Escalated or Suppressed Cocaine Reward, Tegmental BDNF, and Accumbal Dopamine Caused by Episodic versus Continuous Social Stress in Rats
Open accessAbstract
The neural link between ostensibly aversive stress experiences and intensely rewarding drug taking remains to be delineated. Epidemiological data associate stress and the abuse of various drugs, and experimental data identify the conditions that determine how episodic social stress intensifies the motivation for cocaine and the actual self-administration of cocaine. Two types of social stress have been the focus of experimental study in Long-Evans rats, since they engender divergent changes in drug- or sugar-rewarded behavior and in neuroadaptation. Episodic social defeat stress consists of four brief confrontations between the experimental rat and an aggressive resident rat of the Long-Evans strain over the course of 10 d. Subordination stress involves the continuous exposure to an aggressive resident for 5 weeks, while living in a protective cage within the resident's home cage with brief daily confrontations. These stress experiences result in (1) increased intravenous cocaine self-administration under a fixed ratio schedule with prolonged binge-like access in episodically defeated intruder rats but suppressed cocaine intake by continuously subordinate rats; (2) deteriorated sugar preference and intake and decreased exploratory behavior in subordinate, but not intermittently defeated, rats; and (3) a sensitized dopamine (DA) response in the nucleus accumbens via in vivo microdialysis and increased tegmental brain-derived neural growth factor (BDNF) in episodically defeated rats, whereas the continuously subordinate rats show suppression of the DA and BDNF responses. These divergent neuroadaptations to social stress may represent the substrates for the intensification of cocaine "bingeing" relative to the anhedonia-like deterioration of reward processes during subordination stress.
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Rats under a 10-day episodic defeat paradigm had a sensitised dopamine response in the nucleus accumbens, whilst when under a 5-week continuous subordination paradigm they exhibited a suppressed dopamine response.
“Likewise, rats under a 10-day episodic defeat paradigm had a sensitised dopamine response in the nucleus accumbens, whilst when under a 5-week continuous subordination paradigm they exhibited a suppressed dopamine response (Miczek et al., 2011).”
From The effects of psychosocial stress on dopaminergic function and the acute stress response (2019) · cites this paper as Miczek et al., 2011
Acute stressors are encoded by dopamine-releasing neurons in the VTA, cause dopamine sensitization in the nucleus accumbens, and facilitate drug taking; mesolimbic dopamine release also encodes negative motivational states and stress responses.
“Recent experiments also show that acute stressors are encoded by DA-releasing neurons in the VTA, cause DA sensitization in the NAC, and facilitate drug taking; demonstrating that mesolimbic DA release also encodes negative motivational states and stress responses (Miczek et al 2011; Wang and Tsien 2011).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Miczek et al 2011
Some stress-related effects of CRF in the NAC shell may be DA-dependent.
“Some of the stress-related effects of CRF in the NAC shell may be DA-dependent; recall that DA is also modulated by acute and chronic stressors (Miczek et al 2011; Wang and Tsien 2011; Chen et al 2012b).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Miczek et al 2011
The facilitative effects of acute stressors on male pair bonding are directly analogous to the facilitative effects of acute stressors on drug-taking behavior.
“The facilitative effects of acute stressors on male pair bonding are directly analogous to the facilitative effects of acute stressors on drug-taking behavior, a study which, interestingly, was also performed in male rodents (Miczek et al 2011).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Miczek et al 2011
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“experiments also show that acute stressors are encoded by DA-releasing neurons in the ventral tegmental area (VTA), cause DA sensitization in the NAC, and facilitate drug taking, demonstrating that mesolimbic DA release also encodes negative motivational states and stress responses (Miczek et al. 2011; Wang and Tsien…”
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- Authors
- Miczek, K. A., Nikulina, E. M., Shimamoto, A., & Covington, H. E.
- Affiliations
- Tufts University (US)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-07-06
- Volume
- 31
- Issue
- 27
- Pages
- 9848-9857
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3144494
- OpenAlex
- W2053981588
- Cited by
- 162
- References
- 70
- Citations by year
- 2025: 4 · 2024: 8 · 2023: 6 · 2022: 12 · 2021: 7 · 2020: 10 · 2019: 12 · 2018: 11 · 2017: 16 · 2016: 11 · 2015: 14 · 2014: 19 · 2013: 12 · 2012: 15
- FWCI
- 6.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Alcohol Abuse and Alcoholism (R01AA013983)
- National Institute on Drug Abuse (R03DA024817, DA-02632, R01DA026451, DA024817, R01DA002632, R01DA031734, DA026451)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- cocaine self-administration, social stress, nucleus accumbens dopamine, brain-derived neurotrophic factor, cocaine reward, sugar preference, exploratory behavior, anhedonia, neural adaptation, Long-Evans rats
- MeSH terms
- Analysis of Variance, Animals, Body Weight, Cocaine, Conditioning, Operant, Dopamine, Electrochemistry, Food Handling, Gene Expression Regulation, Male, Motor Activity, Nucleus Accumbens, Reinforcement Schedule, Reward, Self Administration, Stress, Psychological, Sucrose, Time Factors, Oncogene Proteins v-fos, Microdialysis, Ventral Tegmental Area, Dopamine Uptake Inhibitors, Brain-Derived Neurotrophic Factor, Rats, Long-Evans, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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