picrotoxin, a GABA-A/C antagonist, and bumetanide, a specific NKCC inhibitor, blocked the sign-conserving effect of HC polarizations on ON-center GC spike activity. Picrotoxin also eliminated the reduction in the RF center response of ON-center GCs produced by hyperpolarizing nearby HCs.
The results indicate that the HC contribution to the RF surround of ON-center BCs (and ON-center GCs) is GABA- and NKCC-dependent. Moreover, the findings are consistent with the view that light-induced activation of D1 receptors and NO synthesis increases NKCC activity in the OPL, enhancing the GABA-dependent HC contribution to the RF surround of the ON pathway.
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