Presynaptic BK channels modulate ethanol-induced enhancement of GABAergic transmission in the rat central amygdala nucleus

J Neurosci. 2014 Oct 8;34(41):13714-24. doi: 10.1523/JNEUROSCI.5284-13.2014.

Abstract

Large-conductance calcium-activated potassium BK channels are widely expressed in the brain and are involved in the regulation of neuronal functions such as neurotransmitter release. However, their possible role in mediating ethanol-induced GABA release is still unknown. We assessed the role of BK channels in modulating the action of ethanol on inhibitory synaptic transmission mediated via GABAA receptors in the rat central nucleus of the amygdala (CeA). Evoked IPSCs (eIPSCs) mediated by GABAA receptors were isolated from CeA neurons under whole-cell voltage clamp, and their response to selective BK channel antagonists, channel activators, or ethanol was analyzed. Blocking BK channels with the specific BK channel antagonist paxilline significantly increased the mean amplitude of eIPSCs, whereas the activation of BK channels with the channel opener NS1619 reversibly attenuated the mean amplitude of eIPSCs. Ethanol (50 mM) alone enhanced the amplitude of eIPSCs but failed to further enhance eIPSCs in the slices pretreated with paxilline. Bath application of either BK channel blockers significantly increased the frequency of miniature IPSCs (mIPSCs). Similarly, 50 mM ethanol alone also enhanced mIPSC frequency. Increases in mIPSC frequency by either selective BK channel antagonists or ethanol were not accompanied with changes in the amplitude of mIPSCs. Furthermore, following bath application of BK channel blockers for 10 min, ethanol failed to further increase mIPSC frequency. Together, these results suggest that blocking BK channels mimics the effects of ethanol on GABA release and that presynaptic BK channels could serve as a target for ethanol effects in CeA.

Keywords: GABA; anxiolytic; inhibition; potassium; presynaptic.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Amygdala / cytology
  • Amygdala / drug effects
  • Amygdala / physiology*
  • Animals
  • Calcium Channels / physiology
  • Central Nervous System Depressants / pharmacology*
  • Ethanol / pharmacology*
  • Excitatory Postsynaptic Potentials / drug effects
  • In Vitro Techniques
  • Large-Conductance Calcium-Activated Potassium Channels / antagonists & inhibitors*
  • Male
  • Potassium Channel Blockers / pharmacology
  • Presynaptic Terminals / drug effects*
  • Rats
  • Rats, Sprague-Dawley
  • Synaptic Transmission / drug effects*
  • gamma-Aminobutyric Acid / physiology*

Substances

  • Calcium Channels
  • Central Nervous System Depressants
  • Large-Conductance Calcium-Activated Potassium Channels
  • Potassium Channel Blockers
  • Ethanol
  • gamma-Aminobutyric Acid