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Prefrontal Regulation of Punished Ethanol Self-administration

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Halladay, Lindsay R., Kocharian, Adrina, Piantadosi, Patrick T., Authement, Michael E., Lieberman, Abby G., Spitz, Nathen A., Coden, Kendall, Glover, Lucas R. +3 more·2020·Biological Psychiatry
DOI 10.1016/j.biopsych.2019.10.030PMC PMC7217757
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Abstract

Background A clinical hallmark of alcohol use disorder is persistent drinking despite potential adverse consequences. The ventromedial prefrontal cortex (vmPFC) and dorsomedial prefrontal cortex (dmPFC) are positioned to exert top-down control over subcortical regions, such as the nucleus accumbens shell (NAcS) and basolateral amygdala, which encode positive and negative valence of ethanol (EtOH)-related stimuli. Prior rodent studies have implicated these regions in regulation of punished EtOH self-administration (EtOH-SA). Methods We conducted in vivo electrophysiological recordings in mouse vmPFC and dmPFC to obtain neuronal correlates of footshock-punished EtOH-SA. Ex vivo recordings were performed in NAcS D 1 receptor–expressing medium spiny neurons receiving vmPFC input to examine punishment-related plasticity in this pathway. Optogenetic photosilencing was employed to assess the functional contribution of the vmPFC, dmPFC, vmPFC projections to NAcS, or vmPFC projections to basolateral amygdala, to punished EtOH-SA. Results Punishment reduced EtOH lever pressing and elicited aborted presses (lever approach followed by rapid retraction). Neurons in the vmPFC and dmPFC exhibited phasic firing to EtOH lever presses and aborts, but only in the vmPFC was there a population-level shift in coding from lever presses to aborts with punishment. Closed-loop vmPFC, but not dmPFC, photosilencing on a postpunishment probe test negated the reduction in EtOH lever presses but not in aborts. Punishment was associated with altered plasticity at vmPFC inputs to D 1 receptor–expressing medium spiny neurons in the NAcS. Photosilencing vmPFC projections to the NAcS, but not to the basolateral amygdala, partially reversed suppression of EtOH lever presses on probe testing. Conclusions These findings demonstrate a key role for the vmPFC in regulating EtOH-SA after punishment, with implications for understanding the neural basis of compulsive drinking in alcohol use disorder.

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  • Ventral medial PFC projections to the NAc shell are involved in suppressing ethanol self-administration in the presence of aversive stimuli.

    “Optogenetic experiments have also revealed that ventral medial PFC projections to the NAc shell are involved in suppressing ethanol self-administration in the presence of aversive stimuli (191).”

    From Psychedelics and Other Psychoplastogens for Treating Mental Illness. (2021) · cites this paper as [191]

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Authors
Halladay, L. R., Kocharian, A., Piantadosi, P. T., Authement, M. E., Lieberman, A. G., Spitz, N. A., Coden, K., Glover, L. R., Costa, V. D., Alvarez, V. A., & Holmes, A.
Affiliations
  • National Institutes of Health (US)
  • Oregon Health & Science University (US)
Corresponding author
Halladay, Lindsay R.
ORCID
Venue
Biological Psychiatry
Publisher
Elsevier BV
Published
2020-06
Volume
87
Issue
11
Pages
967-978
ISSN
0006-3223 (ISSN-L)
DOI
10.1016/j.biopsych.2019.10.030
PMC
PMC7217757
OpenAlex
W2985092233
Cited by
74
References
6
Citations by year
2026: 5 · 2025: 6 · 2024: 8 · 2023: 13 · 2022: 8 · 2021: 18 · 2020: 15 · 2019: 1
FWCI
5.02
Type
journal article
Language
en
Open access
Licence
Locations
  • Biological Psychiatry (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute of Neurological Disorders and Stroke
  • National Institute on Alcohol Abuse and Alcoholism
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
ethanol self-administration, punishment, ventromedial prefrontal cortex, dorsomedial prefrontal cortex, alcoholism, nucleus accumbens shell, basolateral amygdala, footshock, compulsive drinking, neural coding, synaptic plasticity, feedback control
MeSH terms
Ethanol, Animals, Nucleus Accumbens, Punishment, Self Administration, Prefrontal Cortex, Mice

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