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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OT fibers in the NAcc have been mentioned previously in rats using immunohistochemistry and radioimmunoassay.
“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]
Monogamous male prairie voles have elevated levels of vasopressin after mating, leading to territoriality and partner protection.
“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
ICV injections of OTR antagonist failed to inhibit partner preference in male prairie voles, but injections into the lateral septum did.
“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
AVP expression within the BST and CMA is involved in a number of social behaviors, including social play behavior.
“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]
Vasopressin facilitates selective aggression or mate guarding behaviour in male prairie voles.
“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]
ICV V1aR antagonist impaired partner preference formation in male prairie voles, but had no effect in females.
“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 rodents, the VP system regulates partner preference in prairie voles in sex-specific ways.
“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
ICV OT administration facilitated partner preference formation in female, but not male, prairie voles.
“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
OT plays a stronger role in partner preference in female prairie voles compared to males.
“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
ICV V1aR antagonist administration impaired partner preference in male voles only.
“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
Pair bonding in prairie voles is operationally defined by two observable behaviors: partner preference and selective aggression.
“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 male prairie voles, AVP plays a critical role in the regulation of partner preferences.
“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]
Increased AVP signaling, especially in the ventral pallidum and lateral septum, is a prerequisite for partner preference formation and expression in male prairie voles.
“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
A single seminal paper failed to show that oxytocin receptor blockade inhibits mating-induced partner preferences in male prairie voles.
“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
Previous work suggested that the central OT system may modulate pair bonding in prairie voles in a sex-specific manner, with central OTRs modulating pair bonding in females but not in males.
“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
A single pharmacological study using a less selective OTA and relatively small sample sizes (n=6-8 per group) failed to demonstrate an effect of OTA on male pair bonding.
“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 addition to the critical role of AVP in partner-preference formation, it is also highly involved in other male-typic behavior, including aggression and courtship.
“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
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).
“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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“As earlier studies have shown that the effects of vasopressin on pair-bonding behavior differ between sexes (20), all analyses were performed for men and women separately.”
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“These activations are indicated with the superscript ‘e’ in Table 1 to highlight common activation for Partner and CF effects.”
BackgroundIs social attachment an addictive disorder?
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“This suggests that the efferent pathway from the MPOA to the VTA is critical for maternal care.”
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BackgroundSex differences in oxytocin and vasopressin: Implications for autism spectrum disorders?
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Self-citationThe neurobiology of pair bonding: Insights from a socially monogamous rodent
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“1A) is accompanied by selective aggression toward unfamiliar conspecifics [8,99,100,124,223,224,231].”
MethodInfluentialRomantic love: a mammalian brain system for mate choice
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Cerebrospinal Fluid Vasopressin Levels
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“Centrally acting arginine vasopressin (AVP) has been reported to have a facilitatory role for aggression in the golden hamster,(13-18) in rats,(19-21) and in prairie voles.(22) In the case of hamsters, injections of AVP into either the anterior(15,16,18) or ventrolateral(17) hypothalamus turns on aggressive display be…”
BackgroundInfluentialRole of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster).
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“, 1995), where a number of neuropeptides controlling sexual behavior are present (Wehrenberg et al., 1989; DeVries, 1990; Kalra et al., 1990; Kawata et al., 1991; Albers et al., 1992; Andersen et al., 1992; King and Millar, 1992; Sherwood et al., 1993; Winslow et al., 1993; Moore et al., 1994), suggests that some of t…”
The neural mechanisms and circuitry of the pair bond
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“Prior to pair bonding, male prairie voles show little aggression toward strangers; however, following successful pair bond formation, male prairie voles (and sometimes females) will actively attack strangers including sexually receptive females (Aragona et al., 2006; Gobrogge et al., 2007; Insel et al., 1995; Wang et…”
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“Early research in male prairie voles suggested that arginine vasopressin (AVP, which is structurally similar to OT), but not OT, regulated the development of partner preferences following mating (Winslow et al., 1993).”
BackgroundResultInfluentialBielsky, I. F., Hu, S.-B., Ren, X., Terwilliger, E. F., & Young, L. J. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.031 · Cited by 367 · see citing works
Developmental consequences of oxytocin
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“In prairie voles, sexual experience can hasten the onset of selective partner preferences [119] and in males induces aggression toward strangers [121].”
BackgroundSelf-citationA critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles
Aragona, B. J., Liu, Y., Curtis, J. T., Stephan, F. K., & Wang, Z. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03483.2003 · Cited by 351 · see citing works
“Vasopressin (Winslow et al., 1993; Cho et al., 1999; Liu et al., 2001), oxytocin (Williams et al.”
BackgroundInfluentialdo Rego, J. L., Seong, J. Y., Burel, D., Leprince, J., Luu-The, V., Tsutsui, K., Tonon, M., Pelletier, G., & Vaudry, H. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.006 · Cited by 356 · see citing works
Infant vocalization, adult aggression, and fear behavior of an oxytocin null mutant mouse
Winslow, J. T., Hearn, E. F., Ferguson, J., Young, L. J., Matzuk, M. M., & Insel, T. R. (2000) · Hormones and Behavior · doi:10.1006/hbeh.1999.1566 · Cited by 348 · see citing works
Self-citationRoss, H. E., Freeman, S. M., Spiegel, L. L., Ren, X., Terwilliger, E. F., & Young, L. J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5039-08.2009 · Cited by 322 · see citing works
“In male prairie voles, vasopressin plays a critical role in the display of paternal behavior as well as partner preference formation, paralleling the role of oxytocin in females (Winslow et al., 1993; Wang et al., 1994).”
BackgroundGenetics of Human Social Behavior
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Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole
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Characterization of the oxytocin system regulating affiliative behavior in female prairie voles
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“The role of OT in facilitating partner preference in male prairie voles is not clear, as one study found that OT or OT antagonist administered ICV did not effect partner preference formation (Winslow et al., 1993); while another lab found central OT infusion in males did facilitate partner preference formation (Cho et…”
BackgroundSex-specific influences of vasopressin on human social communication
Thompson, R. R., George, K., Walton, J. C., Orr, S. P., & Benson, J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600406103 · Cited by 312 · see citing works
The social deficits of the oxytocin knockout mouse
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“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…”
Sensory, hormonal, and neural control of maternal aggression in laboratory rodents
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“[240] Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR.”
BackgroundPitkow, L. J., Sharer, C. A., Ren, X., Insel, T. R., Terwilliger, E. F., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07392.2001 · Cited by 295 · see citing works
“Conversely, central infusions of AVP facilitate partner-preference formation even in the absence of mating (Winslow et al., 1993).”
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The Interpersonal Dimension of Borderline Personality Disorder: Toward a Neuropeptide Model
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Oxytocin, vasopressin and pair bonding: implications for autism
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“Additionally, prairie voles show selective aggression towards novel conspecifics after becoming sexually experienced (Winslow et al. 1993).”
BackgroundAlbers, H. E. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.10.007 · Cited by 288 · see citing works
“Further support for this hypothesis has come from studies in male prairie voles where aggression is influenced by an individual's prior social experience (Winslow et al., 1993).”
BackgroundBester‐Meredith, J. K., Young, L. J., & Marler, C. A. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1522 · Cited by 285 · see citing works
Brain vasopressin is an important regulator of maternal behavior independent of dams’ trait anxiety
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“ABN Dam on A B VEH (8) (7) AVP-R-AS (9)”
BackgroundThe prairie vole: An emerging model organism for understanding the social brain
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Neuropeptides and the evolution of social behavior
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The genetic basis of parental care evolution in monogamous mice
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“Partner Preference Testing This is an operational index of pair-bond formation (55), used extensively with prairie voles to investigate the effects of hormones and early experience on pair-bonding (4,35,56,57).”
Neuroendocrine bases of monogamy
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Self-citationModular Genetic Control of Sexually Dimorphic Behaviors
Xu, X., Coats, J., Yang, C. F., Wang, A., Ahmed, O. M., Alvarado, M., Izumi, T., & Shah, N. M. (2012) · Cell · doi:10.1016/j.cell.2011.12.018 · Cited by 266 · see citing works
“Individual genes can control complex behaviors as well as reflexive displays (Winslow et al., 1993; Brown et al., 1996; Scheller et al., 1983; Nishimori et al., 1996; Osborne et al., 1997; de Bono and Bargmann, 1998; Bendesky et al., 2011; Liu et al., 2011).”
Liu, Y., Curtis, J. T., & Wang, Z. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.4.910 · Cited by 282 · see citing works
“The partner preferences were assessed in a three-chamber apparatus as described previously (Williams et al., 1992; Winslow et al., 1993).”
MethodAlbeck, D. S., McKittrick, C. R., Blanchard, D. C., Blanchard, R. J., Nikulina, J., McEwen, B. S., & Sakai, R. R. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-12-04895.1997 · Cited by 261 · see citing works
“, 1993) and sexual (Winslow et al., 1993; Minerbo et al., 1994) behaviors in rodents.”
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“Arginine vasopressin (AVP), acting through the vasopressin 1a receptor (V1aR), shows similar effects, predominately in males (Winslow et al., 1993; Wang et al., 1994).”
Sex differences in the brain: The relation between structure and function
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“These changes, which do not occur in females, may precipitate mating-induced changes in aggression and social behavior, which indeed can be blocked with a VP antagonist (Winslow et al., 1993).”
BackgroundPrecision grips, hand morphology, and tools
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MALE PARENTAL BEHAVIOR IN BIRDS
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“The length of cohabitation required to form partner preferences is reduced in female prairie voles if the pair mates (Williams et al., 1992; Insel et al., 1995) or if exogenous OT is infused into the brain (Winslow et al., 1993b; Williams et al., 1994; Insel and Hulihan, 1995).”
InfluentialThe effects of stress on social preferences are sexually dimorphic in prairie voles.
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Self-citationMating in the monogamous male: Behavioral consequences
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Self-citation
- 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
- Social Sciences › Psychology › Social Psychology › 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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