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Cited by 31Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchMemory and Neural Mechanisms

An extended amygdala-midbrain circuit controlling cocaine withdrawal-induced anxiety and reinstatement

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Tian, Guilian, Hui, May, Macchia, Desiree, Derdeyn, Pieter, Rogers, Alexandra, Hubbard, Elizabeth, Liu, Chengfeng, Vasquez, Jose J. +4 more·2022·Cell Reports
DOI 10.1016/j.celrep.2022.110775PMC PMC9225486

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Abstract

ABSTRACT While midbrain dopamine (DA) neuronal circuits are central to motivated behaviors, much remains unknown about our knowledge of how these circuits are modified over time by experience to facilitate selective aspects of experience-dependent plasticity. Most studies of the DA system in drug addiction focus on the role of the mesolimbic DA pathway from the ventral tegmental area (VTA) to the nucleus accumbens (NAc) in facilitating drug-associated reward. In contrast, less is known about how midbrain DA cells and associated circuits contribute to negative affective states including anxiety that emerge during protracted withdrawal from drug administration. Here, we demonstrate the selective role of a midbrain DA projection to the amygdala (VTA DA →Amygdala) for anxiety that develops during protracted withdrawal from cocaine administration but does not participate in cocaine reward or sensitization. Our rabies virus-mediated circuit mapping approach revealed a persistent elevation in spontaneous and task-related activity of GABAergic cells from the bed nucleus of the stria terminals (BNST) and downstream VTA DA →Amygdala cells that could be detected even after a single cocaine exposure. Activity in BNST GABA cells was related to cocaine-induced anxiety but not reward or sensitization, and silencing the projection from these cells to the midbrain was sufficient to prevent the development of anxiety during protracted withdrawal following cocaine administration. We observed that VTA DA →Amygdala cells, but not other midbrain DA cells, were strongly activated after a challenge exposure to cocaine, and found that activity in these cells was necessary for the expression of reinstatement of cocaine place preference. Lastly, the importance of activity in VTA DA →Amygdala cells extends beyond cocaine, as these cells mediate the development of anxiety states triggered by morphine and a predator odor. Our results provide an exemplar for how to identify key circuit substrates that contribute to behavioral adaptations and reveal a critical role for BNST GABA →VTA DA →Amygdala pathway in anxiety states induced by drugs of abuse or natural experiences as well as cocaine-primed reinstatement of conditioned place preference.

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  • Optogenetic studies show projection-specific effects of BNST neurons on behavior.

    “This is supported by optogenetic studies showing the projection-specific effects of BNST neurons on behavior (87–90).”

    From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [87]

    The Results section (‘Activity in the BNSTGABA→midbrain projection is required for cocaine-induced anxiety’; page unavailable) reports that selectively inhibiting this projection prevented cocaine-withdrawal anxiety without affecting reward or sensitization. But the paper describes this as chemogenetic inhibition using hM4Di and CNO microspheres, not an optogenetic study. (LLM, conf=0.88)

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Cited by

Sorted by citations

Authors
Tian, G., Hui, M., Macchia, D., Derdeyn, P., Rogers, A., Hubbard, E., Liu, C., Vasquez, J. J., Taniguchi, L., Bartas, K., Carroll, S., & Beier, K. T.
Affiliations
University of California, Irvine (US)
Corresponding author
Beier, Kevin T.
ORCID
Venue
Cell Reports
Publisher
Elsevier BV
Published
2022-05
Volume
39
Issue
5
Pages
110775
ISSN
2211-1247 (ISSN-L)
DOI
10.1016/j.celrep.2022.110775
PMC
PMC9225486
OpenAlex
W4229013103
Cited by
31
References
6
Citations by year
2026: 4 · 2025: 5 · 2024: 11 · 2023: 7 · 2022: 4
FWCI
2.98
Type
journal article
Language
en
Open access
Licence
Locations
  • Cell Reports (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion, cc-by-nc-nd)
  • eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • National Alliance for Research on Schizophrenia and Depression (26845, T32 GM136624-01)
  • National Institutes of Health (T32 GM136624-01, R00 DA041445, DP2 AG067666)
  • National Science Foundation (DGE-1839285)
  • Brain and Behavior Research Foundation
  • Tobacco-Related Disease Research Program (T31KT1437, T31DT1729, T31P1426)
  • Donors Cure Foundation (CCAD2020-002)
  • American Parkinson Disease Association (APDA-5589562)
  • Alzheimer's Association (AARG-NTF-20-685694)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
cocaine withdrawal, cocaine reinstatement, ventral tegmental area, amygdala, midbrain dopamine, bed nucleus of the stria terminalis, GABAergic neurons, cocaine sensitization, cocaine reward, neural circuits
MeSH terms
Amygdala, Anxiety, Cocaine, Dopamine, Humans, Ventral Tegmental Area, Cocaine-Related Disorders

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