The DOI matches its Crossref record; 48 of the 48 references it cites were found in a registry or an index.
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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“…at the dose of 1.0 ng in the NAcc increased the time that female prairie voles spent with a partner compared with the time that they spent with a stranger (Liu and Wang, 2003) Thus, OT or OTR-A microinjection at different doses in the NAcc and amygdala induces different effects on social behaviors.”
BackgroundResultInfluentialBaby Love? Oxytocin-Dopamine Interactions in Mother-Infant Bonding
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“Oxytocin release increases in the nucleus accumbens in female voles during pairing (15), although the source of oxytocin was not reported, and coactivation of dopamine and oxytocin in the nucleus accumbens facilitates pair bonding in female prairie voles (16).”
BackgroundThe effects of oxytocin on social reward learning in humans
Clark-Elford, R., Nathan, P. J., Bonnie Auyeung, B., Voon, V., Sule, A., Müller-Sedgwick, U., Dudas, R. B., Sahakian, B. J., Phan, K. L., & Baron‐Cohen, S. (2013) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145713001120 · Cited by 35
“Complimentary evidence also suggests that both oxytocin and dopamine are necessary for such partner formation and that these interactions are regulated in the NAcc (Young et al., 2001; Liu and Wang, 2003).”
BackgroundOpioid receptor function in social attachment in young domestic fowl
Warnick, J. E., McCurdy, C. R., & Sufka, K. J. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.12.009 · Cited by 35
Pharmacotherapy for Neuropsychiatric Symptoms in Frontotemporal Dementia
Le, C., & Finger, E. (2021) · CNS Drugs · doi:10.1007/s40263-021-00854-5 · Cited by 26
Oxytocin And Individual Variation in Parental Care in Prairie Voles
Olazábal, D. E., & Young, L. J. (2008) · Elsevier eBooks · doi:10.1016/b978-0-12-374285-8.00021-4 · Cited by 35
Familiarity and Mate Preference Assessment with the Partner Preference Test
Beery, A. K. (2021) · Current Protocols · doi:10.1002/cpz1.173 · Cited by 39
Banerjee, S. B., Dias, B. G., Crews, D. P., & Adkins–Regan, E. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12378 · Cited by 39
Samuel, S., Hayton, B. C., Gold, I., Feeley, N., Carter, C. S., & Zelkowitz, P. (2015) · Attachment & Human Development · doi:10.1080/14616734.2015.1029951 · Cited by 37
“Through a bio-behavioral feedback mechanism, women with lower levels of OT may be less likely to approach others (Francis et al., 2000) or to view their social interactions as rewarding (Carter, 1998; Liu & Wang, 2003; Pedersen, 1997; Strathearn et al., 2009).”
BackgroundInterplay between the oxytocin and opioid systems in regulating social behaviour
Putnam, P. T., & Chang, S. W. C. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0050 · Cited by 34
“Both the opioid and oxytocin systems have been demonstrated to interact with dopaminergic circuits in pair-bonding behaviours [100,152,153], leading to a theorized tripartite link between these systems [154].”
BackgroundInteractions of Oxytocin and Dopamine—Effects on Behavior in Health and Disease
Petersson, M., & Uvnäs‐Moberg, K. (2024) · Biomedicines · doi:10.3390/biomedicines12112440 · Cited by 44
“Additionally, when a dopaminergic antagonistic was administered, the effects of oxytocin on partner preference in female prairie voles were diminished [49].”
Wang, B., Li, Y., Wu, R., Zhang, S., & Tai, F. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.11.013 · Cited by 34
“The simultaneous increases in OTR and DR mRNA expression in the Nacc of new fathers suggest an interaction in this brain region, as proposed previously (Kovacs et al., 1990; Liu and Wang, 2003).”
The role of dopamine signaling in prairie vole peer relationships
Lee, N. S., & Beery, A. K. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104876 · Cited by 34
Sexuality during the climacteric period
Lara, L. A. D. S., Useche, B., Silva, J. C. R. E., Ferriani, R. A., dos Reis, R. M., de Sá, M. F. S., de Carvalho, B. R., Carvalho, M. Â. C. R., & Silva, A. C. J. D. S. R. E. (2009) · Maturitas · doi:10.1016/j.maturitas.2008.12.014 · Cited by 34
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Self-citationA unified circuit for social behavior
Modi, M. E., & Şahin, M. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.08.010 · Cited by 36
Comparative role of reward in long-term peer and mate relationships in voles
Goodwin, N. L., Lopez, S., Lee, N. S., & Beery, A. K. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.10.012 · Cited by 35
“While oxytocin receptor (OTR), vasopressin V1a receptor, and dopamine receptor antagonists can each block PP formation independently, concurrent activation of OTR and dopamine D2 receptors in the NAcc are necessary for partner preference formation in mates (Liu and Wang, 2003).”
BackgroundShih, H.-C., Kuo, M.-E., Wu, C., Chao, Y.-P., Huang, H.-W., & Huang, C.-M. (2022) · Brain Sciences · doi:10.3390/brainsci12070830 · Cited by 32
“Liu’s (2003) study has shown that the activation of oxytocin and dopamine D2-type receptors in the NA, a strong projection target of the VTA, is essential for pair bond formation [62].”
BackgroundNucleus accumbens dopamine release reflects the selective nature of pair bonds
Pierce, A. F., Protter, D. S. W., Watanabe, Y. L., Chapel, G. D., Cameron, R. T., & Donaldson, Z. R. (2024) · Current Biology · doi:10.1016/j.cub.2023.12.041 · Cited by 36
Consequences of prenatal exposure to valproic acid in the socially monogamous prairie voles
Sailer, L. L., Duclot, F., Wang, Z., & Kabbaj, M. (2019) · Scientific Reports · doi:10.1038/s41598-019-39014-7 · Cited by 31
Self-citationHelping behavior in prairie voles: a model of empathy and the importance of oxytocin
Kitano, K., Yamagishi, A., Horie, K., Nishimori, K., & Sato, N. (2022) · iScience · doi:10.1016/j.isci.2022.103991 · Cited by 31
“Especially in mice, previous studies indicated that oxytocin gene knockout caused a lack of social recognition (Bielsky and Young, 2004; Ferguson et al., 2001), formation of social bonds (Liu and Wang, 2003; Young and Wang, 2004), and social rewards (Dölen et al., 2013; Hung et al., 2017).”
Romantic love evolved by co-opting mother-infant bonding
Bode, A. (2023) · Frontiers in Psychology · doi:10.3389/fpsyg.2023.1176067 · Cited by 32
“However, it has been demonstrated that concurrent oxytocin (i.e., to OXTR) and dopamine (i.e., to D2R) signaling is required for pair bond formation in female prairie voles (Liu and Wang, 2003).”
BackgroundInoue, K., Burkett, J. P., & Young, L. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.03.035 · Cited by 33
“…and NAcsh show significantly higher density of the MOR protein in prairie voles than in meadow voles, as each of these regions has been implicated in species-specific pair bonding in prairie voles (Liu and Wang, 2003, Lim et al., 2004, Lim et al., 2007, Ross et al., 2009, Burkett et al., 2011).”
BackgroundStress impairs new but not established relationships in seasonally social voles
Anacker, A. M. J., Reitz, K. M., Goodwin, N. L., & Beery, A. K. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.01.004 · Cited by 32
Weitekamp, C. A., Nguyen, J. M., & Hofmann, H. A. (2017) · Genes Brain & Behavior · doi:10.1111/gbb.12389 · Cited by 35
“An interaction between these pathways in the POA has been reported for regulating pair bonding and maternal care in rodents (Liu & Wang 2003; Numan & Stolzenberg 2009).”
BackgroundRío, R. T.-D., Tecamachaltzi-Silvarán, M. B., Díaz-Estrada, V. X., Herrera‐Covarrubias, D., Corona-Morales, A. A., Pfaus, J. G., & Coria‐Ávila, G. A. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.01.019 · Cited by 33
Angioni, L., Cocco, C., Ferri, G., Argiolas, A., Melis, M. R., & Sanna, F. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.05.012 · Cited by 31
“Accordingly, a physiological role of this neuropeptide is thought to occur in the control of different behaviors, from sexual behavior and food consumption to empathy, social and affective behaviors (Argiolas and Melis, 2013, Crespi, 2015; Feeser et al., 2012; Liu and Wang, 2003; Lin, 2012; Parker and Bloom, 2012; Gil…”
BackgroundThe role of orgasm in the development and shaping of partner preferences
Coria‐Ávila, G. A., Herrera‐Covarrubias, D., Ismail, N., & Pfaus, J. G. (2016) · Socioaffective Neuroscience & Psychology · doi:10.3402/snp.v6.31815 · Cited by 30
“In the NAc, there is a simultaneous interaction of DA and OT during the formation of partner preferences, since blockade of either receptor with infusions of antagonists prevents the development of pairbonds induced by copulation (Liu & Wang, 2003; Young, Lim, Gingrich, & Insel, 2001).”
BackgroundMooney, S. J., Coen, C. W., Holmes, M. M., & Beery, A. K. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.06.043 · Cited by 30
“…oxytocin binding in certain regions, particularly the nucleus accumbens, is crucial to the maintenance of monogamous attachments (Young et al., 2001; Liu and Wang, 2003), suggesting a potentially broad functional significance to species differences in the anatomical distribution of this receptor.”
Normandin, J. J., & Murphy, A. Z. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.02.006 · Cited by 30
“In addition, OT in the accumbens is critical for the expression of mating-induced pair-bonding in female voles (Liu and Wang, 2003) and magnocellular oxytocinergic PVN”
Drinking alcohol has sex-dependent effects on pair bond formation in prairie voles
Anacker, A. M. J., Ahern, T. H., Hostetler, C. M., Dufour, B. D., Smith, M. L., Cocking, D. L., Li, J., Young, L. J., Loftis, J. M., & Ryabinin, A. E. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320879111 · Cited by 28
Neural Circuits Underlying Rodent Sociality: A Comparative Approach
Lee, N. S., & Beery, A. K. (2019) · Current topics in behavioral neurosciences · doi:10.1007/7854_2018_77 · Cited by 31
Meng, P., Li, C., Duan, S., Ji, S., Xu, Y., Mao, Y., Wang, H., & Tian, J. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.848251 · Cited by 31
“, 1989) and that OT-DA interactions are mediated by specific types of DA receptors (D2-DA receptor) in the regulation of social bonding (Liu and Wang, 2003).”
BackgroundRío, R. T.-D., Montero-Domínguez, F. Á., Llanderal, T. C., Tecamachaltzi-Silvarán, M. B., García, L. I., Manzo, J., Hernández‐Aguilar, M. E., & Coria‐Ávila, G. A. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.06.006 · Cited by 31
Aggression: Perspectives from social and systems neuroscience
Kelly, A. M., & Wilson, L. C. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.04.010 · Cited by 29
“…from assessment of V1aRs in the ventral-striato pallidum, blockade of OTRs in a key node of the pairbonding circuit, the nucleus accumbens (NAcc), prevents pairbonding, and overexpression of OTRs in this region facilitates pairbonding in female prairie voles (Liu and Wang, 2003; Ross et al., 2009).”
BackgroundResultFriend of the Devil: Negative Social Influences Driving Substance Use Disorders
Pomrenze, M. B., Paliarin, F., & Maiya, R. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.836996 · Cited by 27
Role of Oxytocin in Different Neuropsychiatric, Neurodegenerative, and Neurodevelopmental Disorders
Ghazy, A. A., Soliman, O., Elbahnasi, A. I., Alawy, A. Y., Mansour, A. M., & Gowayed, M. A. (2022) · Reviews of physiology, biochemistry and pharmacology · doi:10.1007/112_2022_72 · Cited by 27
Young, K. A., Liu, Y., Gobrogge, K. L., Dietz, D. M., Wang, H., Kabbaj, M., & Wang, Z. (2011) · Brain Research · doi:10.1016/j.brainres.2010.09.109 · Cited by 27
Self-citationOxytocin receptor behavioral effects and cell types in the bed nucleus of the stria terminalis
Luo, P. X., Zakharenkov, H. C., Torres, L. Y., Rios, R. A., Gegenhuber, B., Black, A. M., Xu, C. K., Minie, V. A., Tran, A. M., Tollkuhn, J., et al. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105203 · Cited by 27
Day, N. F., Saxon, D., Robbins, A., Harris, L., Nee, E., Shroff-Mehta, N., Stout, K., Sun, J., Lillie, N., Burns, M., et al. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.191510 · Cited by 27
Mitchell, I., Gillespie, S. M., & Abu-Akel, A. M. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.018 · Cited by 27
Maninger, N., Hinde, K., Mendoza, S. P., Mason, W. A., Larke, R. H., Ragen, B., Jarcho, M. R., Cherry, S. R., Rowland, D. J., Ferrer, E. E., et al. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.02.028 · Cited by 27
“In brief, pair bond formation is associated with the release of the peptide hormones oxytocin (OT) and vasopressin (AVP) from the hypothalamus (Winslow et al., 1993, Cho et al., 1999, Liu and Wang, 2003, Ross et al., 2009).”
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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