Maturation of spiking activity in trout retinal ganglion cells coincides with upregulation of Kv3.1- and BK-related potassium channels

Abstract

Developmental changes in membrane excitability and the potassium channel profile were monitored in acutely isolated trout retinal ganglion cells by patch-clamp recording in combination with single-cell RT-PCR. During embryonic development in the egg, a sustained above-threshold stimulation of ganglion cells elicited in most cases only a single spike response. After hatching, the proportion of multiply spiking cells increased strongly and the ability of spike frequency coding was acquired. This was accompanied by the occurrence of a highly tetraethylammonium (TEA)- and quinine-sensitive delayed rectifier current, which gradually masked a rapidly inactivating A-type potassium current that was predominant at earlier stages. Pharmacology of the delayed rectifier current closely matched those of recombinant Trawl, a Kv3.1-related potassium channel in trout. The appearance of this current correlated closely with initial expression of Trawl and Traw2 channel transcripts, as revealed by multiplex single-cell RT-PCR, whereas mRNA, encoding Shaker-related channel genes in trout (termed Tshal-Tsha4), were already detectable at early embryonic stages. lberiotoxin-sensitive, calcium-activated potassium currents (BK) were extremely low before hatching, but increased significantly thereafter. These developmental changes in potassium channel expression occurred after the arrival of retinal fibers in the optic tectum and the initiation of synapse formation in the visual center. It is suggested that early expressed Shaker-related potassium channels could act to influence neuronal differentiation, whereas proper neuronal signaling requires expression of Kv3.1 - and BK-related potassium channels. (C) 2003 Wiley-Liss, Inc.