Ventral tegmental area involvement in pair bonding in male prairie voles
Abstract
Dopamine is known to play a critical role in social attachment in monogamous voles. However, little is known about the neurochemical regulation of central dopamine release during pair bond formation. Here we examine the effects on partner preference formation in male prairie voles of neurochemical manipulations in the ventral tegmental area (VTA), a major source of dopamine to brain regions implicated in pair bonding. Administration of NBQX, an AMPA receptor antagonist, or bicuculline, a GABA receptor antagonist, into the VTA induced partner preferences within 6 h in the absence of mating. We also found that, after unilateral administration of NBQX into the VTA, neuronal activation, as indicated by the expression of the immediate early gene c-fos, was decreased in the nucleus accumbens, prefrontal cortex, and medial amygdala, but was unchanged in the lateral septum and in a control region, the arcuate nucleus. These results confirm a role for the VTA in partner preference formation in monogamous voles and extend the list of neurochemicals important in pair bonding to include glutamate and GABA.
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Several studies indicate that mesolimbic DA pathways regulate vole pair-bonding and social behaviors.
“Several studies have indicated that mesolimbic DA pathways regulate vole pair-bonding and social behaviors [537].”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [537]
Application of GABAergic or glutamatergic antagonists within the VTA can induce partner preferences in male prairie voles.
“Dopaminergic activity within the VTA may also contribute to pair bond formation as application of either GABAergic or glutamatergic antagonists within the VTA, both which presumably enhance dopamine release within the nucleus accumbens, can induce partner preferences in male prairie voles (Curtis and Wang, 2005).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Curtis and Wang, 2005
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Evaluation of two automated metrics for analyzing partner preference tests
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“Henderson, Florida State University), which has been used to measure locomotor activity in a number of studies (Curtis et al., 2001; Aragona et al., 2003; Curtis and Wang, 2005), provided nearly identical “social proximity” results as our simplified use of Noldus EthoVision, 3.”
Dopaminergic Dynamics Contributing to Social BehaviorPreprint
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“…raphe, and hypothalamus (Gingrich et al. 2000; Young et al. 2001; Leypold et al. 2002; Robinson et al. 2002; Liu and Wang 2003; Young and Wang 2004; Curtis and Wang 2005; Aragona et al. 2006; Lin et al. 2011; Robinson et al. 2011; Dölen et al. 2013; Yang et al. 2013; Felix-Ortiz and Tye 2014;…”
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“More recent studies also have examined the role of dopamine in mediating social behavior (Aragona et al., 2003, 2006; Curtis and Wang, 2003, 2005a,b; Curtis et al., 2001, 2003b; Gingrich et al., 2000; Keer and Stern, 1999; Lorrain et al., 1999; Mermelstein and Becker, 1995; Mitchell and Gratton,…”
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“Specifically, the medial prefrontal cortex, the dorsal striatum, the ventral pallidum, the ventral tegmental area, bed nucleus of the stria terminalis, insular cortex, and the amygdala are involved in social decision making and reward learning, and represent intriguing targets for future study (58-68).”
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“DAergic neurons in the ventral tegmental area (VTA) may be the predominant source of DA release in the NAcc during mating (Curtis and Wang, 2005), but we found very little Fos expression in either TH-ir or non-TH-ir cells of the VTA (or the substantia nigra; data not reported) in any group of males.”
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“induced partner preference in monogamous prairie voles (Curtis and Wang, 2005).”
Social Modulation during Songbird Courtship Potentiates Midbrain Dopaminergic Neurons
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“Finally, because the catecholaminergic circuit from the ventral tegmental area (VTA) to NAcc has been well established in a variety of species including voles (31,32), we processed sections spanning the VTA taken from the NAcc FG injection group for TH and FG double-labeling, as an internal control for validating our…”
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“2011), an area that is part of the mesolimbic dopamine circuitry and implicated in pair bonding in male prairie voles (Curtis and Wang 2005).”
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“Areas of the brain where changes in dopaminergic neurotransmission produce these effects include the mesolimbic system (Aragona et al., 2003, 2006; Curtis and Wang, 2005), but, as with other social behaviors, multiple catecholaminergic systems are likely to be involved (Dominguez and Hull, 2005;…”
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“…reinforce courtship and sociosexual interactions in birds (Alger et al., 2011; Barr and Woolley, 2018), promote pair-bonding in prairie voles (Curtis and Wang, 2005), and facilitate sexual behavior in numerous species across taxa (Balfour et al., 2004; Charlier et al., 2005; Kramer et al., 2017).”
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“In prairie voles, DA release in the NAc is particularly important for pair-bond formation [158], with DA actions on the D2 receptor family being important for formation and actions on the D1 receptor family important for retention of the pair bond [159].”
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“…facilitates partner preference formation, without mating, whereas concurrent central (i.c.v) administration of DA receptor antagonists blocks this behavior in female prairie voles, indicating an interaction between DA and glucocorticoids in partner preference formation (Curtis and Wang 2005a).”
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“In contrast, we found a low level of binding in the OB and mPFC (Table 3, Figure 1), and extremely low levels of OTR binding in NAc, LS, PVN, and thalamus (Figure 1).”
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“4 12 Although, this network is thought to be an evolutionarily conserved network, little is known about how this network processes and communicates information for behavioral outputs.”
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“Furthermore, the mesolimbic reward system, both at the level of the cell bodies in the ventral tegmental area 20,21 and downstream in the ventral striatum (i.e.,nucleusaccumbens,NAc),isactive duringsocialinteractionin voles 22 andiscrucialforpairbonding.”
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Dopaminergic Regulation of Pair Bonding in the Socially Monogamous Prairie Vole
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- Authors
- CURTIS, J., & WANG, Z.
- Affiliations
- Florida State University (US)
- Corresponding author
- CURTIS, J
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 2005-10-15
- Volume
- 86
- Issue
- 3
- Pages
- 338-346
- ISSN
- 0031-9384 (ISSN-L)
- OpenAlex
- W2086621160
- Cited by
- 74
- References
- 49
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 8 · 2023: 1 · 2022: 2 · 2021: 2 · 2020: 1 · 2019: 3 · 2018: 4 · 2017: 1 · 2016: 6 · 2015: 3 · 2014: 4 · 2013: 5 · 2012: 3
- FWCI
- 5.35
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (MH 58616, MH-66734, R21MH066734, R01MH058616)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (F32HD040722, HD 40722)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- ventral tegmental area, pair bonding, mate preferences, Microtus ochrogaster, monogamy, dopamine, glutamate, GABA, AMPA receptors, GABA receptors, c-fos, nucleus accumbens, prefrontal cortex, medial amygdala, lateral septum, arcuate nucleus, social attachment
- MeSH terms
- Animals, Behavior, Animal, Bicuculline, Arvicolinae, Gene Expression Regulation, Immunohistochemistry, Male, Pair Bond, Quinoxalines, Random Allocation, Reaction Time, Tyrosine 3-Monooxygenase, Genes, fos, Ventral Tegmental Area, Excitatory Amino Acid Antagonists, GABA Antagonists
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