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Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles
Abstract
Although oxytocin (OT) and dopamine (DA) have been implicated in pair bond formation in monogamous prairie voles (Microtus ochrogaster), the nature of potential interactions between these two neurochemical systems and the brain circuits important for such interactions in the regulation of pair bonding have not been explored. Here, we demonstrated that access to both OT and DA D2-type receptors is necessary for pair bond formation, as blockade of either type of receptor prevented partner preferences induced by OT or a D2-type agonist. We also demonstrated that the nucleus accumbens (NAcc) is a brain area important for such OT-DA interactions. In NAcc, blockade of OT receptors prevented partner preferences induced by a D2-type agonist whereas blockade of D2-type, but not D1-type, DA receptors blocked OT-induced partner preferences. Together, our data suggest that concurrent activation of OT and DA D2-type receptors in NAcc is essential for pair bond formation in female prairie voles.
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In the citing paper
“It acts as learning signal, helping to imprint details of the partner and to associate those details with positive emotions and relationship-promoting habits (Aragona et al. 2006; Liu and Wang 2003; Curtis et al. 2006).”
From Natural Selection, Childrearing, and the Ethics of Marriage (and Divorce): Building a Case for the Neuroenhancement of Human Relationships (2012) · cites this paper as Liu and Wang 2003
In the citing paper
“whereas the direct injection of OXT into the NAcc (7) does so in females”
From Oxytocin enhances brain reward system responses in men viewing the face of their female partner (2013) · cites this paper as [7]
In the citing paper
“Supporting the notion that OXT-DA interactions might contribute to the OXT-induced effects on social bonding (Young et al., 2014), the systemic administration of a dopaminergic antagonist effectively blocked the partner preference induced by OXT in female prairie voles (Liu and Wang, 2003).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Liu and Wang, 2003
In the citing paper
“the effects of OT on partner preference in females could be located in the nucleus accumbens and in the prefrontal cortex, but these studies did not include males”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Liu and Wang, 2003
In the citing paper
“In addition, OT injected into the NAC is sufficient to induce pair bonds in female prairie voles in the absence of mating, and interacts with DA D2R to do so (Liu and Wang 2003).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Liu and Wang 2003
In the citing paper
“In monogamous but not polygamous vole species, oxytocin receptors are found in the nucleus accumbens, a neural center associated with reward and reinforcement (Liu and Wang, 2003).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Liu and Wang, 2003
In the citing paper
“In addition to the AVP and OT systems, the neurotransmitter dopamine DA, acting within the NAcc, plays a critical role in social bond formation in both male and female prairie voles [24, 25].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [24]
In the citing paper
“Dopamine (DA) acting on D2, but not on D1, receptors in the nucleus accumbens (NAc) promotes partner preference formation in both male and female prairie voles”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Liu and Wang 2003
In the citing paper
“several studies have characterized the role of intra-NAc OR activation in facilitating partner preference formation in female, but not male, prairie voles”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Liu and Wang 2003
In the citing paper
“It appeared that endogenous vasopressin, and not OT, regulated pair bonding in male prairie voles by acting at V1aR receptors in the ventral pallidum and lateral septum (Lim et al., 2004b; Lim and Young, 2004; Liu and Wang, 2003).”
From Central oxytocin receptors mediate mating-induced partner preferences and enhance correlated activation across forebrain nuclei in male prairie voles (2016) · cites this paper as Liu and Wang, 2003
In the citing paper
“Dopamine is released in the NAcc during mating and an intra-NAcc shell injection of dopamine 2 receptor antagonist inhibit mating-induced partner preference or partner preference induced by OT treatment (Aragona et al. 2003; Liu and Wang 2003; Wang et al. 1999).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Liu and Wang 2003
In the citing paper
“Dopamine is released in the NAcc during mating and an intra-NAcc shell injection of dopamine 2 receptor antagonist inhibit mating-induced partner preference or partner preference induced by OT treatment (Aragona et al. 2003; Liu and Wang 2003; Wang et al. 1999).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Liu and Wang 2003
In the citing paper
“Pair bond development is influenced by dopaminergic activity within the nucleus accumbens (Liu and Wang, 2003, Young et al., 1998).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Liu and Wang, 2003
In the citing paper
“For instance, it appears that both D2 receptors and oxytocin receptors must be stimulated in order to facilitate the formation of partner preferences (Liu and Wang, 2003).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Liu and Wang, 2003
In the citing paper
“Injection of a D2-receptor antagonist into the nucleus accumbens of female prairie voles can prevent partner preference formation induced by oxytocin and oxytocin antagonists can block partner preference formation induced by D2-receptor agonist administration (Liu and Wang, 2003).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Liu and Wang, 2003
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“Work in rodents has shown consistently that dopamine and oxytocin can interact [37] and in humans oxytocin can increase generosity, possibly by inducing striatal dopamine release [38] suggesting that dopamine and oxytocin may interact to determine Figure 2.”
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The neural circuits of monogamous behavior
López-Gutiérrez, M. F., Mejía-Chávez, S., Alcauter, S., & Portillo, W. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.978344 · Cited by 12
“…of vole pair-bonding behavior through the pharmacological manipulation of only a single region (NAcc, VP, or LS) (Liu et al., 2001; Liu and Wang, 2003; Lim and Young, 2004; Ross et al., 2009b; Barrett et al., 2013; Anacker et al., 2016) also imply that the whole circuit needs to be intact…”
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CART peptide following social novelty in the prairie vole (Microtus ochrogaster)
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“…of DA receptor type 2 and OTR binding within the nucleus accumbens (NAc), a node of the SDMN, is necessary for encoding partner-specific social stimuli as rewarding and promoting the formation of a pair bond in the prairie vole [Aragona et al., 2003; Liu and Wang, 2003; Johnson et al., 2017].”
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“Given that pair bond formation is dependent upon dopaminergic reward pathways in the NAc (Wang et al., 1999; Gingrich et al., 2000; Liu and Wang, 2003; Aragona et al., 2003), it is possible that pair bonding may function as a natural reward, leading to an upregulation of fosB in this region.”
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“, 2006), whereas blockade of dopamine in the nucleus accumbens prevents the development of a partner preference (Liu and Wang, 2003) and decreases time spent with a familiar partner over an unfamiliar partner (Aragona et al.”
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“This role of OT, modulating dopamine function during song learning and song production, would be consistent with evidence in mammals that OT modulates midbrain dopamine to promote social behaviors (Charlet &Grinevich, 2017; Liu &Wang, 2003).”
ResultBerendzen, K. M., Bales, K. L., & Manoli, D. S. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105339 · Cited by 10
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“In female prairie voles, blockade of the NAc oxytocin receptor prevents partner preferences induced by quinpirole, a D2 receptor agonist [101].”
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“Pair bonding observed in female prairie voles is also driven through Oxt in the ACB along with dopamine receptor 2 (Liu and Wang, 2003; Borie et al., 2022).”
BackgroundForero, S. A., Sailer, L. L., Girčytė, A., Madrid, J. E., Sullivan, N., & Ophir, A. G. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105351 · Cited by 11
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“…(AVP) and oxytocin (OT), can facilitate close ocial attachment to enhance the reward value by co-activating he dopaminergic circuits that are involved in motivation and eward, which leads to social-bond formation (Liu and Wang, 2003; elgado, 2007; Skuse and Gallagher, 2009; Wang et al., 2017).”
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“The dopamine receptor antagonist haloperidol blocks partner preference formation in prairie vole mates (Wang et al., 1999), and activation of both dopamine and oxytocin receptors is necessary for pair bond formation (Liu and Wang, 2003).”
BackgroundPrairie voles as a model for adaptive reward remodeling following loss of a bonded partner
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Does the Amygdala Mediate Oxytocin Effects on Socially Reinforced Learning?
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Comparative neurobiology and genetics of mammalian social behavior
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Metadata
- Authors
- Liu, Y., & Wang, Z. X.
- Affiliations
- Florida State University (US)
- Corresponding author
- Wang, Z.X
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2003-10
- Volume
- 121
- Issue
- 3
- Pages
- 537-544
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2147762584
- Cited by
- 580
- References
- 47
- Citations by year
- 2026: 21 · 2025: 25 · 2024: 20 · 2023: 15 · 2022: 33 · 2021: 25 · 2020: 76 · 2019: 23 · 2018: 27 · 2017: 39 · 2016: 33 · 2015: 36 · 2014: 33 · 2013: 35 · 2012: 17
- FWCI
- 13.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r29mh054554-06)
- National Institute of Mental Health (MH 58616, MH54554, MH-66734, R21MH066734, R01MH058616)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › 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
- oxytocin, dopamine, pair bonding, nucleus accumbens, dopamine D2 receptor, dopamine D1 receptor, mate preferences, monogamy, Microtus ochrogaster, receptor antagonism
- MeSH terms
- Animals, Behavior, Animal, Benzazepines, Arvicolinae, Dopamine, Dose-Response Relationship, Drug, Drug Administration Routes, Drug Interactions, Female, Hormone Antagonists, Male, Microinjections, Nucleus Accumbens, Oxytocin, Pair Bond, Salicylamides, Stereotaxic Techniques, Time Factors, Infusion Pumps, Implantable, Dopamine Agonists, Dopamine Antagonists, Quinpirole
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