Nucleus accumbens dopamine mediates amphetamine-induced impairment of social bonding in a monogamous rodent species
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The prairie vole ( Microtus ochrogaster ) is a socially monogamous rodent species that forms pair bonds after mating, a behavior in which central dopamine (DA) has been implicated. Here, we used male prairie voles to examine the effects of drug exposure on pair bonding and related neural circuitry. In our first experiment, amphetamine (AMPH) motivated behavior was examined using a conditioned place preference (CPP) paradigm and was shown to be mediated by activation of D1-like DA receptors. Next, we examined the effects of repeated AMPH exposure on pair bonding. Intact and saline pretreated control males displayed mating-induced partner preferences, whereas males pretreated with AMPH at the doses effective to induce CPP failed to show mating-induced partner preferences. Such AMPH treatment also enhanced D1, but not D2, DA receptor expression in the nucleus accumbens (NAcc). Furthermore, pharmacological blockade of D1-like DA receptors in the NAcc rescued mating-induced partner preferences in AMPH-treated males. Together, our data indicate that repeated AMPH exposure may narrow the behavioral repertoire of male prairie voles via a DA receptor-specific mechanism in the NAcc, resulting in the impairment of pair bond formation.
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SPECT investigations in TS have found higher DAT binding in the right caudate, the striatum, the putamen after amphetamine challenge, and the basal ganglia.
“Single-photon emission computed tomography investigations in TS have found higher DAT binding in the right caudate [635], the striatum [636-639], the putamen after amphetamine challenge [640], and the basal ganglia [641].”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [637]
Sexually naïve male prairie voles that receive this treatment reject potential female partners and fail to bond with them, exactly as is observed in pair-bonded males.
“Sexually naïve male prairie voles that receive this treatment reject potential female partners and fail to bond with them, exactly as is observed in pair-bonded males (Liu et al 2010).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Liu et al 2010
Administering amphetamines to prairie voles daily for 3 days causes an upregulation of D1R in the nucleus accumbens that mimics the upregulation seen in pair bonding.
“More directly, administering amphetamines to prairie voles daily for 3 days causes an upregulation of D1R in the NAC that mimics the upregulation seen in pair bonding (Liu et al 2010).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Liu et al 2010
These same males are able to form a pair bond if D1R in the nucleus accumbens shell is blocked with an antagonist, a manipulation that prevents the expression of selective aggression in drug-naïve, pair bonded males.
“These same males are able to form a pair bond if D1R in the NAC shell is blocked with an antagonist, a manipulation that prevents the expression of selective aggression in drug-naïve, pair bonded males (Aragona et al 2006; Liu et al 2010).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Liu et al 2010
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- Authors
- Liu, Y., Aragona, B. J., Young, K. A., Dietz, D. M., Kabbaj, M., Mazei-Robison, M., Nestler, E. J., & Wang, Z.
- Affiliations
- Florida State University (US)
- University of Michigan (US)
- Fishberg Department of Neuroscience, Mount Sinai School of Medicine, New York, NY 10029
- Icahn School of Medicine at Mount Sinai (US)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-12-29
- Volume
- 107
- Issue
- 3
- Pages
- 1217-1222
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2824263
- OpenAlex
- W2032569537
- Cited by
- 101
- References
- 53
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 4 · 2023: 5 · 2022: 3 · 2021: 5 · 2020: 3 · 2019: 3 · 2018: 8 · 2017: 9 · 2016: 13 · 2015: 3 · 2014: 6 · 2013: 11 · 2012: 11
- FWCI
- 3.05
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Public Health Service (DAK02-23048, DAR01-19627, MHR01-58616)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- nucleus accumbens, dopamine, amphetamine, pair bonding, social monogamy, Microtus ochrogaster, dopamine D1 receptor, dopamine D2 receptor, conditioned place preference, mate preferences, dopamine receptor expression
- MeSH terms
- Amphetamine, Animals, Arvicolinae, Dopamine, Female, Male, Nucleus Accumbens, Sexual Behavior, Animal, Social Behavior, Blotting, Western
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