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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“…accumbens) OT treatment, compared to artificial cerebrospinal fluid treatment, results in the formation of partner preference, an index of bond formation (Insel and Hulihan, 1995), in female prairie voles (Williams et al., 1992a; Insel and Hulihan, 1995; Cho et al., 1999; Liu and Wang, 2003).”
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“Blockade of either type of receptor inhibits pair bonds induced by activation of the other (Liu and Wang, 2003).”
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“Thus, neither of these systems serves as an upstream regulator of the other with respect to bond formation (77).”
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“Liu and Wang (2003) proposed that OT and dopamine may act on different aspects necessary for partner preference, where OT could be responsible for creating preference and OT would mediate the expression of this behaviour.”
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“Thus co-activation of D2R and OXTR in the striatum may be important for pair bond formation and its maintenance (Liu and Wang, 2003).”
BackgroundThe neurobiology of pair bond formation, bond disruption, and social buffering
Lieberwirth, C., & Wang, Z. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.05.006 · Cited by 72
Self-citationPathways Relating the Neurobiology of Attachment to Drug Addiction
Strathearn, L., Mertens, C. E., Mayes, L. C., Rutherford, H. J. V., Rajhans, P., Xu, G., Potenza, M. N., & Kim, S. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00737 · Cited by 79
“These systems all appear to play an important role in maternal behavior, pair-bond formation and social attachment (143, 144).”
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Oxytocin in the medial preoptic area facilitates male sexual behavior in the rat
Gil, M., Bhatt, R., Picotte, K. B., & Hull, E. M. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.12.012 · Cited by 70
“Mating-induced partner preference can be disrupted by intracerebroventricular (i.c.v.) administration of an oxytocin antagonist, whereas an oxytocin agonist promotes this behavior in the absence of copulation (Lim et al., 2004; Liu & Wang, 2003).”
InfluentialDeMayo, M. M., Song, Y. J. C., Hickie, I. B., & Guastella, A. J. (2017) · Pediatric Drugs · doi:10.1007/s40272-017-0248-y · Cited by 73
Effects of Oxytocin on Neural Response to Facial Expressions in Patients with Schizophrenia
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“Prior studies have suggested that biological function of oxytocin is moderated by dopaminergic system in animals (Bale et al, 2001; Liu and Wang, 2003).”
BackgroundMorales‐Medina, J. C., Dumont, Y., Benoit, C.-É., Bastianetto, S., Flores, G., Fournier, A., & Quirion, R. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.06.030 · Cited by 70
May oxytocin be a trait marker for bipolar disorder?
Turan, T., Uysal, C., Asdemir, A., & Kılıç, E. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.07.017 · Cited by 66
“There is evidence from recent animal studies suggesting that cells expressing hypothalamic oxytocin modulate dopamine receptors and that oxytocin and dopamine increase together in the same esponse to the treatment. brain regions (Liu and Wang, 2003; Smeltzer et al., 2006; Succu et al., 2007).”
Oxytocin and sex differences in behavior
Caldwell, H. K. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.02.002 · Cited by 68
The Cambridge Handbook of Substance and Behavioral Addictions
Sussman, S. Y. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108632591 · Cited by 64
Neuropeptidergic regulation of pair-bonding and stress buffering: Lessons from voles
Gobrogge, K. L., & Wang, Z. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.08.010 · Cited by 64
“Partner preference can be blocked with concurrent micro-injection of an OTR antagonist in the NAcc (Figure 1E) and prelimbic cortex (PLC), in the absence of mating (Liu & Wang, 2003, Young et al., 2001).”
BackgroundMethodInfluentialSelf-citationTargeting the Oxytocin System: New Pharmacotherapeutic Approaches
Gulliver, D. W., Werry, E. L., Reekie, T. A., Katte, T. A., Jorgensen, W. T., & Kassiou, M. (2018) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2018.11.001 · Cited by 67
“…OXTR and D 2 R signaling is a necessary component of pair-bond formation in the monogamous prairie vole, a widely studied model of social behavior, suggesting that OXTR-D 2 R heterodimers in the mesolimbic pathway have an important physiological role in mediating the prosocial effects of OT [15].”
Caldwell, H. K. (2012) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4614-1704-0_12 · Cited by 58
Ophir, A. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00397 · Cited by 66
“For example, manipulation of VP and its receptor (V1aR) in the ventral pallidum (VPall) or lateral septum (LS), and OT or its receptor (OTR) in the nucleus accumbens (NAcc) can either facilitate or diminish the pairbond (Winslow et al., 1993; Williams et al., 1994; Cho et al., 1999; Liu et al., 2001; Liu and Wang, 200…”
BackgroundLove-related changes in the brain: a resting-state functional magnetic resonance imaging study
Song, H., Zou, Z., Kou, J., Liu, Y., Yang, L., Zilverstand, A., Uquillas, F. D., & Zhang, X. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00071 · Cited by 64
Self-citationAversive motivation and the maintenance of monogamous pair bonding
Resendez, S. L., & Aragona, B. J. (2013) · Reviews in the Neurosciences · doi:10.1515/revneuro-2012-0068 · Cited by 58
Kohli, S., King, M. V., Williams, S. A., Edwards, A., Ballard, T. M., Steward, L. J., Alberati, D., & Fone, K. C. F. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0171-0 · Cited by 61
Lei, K., Liu, Y., Smith, A. S., Lonstein, J. S., & Wang, Z. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13673 · Cited by 59
Self-citationBateman, C., & Nacke, L. E. (2010) · International Academic Conference on the Future of Game Design and Technology (Futureplay) · doi:10.1145/1920778.1920780 · Cited by 66
“There may be interesting interactions between the reward system and the social centre yet to be studied, since research on prarie voles has shown that dopamine and oxytocin interactions are associated with pair bonding [39].”
BackgroundEffects of intranasal oxytocin on symptoms of schizophrenia: A multivariate Bayesian meta-analysis
Williams, D. R., & Bürkner, P. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.10.013 · Cited by 58
Current findings on the role of oxytocin in the regulation of food intake
Spetter, M. S., & Hallschmid, M. (2017) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.03.007 · Cited by 61
Althaus, M., Groen, Y., Wijers, A. A., Noltes, H., Tucha, O., & Hoekstra, P. J. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.10.025 · Cited by 57
“The pathways related to pro-social motivation and reward processing contain high levels of OXT receptors (Insel, 2003), while furthermore OXT has been shown to facilitate dopamine release in particularly the midbrain striatal nucleus accumbens (Liu and Wang, 2003).”
BackgroundThe Mesolimbic Dopamine Pathway and Romantic Love
Xu, X., Weng, X., & Aron, A. P. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-397025-1.00057-9 · Cited by 57
Oxytocin and opioid addiction revisited: old drug, new applications
Zanos, P., Georgiou, P., Weber, C. D., Robinson, F., Kouimtsidis, C., Niforooshan, R., & Bailey, A. (2017) · British Journal of Pharmacology · doi:10.1111/bph.13757 · Cited by 54
“Oxytocinergic interactions with the dopaminergic system in the brain were shown to underlie this pair bonding (Liu and Wang, 2003), indicating possible association between the oxytocinergic and dopaminergic systems to regulate behaviour.”
BackgroundMadrid, J. E., Parker, K. J., & Ophir, A. G. (2020) · Advances in the study of behavior · doi:10.1016/bs.asb.2020.02.001 · Cited by 55
“Similarly, in female prairie voles, OT administration in the NAcc induces a partner preference in the absence of mating, whereas pharmacological blockade prevents the formation of a mating-induced partner preference (Gobrogge & Wang, 2016; Liu & Wang, 2003).”
BackgroundNeuronal activation by stimuli that predict sexual reward in female rats
Coria‐Ávila, G. A., & Pfaus, J. G. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.05.052 · Cited by 55
Earp, B. D., Sandberg, A., & Savulescu, J. (2012) · Philosophy & Technology · doi:10.1007/s13347-012-0081-8 · Cited by 58
“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).”
BackgroundChang, W. H., Lee, I. H., Chen, K. C., Chi, M. H., Chiu, N.-T., Yao, W. J., Lu, R., Yang, Y. K., & Chen, P. S. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.05.020 · Cited by 54
Social touch during development: Long-term effects on brain and behavior
Bales, K. L., Witczak, L. R., Simmons, T. C., Savidge, L. E., Rothwell, E. S., Rogers, F. D., Manning, R., Heise, M. J., Englund, M., & Razo, R. A. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.019 · Cited by 59
A Neuroscientist’s Guide to the Vole
Kenkel, W. M., Gustison, M. L., & Beery, A. K. (2021) · Current Protocols · doi:10.1002/cpz1.175 · Cited by 52
Kelly, A. M., Ong, J. Y., Witmer, R. A., & Ophir, A. G. (2020) · Science Advances · doi:10.1126/sciadv.abb9116 · Cited by 55
“…plays a key role in modulating context-specific motivational states ( 27 , 28 ); (ii) nucleus accumbens (NAcc), which is crucial for pair bonding ( 29 ); (iii) HPC, which is important for social recognition and spatial and contextual learning and memory ( 30 ); and (iv) retrosplenial cortex…”
Oxytocin in health and disease
Tom, N., & Assinder, S. J. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.10.008 · Cited by 53
Mooney, S. J., Douglas, N. R., & Holmes, M. M. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.02.003 · Cited by 52
Thielke, L. E., & Udell, M. A. R. (2015) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12235 · Cited by 55
“This neurotransmitter has been shown to interact with OT to produce differences in maternal behaviour in rats (Shahrokh et al., 2010) and influences pair-bond formation behaviour in female prairie voles (Mircotus ochrogaster) (Liu & Wang, 2003).”
BackgroundAssociation between the oxytocin receptor (OXTR) gene and mesolimbic responses to rewards
Damiano, C. R., Aloi, J. M., Dunlap, K., Burrus, C. J., Mosner, M. G., Kozink, R. V., McLaurin, R. E., Mullette-Gillman, O. A., Carter, R., Huettel, S. A., et al. (2014) · Molecular Autism · doi:10.1186/2040-2392-5-7 · Cited by 56
“Additionally, OXT plays a key role in regulating dopaminergic activity in mesolimbic reward circuitry [40-43].”
BackgroundResultOxytocin and Eating Disorders: A Narrative Review on Emerging Findings and Perspectives
Giel, K. E., Zipfel, S., & Hallschmid, M. (2018) · Current Neuropharmacology · doi:10.2174/1570159x15666171128143158 · Cited by 58
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Duclot, F., Wang, H., Youssef, C., Liu, Y., Wang, Z., & Kabbaj, M. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.04.001 · Cited by 52
“Furthermore, central oxytocin injection facilitates the formation of partner preference, whereas OTR antagonism either centrally or in the NAcc prevents mating-induced partner preference (Cho et al., 1999; Liu and Wang, 2003; Williams et al., 1994).”
BackgroundSelf-citationOxytocin in the anterior cingulate cortex is involved in helping behaviour
Yamagishi, A., Lee, J., & Sato, N. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112790 · Cited by 53
Autism: Oxytocin, serotonin, and social reward
Dölen, G. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1087875 · Cited by 57
“This D2 agonist-induced partner preference requires activation of oxytocin receptors, and is absent if D2 agonists are administered in the presence of oxytocin receptor antagonists (Gingrich et al., 2000; Liu & Wang, 2003; Wang et al., 1999).”
BackgroundNeural circuits regulating sexual behaviors via the olfactory system in mice
Ishii, K. K., & Touhara, K. (2018) · Neuroscience Research · doi:10.1016/j.neures.2018.10.009 · Cited by 55
Rappeneau, V., & Castillo Díaz, F. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105675 · Cited by 51
“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).”
BackgroundComplexity of oxytocin׳s effects in a chronic cocaine dependent population
Lee, M. R., Glassman, M., King‐Casas, B., Kelly, D. L., Stein, E. A., Schroeder, J. R., & Salmeron, B. J. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2014.06.005 · Cited by 52
Vargas-Martínez, F., Uvnäs-Moberg, K., Petersson, M., Olausson, H. A., & Jiménez-Estrada, I. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.10.001 · Cited by 51
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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