Effects of chronic ethanol exposure on neuronal function in the prefrontal cortex and extended amygdala

Kristen E Pleil; Emily G Lowery-Gionta; Nicole A Crowley; Chia Li; Catherine A Marcinkiewcz; Jamie H Rose; Nora M McCall; Antoniette M Maldonado-Devincci; A. Leslie Morrow; Sara R Jones; Thomas L Kash

doi:10.1016/j.neuropharm.2015.06.017

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Effects of chronic ethanol exposure on neuronal function in the prefrontal cortex and extended amygdala

Journal article

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Effects of chronic ethanol exposure on neuronal function in the prefrontal cortex and extended amygdala

Kristen E Pleil, Emily G Lowery-Gionta, Nicole A Crowley, Chia Li, Catherine A Marcinkiewcz, Jamie H Rose, Nora M McCall, Antoniette M Maldonado-Devincci, A. Leslie Morrow, Sara R Jones, …

Neuropharmacology, Vol.99, pp.735-749

12/2015

DOI: 10.1016/j.neuropharm.2015.06.017

PMCID: PMC4781662

PMID: 26188147

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https://www.ncbi.nlm.nih.gov/pmc/articles/4781662View

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Abstract

Chronic alcohol consumption and withdrawal leads to anxiety, escalated alcohol drinking behavior, and alcohol dependence. Alterations in the function of key structures within the cortico-limbic neural circuit have been implicated in underlying the negative behavioral consequences of chronic alcohol exposure in both humans and rodents. Here, we used chronic intermittent ethanol vapor exposure (CIE) in male C57BL/6J mice to evaluate the effects of chronic alcohol exposure and withdrawal on anxiety-like behavior and basal synaptic function and neuronal excitability in prefrontal cortical and extended amygdala brain regions. Forty-eight hours after four cycles of CIE, mice were either assayed in the marble burying test (MBT) or their brains were harvested and whole-cell electrophysiological recordings were performed in the prelimbic and infralimbic medial prefrontal cortex (PLC and ILC), the lateral and medial central nucleus of the amygdala (lCeA and mCeA), and the dorsal and ventral bed nucleus of the stria terminalis (dBNST and vBNST). Ethanol-exposed mice displayed increased anxiety in the MBT compared to air-exposed controls, and alterations in neuronal function were observed in all brain structures examined, including several distinct differences between subregions within each structure. Chronic ethanol exposure induced hyperexcitability of the ILC, as well as a shift toward excitation in synaptic drive and hyperexcitability of vBNST neurons; in contrast, there was a net inhibition of the CeA. This study reveals extensive effects of chronic ethanol exposure on the basal function of cortico-limbic brain regions, suggests that there may be complex interactions between these regions in the regulation of ethanol-dependent alterations in anxiety state, and highlights the need for future examination of projection-specific effects of ethanol in cortico-limbic circuitry. •Ethanol-exposed mice displayed increased anxiety compared to air-exposed controls.•CIE induced hyperexcitability of the infralimbic cortex.•CIE induced a shift toward excitation in synaptic drive and hyperexcitability of vBNST neurons.•CIE exposure induced a net inhibition of the CeA.

Central amygdala

Synaptic transmission

Limbic system

Prefrontal cortex

Bed nucleus of the stria terminalis

Patch-clamp electrophysiology

Chronic alcohol exposure

Neuronal excitability

Details

Title: Subtitle: Effects of chronic ethanol exposure on neuronal function in the prefrontal cortex and extended amygdala
Creators: Kristen E Pleil - Bowles Center for Alcohol Studies, University of North Carolina School of Medicine, Chapel Hill, NC, USA
Emily G Lowery-Gionta - Bowles Center for Alcohol Studies, University of North Carolina School of Medicine, Chapel Hill, NC, USA
Nicole A Crowley - Bowles Center for Alcohol Studies, University of North Carolina School of Medicine, Chapel Hill, NC, USA
Chia Li - Bowles Center for Alcohol Studies, University of North Carolina School of Medicine, Chapel Hill, NC, USA
Catherine A Marcinkiewcz - Bowles Center for Alcohol Studies, University of North Carolina School of Medicine, Chapel Hill, NC, USA
Jamie H Rose - Department of Physiology & Pharmacology, Wake Forest School of Medicine, Winston-Salem, NC, USA
Nora M McCall - Bowles Center for Alcohol Studies, University of North Carolina School of Medicine, Chapel Hill, NC, USA
Antoniette M Maldonado-Devincci - Bowles Center for Alcohol Studies, University of North Carolina School of Medicine, Chapel Hill, NC, USA
A. Leslie Morrow - Bowles Center for Alcohol Studies, University of North Carolina School of Medicine, Chapel Hill, NC, USA
Sara R Jones - Department of Physiology & Pharmacology, Wake Forest School of Medicine, Winston-Salem, NC, USA
Thomas L Kash - Bowles Center for Alcohol Studies, University of North Carolina School of Medicine, Chapel Hill, NC, USA
Resource Type: Journal article
Publication Details: Neuropharmacology, Vol.99, pp.735-749
DOI: 10.1016/j.neuropharm.2015.06.017
PMID: 26188147
PMCID: PMC4781662
NLM abbreviation: Neuropharmacology
ISSN: 0028-3908
eISSN: 1873-7064
Publisher: Elsevier Ltd
Grant note: name: NIH, award: F32 AA021043, K99 AA023599, U01 AA020911, R01 AA019454, U01 AA020935, F31 AA022280, F32 AA022549, F32 AA021319, T32 ES007126, F31 DA03558, P01 AA017056, U01 AA014091; name: Bowles Center for Alcohol Studies, award: P60 AA011605
Language: English
Date published: 12/2015
Academic Unit: Iowa Neuroscience Institute; Neuroscience and Pharmacology
Record Identifier: 9984040397302771

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