Withdrawal from chronic ethanol exposure increases postsynaptic glutamate function of insular cortex projections to the rat basolateral amygdala

Neuropharmacology. 2020 Aug 1:172:108129. doi: 10.1016/j.neuropharm.2020.108129. Epub 2020 May 8.

Abstract

A key feature of alcohol use disorder (AUD) is negative affect during withdrawal, which often contributes to relapse and is thought to be caused by altered brain function, especially in circuits that are important mediators of emotional behaviors. Both the agranular insular cortex (AIC) and the basolateral amygdala (BLA) regulate emotions and are sensitive to ethanol-induced changes in synaptic plasticity. The AIC and BLA are reciprocally connected; and the effects of chronic ethanol exposure on this circuit have yet to be explored. Here, we use a combination of optogenetics and electrophysiology to examine the pre- and postsynaptic changes that occur to AIC-BLA synapses following withdrawal from 7- or 10-days of chronic intermittent ethanol (CIE) exposure. While CIE/withdrawal did not alter presynaptic glutamate release probability from AIC inputs, withdrawal from 10, but not 7, days of CIE increased AMPA receptor-mediated postsynaptic function at these synapses. Additionally, NMDA receptor-mediated currents evoked by electrical stimulation of the external capsule, which contains AIC afferents, were also increased during withdrawal. Notably, a single subanesthetic dose of ketamine administered at the onset of withdrawal prevented the withdrawal-induced increases in both AMPAR and NMDAR postsynaptic function. Ketamine also prevented the withdrawal-induced increases in anxiety-like behavior measured using the elevated zero maze. Together, these findings suggest that chronic ethanol exposure increases postsynaptic function within the AIC-BLA circuit and that ketamine can prevent ethanol withdrawal-induced alterations in synaptic plasticity and negative affect.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Administration, Inhalation
  • Alcoholism / physiopathology*
  • Animals
  • Basolateral Nuclear Complex / drug effects*
  • Central Nervous System Depressants / pharmacology*
  • Cerebral Cortex / drug effects*
  • Electric Stimulation
  • Electrophysiological Phenomena
  • Ethanol / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Excitatory Postsynaptic Potentials / drug effects*
  • Glutamic Acid / metabolism*
  • Ketamine / pharmacology
  • Male
  • Neural Pathways / drug effects*
  • Optogenetics
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, AMPA / drug effects
  • Receptors, N-Methyl-D-Aspartate / drug effects
  • Substance Withdrawal Syndrome / metabolism*

Substances

  • Central Nervous System Depressants
  • Excitatory Amino Acid Antagonists
  • Receptors, AMPA
  • Receptors, N-Methyl-D-Aspartate
  • Ethanol
  • Glutamic Acid
  • Ketamine