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The Journal of Neuroscience, May 11, 2005, 25(19):4801-4805; doi:10.1523/JNEUROSCI.0172-05.2005

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GABA Type-A Activity Controls Its Own Developmental Polarity Switch in the Maturing Retina

Elizabeth Leitch, Julie Coaker, Carol Young, Vandana Mehta, and Evelyne Sernagor

School of Neurology, Neurobiology, and Psychiatry, Medical Sciences, University of Newcastle upon Tyne, Newcastle upon Tyne NE2 4HH, United Kingdom

In the developing CNS, GABA_A responses switch from early excitation to late mature inhibition. The developmental factors that induce the polarity switch remain to be unraveled. Here, we bring the first experimental evidence in vivo in the retina that chronic activation of GABA_A receptors is necessary for the switch to occur and for the chloride extrusion mechanism (through the K⁺/Cl^- cotransporter KCC2) to develop. Using a turtle model and calcium imaging, we investigated how chronic blockade of GABA_A receptors with bicuculline during the period of the GABAergic polarity switch (from 1 week before hatching until 4 weeks after hatching) influences developmental changes in the patterns of spontaneously generated electrical activity in the retinal ganglion cell (RGC) layer. During that period, spontaneous activity normally switches from propagating waves to stationary patches of coactive cells, until correlated activity completely disappears. These changes in activity patterns coincide with the switch of GABA_A responses from excitation to inhibition. When GABA_A receptors are chronically blocked, GABA_A responses remain excitatory and spontaneous waves keep propagating across the RGC layer. Concomitantly, the developmental upregulation of KCC2 is inhibited on dendritic processes in the inner plexiform layer, suggesting that the intracellular concentration of chloride remains higher, as in younger cells. This study presents the first demonstration in vivo that GABA autoregulates its developmental polarity switch, emphasizing the importance of GABAergic activity in controlling activity patterns in the maturing retina.

Key words: retinal waves; retinal development; GABA; KCC2; calcium imaging; spontaneous activity

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Received May 27, 2004; revised March 14, 2005; accepted March 31, 2005.

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