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Research Articles, Behavioral/Cognitive

Anterior Insular Cortex is Critical for the Propensity to Relapse Following Punishment-Imposed Abstinence of Alcohol Seeking

Erin J. Campbell, Jeremy P.M. Flanagan, Leigh C. Walker, Mitchell K.R.I. Hill, Nathan J. Marchant and Andrew J. Lawrence
Journal of Neuroscience 6 February 2019, 39 (6) 1077-1087; DOI: https://doi.org/10.1523/JNEUROSCI.1596-18.2018
Erin J. Campbell
1The Florey Institute of Neuroscience and Mental Health, Parkville, Victoria 3052, Australia, 2Florey Department of Neuroscience and Mental Health, The University of Melbourne, Victoria 3010, Australia, and
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Jeremy P.M. Flanagan
1The Florey Institute of Neuroscience and Mental Health, Parkville, Victoria 3052, Australia, 2Florey Department of Neuroscience and Mental Health, The University of Melbourne, Victoria 3010, Australia, and
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Leigh C. Walker
1The Florey Institute of Neuroscience and Mental Health, Parkville, Victoria 3052, Australia, 2Florey Department of Neuroscience and Mental Health, The University of Melbourne, Victoria 3010, Australia, and
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Mitchell K.R.I. Hill
1The Florey Institute of Neuroscience and Mental Health, Parkville, Victoria 3052, Australia, 2Florey Department of Neuroscience and Mental Health, The University of Melbourne, Victoria 3010, Australia, and
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Nathan J. Marchant
1The Florey Institute of Neuroscience and Mental Health, Parkville, Victoria 3052, Australia, 2Florey Department of Neuroscience and Mental Health, The University of Melbourne, Victoria 3010, Australia, and 3Department of Anatomy and Neurosciences, VU University Medical Center, Amsterdam, 1081 HZ, The Netherlands
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Andrew J. Lawrence
1The Florey Institute of Neuroscience and Mental Health, Parkville, Victoria 3052, Australia, 2Florey Department of Neuroscience and Mental Health, The University of Melbourne, Victoria 3010, Australia, and
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Abstract

Humans with alcohol use disorder typically abstain because of the negative consequences associated with excessive drinking, and exposure to contexts previously associated with alcohol use can trigger relapse. We used a rat model that captures a characteristic of this human condition: namely voluntary abstinence from alcohol use because of contingent punishment. There is substantial variability in the propensity to relapse following extended periods of abstinence, and this is a critical feature preventing the successful treatment of alcohol use disorder. Here we examined relapse following acute or prolonged abstinence. In male alcohol preferring P rats, we found an increased propensity to relapse in Context B, the punishment context after prolonged abstinence. Next, we found that neither alcohol intake history nor the motivational strength of alcohol predicted the propensity to relapse. We next examined the putative circuitry of context-induced relapse to alcohol seeking following prolonged abstinence using Fos as a marker of neuronal activation. The anterior insular cortex (AI) was the only brain region examined where Fos expression correlated with alcohol seeking behavior in Context B after prolonged abstinence. Finally, we used local infusion of GABAA and GABAB receptor agonists (muscimol + baclofen) to show a causal role of the AI in context-induced relapse in Context B, the punishment context after prolonged abstinence. Our results show that there is substantial individual variability in the propensity to relapse in the punishment-associated context after prolonged abstinence, and this is mediated by activity in the AI.

SIGNIFICANCE STATEMENT A key feature of alcohol use disorder is that sufferers show an enduring propensity to relapse throughout their lifetime. Relapse typically occurs despite the knowledge of adverse consequences including health complications or relationship breakdowns. Here we use a recently developed rodent model that recapitulates this behavior. After an extended period of abstinence, relapse propensity is markedly increased in the “adverse consequence” environment, akin to humans with alcohol use disorder relapsing in the face of adversity. From a circuitry perspective, we demonstrate a causal role of the anterior insular cortex in relapse to alcohol seeking after extended abstinence following punishment imposed voluntary cessation of alcohol use.

  • alcohol use disorder
  • anterior insular cortex
  • context
  • iP rat
  • punishment
  • relapse
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The Journal of Neuroscience: 39 (6)
Journal of Neuroscience
Vol. 39, Issue 6
6 Feb 2019
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Anterior Insular Cortex is Critical for the Propensity to Relapse Following Punishment-Imposed Abstinence of Alcohol Seeking
Erin J. Campbell, Jeremy P.M. Flanagan, Leigh C. Walker, Mitchell K.R.I. Hill, Nathan J. Marchant, Andrew J. Lawrence
Journal of Neuroscience 6 February 2019, 39 (6) 1077-1087; DOI: 10.1523/JNEUROSCI.1596-18.2018

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Anterior Insular Cortex is Critical for the Propensity to Relapse Following Punishment-Imposed Abstinence of Alcohol Seeking
Erin J. Campbell, Jeremy P.M. Flanagan, Leigh C. Walker, Mitchell K.R.I. Hill, Nathan J. Marchant, Andrew J. Lawrence
Journal of Neuroscience 6 February 2019, 39 (6) 1077-1087; DOI: 10.1523/JNEUROSCI.1596-18.2018
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Keywords

  • alcohol use disorder
  • anterior insular cortex
  • context
  • iP rat
  • punishment
  • relapse

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