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A role for central vasopressin in pair bonding in monogamous prairie voles
Abstract
Monogamous social organization is characterized by selective affiliation with a partner, high levels of paternal behaviour and, in many species, intense aggression towards strangers for defence of territory, nest and mate. Although much has been written about the evolutionary causes of monogamy, little is known about the proximate mechanisms for pair bonding in monogamous mammals. The prairie vole, Microtus ochrogaster, is a monogamous, biparental rodent which exhibits long-term pair bonds characterized by selective affiliation (partner preference) and aggression. Here we describe the rapid development of both selective aggression and partner preferences following mating in the male of this species. We hypothesized that either arginine-vasopressin (AVP) or oxytocin (OT), two nine-amino-acid neuropeptides with diverse forebrain projections, could mediate the development of selective aggression and affiliation. This hypothesis was based on the following observations: (1) monogamous and polygamous voles differ specifically in the distribution of forebrain AVP and OT receptors; (2) AVP innervation in the prairie vole brain is sexually dimorphic and important for paternal behaviour; (3) central AVP pathways have been previously implicated in territorial displays and social memory; and (4) central OT pathways have been previously implicated in affiliative behaviours. We now demonstrate that central AVP is both necessary and sufficient for selective aggression and partner preference formation, two critical features of pair bonding in the monogamous prairie vole.
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In the citing paper
“Although not shown in a photomicrograph, OT fibers in the NAcc have been mentioned previously in rats using immunohistochemisry [122] and radioimmunoassay [137].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [137]
In the citing paper
“Monogamous male prairie voles have elevated levels of the hormone vasopressin after mating, leading to territoriality and partner protection (Winslow, Hastings, Carter, Harbaugh, & Insel, 1993).”
From Birth of a Father: Fathering in the First 1,000 Days (2019) · cites this paper as Winslow et al., 1993
In the citing paper
“In support, ICV injections of OTR antagonist failed to inhibit partner preference in male prairie voles (Winslow et al., 1993), but injections into the lateral septum did (Liu et al., 2001).”
From Sex-specific modulation of juvenile social play by vasopressin (2013) · cites this paper as Winslow et al., 1993
In the citing paper
“AVP expression within the bed nucleus of the striaterminalis (BST) and the centromedial amygdala (CMA) is known to be involved in a number of social behaviors, [18][19][20] including social play behavior.21”
From Neonatal MeCP2 is important for the organization of sex differences in vasopressin expression (2012) · cites this paper as [18]
In the citing paper
“AVP also facilitates the expression of selective aggression, or mate guarding behaviour, in male prairie voles (7).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [7]
In the citing paper
“intracerebroventricular (ICV) V1aR antagonist impaired partner preference formation in males (Winslow et al., 1993), but there was no effect in females (Insel & Hulihan, 1995).”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Winslow et al., 1993
In the citing paper
“In rodents, sex-specific regulation of partner preference in prairie voles, social recognition in rats, social play in rats, and aggression in hamsters has been found”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Winslow et al., 1993
In the citing paper
“ICV OT administration facilitated partner preference formation in female (Williams et al., 1994; Insel and Hulihan, 1995), but not in male (Winslow et al., 1993) prairie voles.”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Winslow et al., 1993
In the citing paper
“OT plays a stronger role in partner preference in female prairie voles compared to males (Winslow et al., 1993; Williams et al., 1994; Insel and Hulihan, 1995; Liu et al., 2001).”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Winslow et al., 1993
In the citing paper
“ICV V1aR antagonist administration impaired partner preference in male voles only (Winslow et al., 1993; Insel & Hulihan, 1995)”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Winslow et al., 1993
In the citing paper
“Pair bonding in prairie voles is operationally defined based on two observable behaviors: preference for the partner over the stranger in a choice test (or “partner preference”); and intense aggression toward prairie voles other than the mate (or “selective aggression”) (Williams et al 1992; Winslow et al 1993; Insel et al 1995; Wang et al 1997b; Ahern et al 2009).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Winslow et al 1993
In the citing paper
“In male prairie voles, AVP plays a critical role in the regulation of partner preferences, although it is likely that OT also plays a role [18, 19].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [19]
In the citing paper
“Increased arginine-vasopressin (AVP) signaling, especially in the ventral pallidum (VP) and lateral septum (Liu et al. 2001), is a prerequisite for partner preference formation and expression in male prairie voles”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Winslow et al. 1993
In the citing paper
“a single seminal paper failed to show that OTR blockade inhibits mating induced partner preferences in males (Winslow and Insel, 1993).”
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 Winslow and Insel, 1993
In the citing paper
“Previous work has suggested that the central OT system may modulate pair bonding in prairie voles in a sex-specific manner (Insel and Hulihan, 1995; Winslow and Insel, 1993), with central OTRs modulating pair bonding in females but not in males.”
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 Winslow and Insel, 1993
In the citing paper
“A single pharmacological study, using a less selective OTA and relatively small sample sizes for experimental groups (n=6-8 per group), failed to demonstrate an effect of OTA on male pair bonding (Winslow and Insel, 1993)”
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 Winslow and Insel, 1993
In the citing paper
“In addition to the critical role of AVP in partner-preference formation (Winslow et al., 1993), it is also highly involved in other male-typic behavior, including aggression and courtship (Goodson and Bass, 2001).”
From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Winslow et al., 1993
In the citing paper
“First, oxytocin effects are moderated by robust, hard-wired neurobiological mechanisms; thus, centrally administered oxytocin increases aggression to same-sex intruders after mating in monogamous Prairie voles, but not in non-monogamous Montane voles (Winslow et al., 1993).”
From Approaching the biology of human parental attachment: Brain imaging, oxytocin and coordinated assessments of mothers and fathers (2014) · cites this paper as Winslow et al., 1993
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“Early in the study of prairie vole pair-bonding, oxytocin was deemed more important for partnership formation in females than in males, and vasopressinergic pathways became the focus of studies on male prairie voles.(43) In subsequent years, most studies have focused on neuropeptide, dopaminergic, and opioid signaling…”
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“Aggression is elevated following cohabitation with a mate; males housed with a female for 24 h exhibited significantly more strangerdirected aggression in a resident-intruder test than unmated males (Winslow et al., 1993; Insel et al., 1995; Wang et al., 1997).”
BackgroundQuintana, G. R., Cionnaith, C. E. M., & Pfaus, J. G. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23168928 · Cited by 23
Diethorn, E. J., & Gould, E. (2022) · Hippocampus · doi:10.1002/hipo.23476 · Cited by 26
Ragen, B., Mendoza, S. P., Mason, W. A., & Bales, K. L. (2012) · American Journal of Primatology · doi:10.1002/ajp.22026 · Cited by 21
“…hormones play a crucial role in pair-bond formation and maintenance in prairie voles [Carter, 1998; Donaldson and Young, 2008; Williams et al., 1994; Winslow et al., 1993], as well as monogamous primates [Jarcho et al., 2011; Seltzer and Ziegler, 2007; Smith et al., 2010a; Snowdon et al., 2010].”
BackgroundInhaled vasopressin increases sociability and reduces body temperature and heart rate in rats
Ramos, L., Hicks, C., Caminer, A., & McGregor, I. S. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.04.013 · Cited by 21
Liu, Y., Curtis, J. T., Fowler, C. D., Spencer, C. M., Houpt, T. A., & Wang, Z. X. (2001) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2001.00729.x · Cited by 21
“Furthermore, as forced swimming or corticosterone treatment influences pair bond formation differentially between male and female prairie voles (16), and vasopressin is implicated in the regulation of pair bonding in males ( 19 ) and oxytocin in females (20, 21), it has been hypothesized that swimming stress and the s…”
BackgroundHewlett, S. E., Wareham, D. M., & Barron, A. B. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.173054 · Cited by 22
“…social contact and interactions initiate the neural changes that lead to an enduring social attachment in prairie voles (Williams et al., 1994; Winslow et al., 1993; reviewed in Young and Wang, 2004), and social encounters are also essential for honey bee development and social organisation…”
BackgroundDiBenedictis, B. T., Cheung, H. K., Nussbaum, E. R., & Veenema, A. H. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.104462 · Cited by 21
“AVP signaling in the brain has been shown to be necessary for the display of many species-typical social behaviors including social recognition, aggression, social play, pair bonding and parental care (Winslow et al., 1993; Bamshad et al., 1994; Ferris et al., 1997; Albers et al., 2006; Veenema et al., 2010; Veenema e…”
BackgroundDuclot, F., Sailer, L. L., Koutakis, P., Wang, Z., & Kabbaj, M. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.11.022 · Cited by 20
Hunter, R. G., Lim, M. M., Philpot, K. B., Young, L. J., & Kuhar, M. J. (2005) · Brain Research · doi:10.1016/j.brainres.2005.04.032 · Cited by 21
“Previous studies have implicated the neurohypophyseal peptides vasopressin and oxytocin in the neural regulation of pair bond formation in prairie voles [50,51].”
Auger, C. J., & Vanzo, R. J. (2005) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2005.01400.x · Cited by 21
Neonatal exposure to the D1 agonist SKF38393 inhibits pair bonding in the adult prairie vole
Hostetler, C. M., Harkey, S. L., Krzywosinski, T. B., Aragona, B. J., & Bales, K. L. (2011) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32834affd2 · Cited by 19
“Animals were given a dyadic encounter test for intrasexual aggression (Winslow et al., 1993; Harper and Batzli, 1997; Bowler et al., 2002; Bales and Carter, 2003a).”
The Biology of Positive Emotions and Health
Marques, A. H., & Sternberg, E. M. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195182910.003.0012 · Cited by 20
Fakhoury, M. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.02.026 · Cited by 21
“…preclinical research has underscored the role of vasopressin in the regulation of complex social behaviors including social recognition (Bielsky et al., 2005, 2004), pair bond formation (Liu et al., 2001; Winslow et al., 1993), and aggression (Bosch and Neumann, 2010; Gutzler et al., 2010).”
BackgroundSociability and pair-bonding in gerbils: a comparative experimental study
Tchabovsky, A. V., Savinetskaya, L. E., Ovchinnikova, N. L., Safonova, A., Ilchenko, O. N., Sapozhnikova, S. R., & Vasilieva, N. A. (2018) · Current Zoology · doi:10.1093/cz/zoy078 · Cited by 18
“We have focused on male partner preferences as is common in such studies (Winslow et al. 1993; Lim et al. 2004; Ophir et al. 2008; Solomon et al. 2009; Mabry et al. 2011; Blocker and Ophir 2016) because sexual conflict theory predicts that males are more likely to desert their partners than females (Trivers 1972).”
BackgroundOxytocin, vasopressin, and the evolution of mating systems in mammals
Freeman, S. M., & Young, L. J. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139017855.011 · Cited by 19
Romantic love, pair-bonding, and the dopaminergic reward system.
Acevedo, B. P., & Aron, A. P. (2013) · American Psychological Association eBooks · doi:10.1037/14250-004 · Cited by 20
“These behaviors serve to initiate, maintain, and protect the pair-bond as eveidenced by research using animal models (e.g., Aragona et al., 2003; Carter, DeVries, & Getz, 1995; Wang, Hulihan, & Insel, 1997; Winslow et al., 1993).”
Arginine Vasotocin Preprohormone Is Expressed in Surprising Regions of the Teleost Forebrain
Rodriguez-Santiago, M., Nguyen, J. M., Winton, L. S., Weitekamp, C. A., & Hofmann, H. A. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00195 · Cited by 22
Burda, H. (1999) · Springer eBooks · doi:10.1007/978-94-011-4830-6_24 · Cited by 20
Sperm Competition and Mate Guarding in Meadow Voles (Microtus pennsylvanicus)
Storey, A. E., French, R. J., & Payne, R. H. (1995) · Ethology · doi:10.1111/j.1439-0310.1995.tb00364.x · Cited by 20
Oxytocin and vasopressin increase male-directed threats and vocalizations in female macaques
Jiang, Y., & Platt, M. L. (2018) · Scientific Reports · doi:10.1038/s41598-018-36332-0 · Cited by 20
Oxytocin and vasopressin in the hippocampus
Zăgrean, A., Georgescu, I.-A., Ieșanu, M. I., Ionescu, R.-B., Haret, R. M., Panaitescu, A. M., & Zăgrean, L. (2022) · Vitamins and hormones · doi:10.1016/bs.vh.2021.11.002 · Cited by 20
The psychobiology of human semen
Burch, R. L., & Gallup, G. G. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511617812.008 · Cited by 19
The magnocellular medial preoptic nucleus I. sources of afferent input
Wang, J., & Swann, J. M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.04.079 · Cited by 19
Towards meeting Tinbergen's challenge
Ophir, A. G. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.03.012 · Cited by 18
Neurobiology and the Evolution of Mammalian Social Behavior
Carter, C. S., & Porges, S. W. (2012) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199755059.003.0008 · Cited by 19
Self-citationAskew, A., González, F., Stahl, J. M., & Karom, M. C. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.08.001 · Cited by 19
Terleph, T. A., Jean‐Baptiste, N., & Bamshad, M. (2004) · Journal of Mammalogy · doi:10.1644/bns-108.1 · Cited by 19
“In addition, 1 day after mating a male develops a preference for affiliation with his mate as opposed to an unfamiliar female, an indication of pair bonding (Getz et al. 1981; Winslow et al. 1993).”
Hiura, L. C., & Ophir, A. G. (2018) · Integrative Zoology · doi:10.1111/1749-4877.12338 · Cited by 19
“Pair-bonded male prairie voles display aggression toward novel females (Winslow et al. 1993), and this selective aggression is mediated by VP activation of V1aR in the AH (Gobrogge et al.”
BackgroundFemale degus show high sociality but no preference for familiar peers
Insel, N., Shambaugh, K. L., & Beery, A. K. (2020) · Behavioural Processes · doi:10.1016/j.beproc.2020.104102 · Cited by 19
“novelty preferences that was originally developed to assess preferences for mates in socially monogamous prairie voles (Microtus ochrogaster) (e.g. Williams et al., 1992; Winslow et al., 1993).”
Kingsbury, M. A., Gleason, E. D., Ophir, A. G., Phelps, S. M., Young, L. J., & Marler, C. A. (2012) · Brain Behavior and Evolution · doi:10.1159/000339247 · Cited by 18
“…in prairie voles have been reported with regards to mating guarding [Winslow et al., 1993], neuropeptide induction of partner preference [Winslow et al., 1993; Devries et al., 1995; Insel and Hulihan, 1995], and the temporal parameters of partner preference formation [DeVries and…”
BackgroundAnacker, A. M. J., & Ryabinin, A. E. (2013) · Frontiers in Pharmacology · doi:10.3389/fphar.2013.00084 · Cited by 18
Dose-Dependent and Lasting Influences of Intranasal Vasopressin on Face Processing in Men
Price, D., Burris, D., Cloutier, A., Thompson, C. B., Rilling, J. K., & Thompson, R. R. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00220 · Cited by 18
“Even exogenous AVP’s effects on affiliative responses related to pair bonding in male prairie voles have only been examined immediately after manipulations of AVP that are concurrent with social interactions with females (16, 18).”
BackgroundKelly, A. M., Saunders, A. G., & Ophir, A. G. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.01.006 · Cited by 18
Stetzik, L. A., Ganshevsky, D., Lende, M. N., Roache, L. E., Musatov, S. A., & Cushing, B. S. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.05.035 · Cited by 19
“It should be noted that in prairie voles, both males and females display high levels of selective conspecific aggression following prolonged cohabitation/pair bond formation and/or mating, but low levels of territorial or premating aggression [10,11].”
InfluentialLeveraging a translational research approach to drive diagnostic and treatment advances for autism
Parker, K. J. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01532-8 · Cited by 19
Bales, K. L., & Rogers, F. D. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0061 · Cited by 17
“Aversion to novel same-sex animals is viewed asmate-guarding and part of behavioural maintenance of a pair bond in prairie voles [83].”
BackgroundOxytocin and vasopressin in non-human primates
Ragen, B., & Bales, K. L. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139017855.019 · Cited by 18
The Role of Females in Extrapair Copulations in Socially Monogamous Territorial Animals
Stamps, J. A. (1997) · Springer eBooks · doi:10.1007/978-1-4615-5985-6_12 · Cited by 18
Ontogeny of arginine vasopressin-like immunoreactivity in the Brazilian opossum brain
Iqbal, J., & Jacobson, C. D. (1995) · Developmental Brain Research · doi:10.1016/0165-3806(95)00097-w · Cited by 18
Monogamy, Motherhood, and Health
Carter, C. S. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195182910.003.0024 · Cited by 17
Self-citationBaran, N. M., Tomaszycki, M. L., & Adkins–Regan, E. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00058 · Cited by 20
“The present findings are thus consistent with decades of research in prairie voles demonstrating that AVT and V1aR are important for pairing in males (Winslow et al., 1993; Pitkow et al., 2001).”
ResultAn Attachment Theoretical Perspective on Tend-and-Befriend Stress Reactions
Levy, K. N., Hlay, J. K., Johnson, B. N., & Witmer, C. P. (2019) · Evolutionary Psychological Science · doi:10.1007/s40806-019-00197-x · Cited by 19
Lee, G., & Yoon, M. (2020) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2020.106482 · Cited by 17
Oztan, O., Zyga, O., Stafford, D. E. J., & Parker, K. J. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104870 · Cited by 18
“Approximately 15 years later, a “social” role for AVP was also identified: AVP was found to induce pair bonds in male prairie voles (Winslow et al., 1993), as well as paternal care in several vole species (Parker and Lee, 2001; Wang et al.”
BackgroundSex, Drugs, and Violence: Neuromodulation of Attachment and Conflict in Voles
Gobrogge, K. L. (2013) · Current topics in behavioral neurosciences · doi:10.1007/7854_2013_264 · Cited by 16
“Importantly, males display aggression not only toward conspecific males (Winslow et al. 1993; Insel et al. 1995; Wang et al. 1997a; Aragona et al. 2006; Gobrogge et al. 2007) but also toward sexually receptive females (Figs.”
Influential
Metadata
- Authors
- Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R.
- Affiliations
- National Institute of Mental Health (US)
- University of Maryland, College Park (US)
- Venue
- Nature
- Published
- 1993-10
- Volume
- 365
- Issue
- 6446
- Pages
- 545-548
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2043050293
- Cited by
- 948
- References
- 24
- Citations by year
- 2026: 20 · 2025: 19 · 2024: 20 · 2023: 22 · 2022: 30 · 2021: 29 · 2020: 35 · 2019: 26 · 2018: 34 · 2017: 38 · 2016: 32 · 2015: 38 · 2014: 38 · 2013: 49 · 2012: 55
- FWCI
- 25.01
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- vasopressin, pair bonding, monogamy, Microtus ochrogaster, mate preferences, oxytocin, neuropeptides, social behavior, sexual dimorphism
- MeSH terms
- Aggression, Animals, Arginine Vasopressin, Central Nervous System, Arvicolinae, Female, Male, Oxytocin, Sexual Behavior, Animal, Receptors, Oxytocin, Antidiuretic Hormone Receptor Antagonists
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