The DOI matches its Crossref record; 24 of the 24 references it cites were found in a registry or an index.
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
Citations
Cites
Kleiman, D. G. (1977) · The Quarterly Review of Biology · doi:10.1086/409721 · Cited by 1,436
Review Lecture: Mammalian mating systems
Clutton-Brock, T. H. (1989) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1989.0027 · Cited by 1,418
Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles
Insel, T. R., & Shapiro, L. E. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.13.5981 · Cited by 833
Self-citationInsel, T. R. (1992) · Psychoneuroendocrinology · doi:10.1016/0306-4530(92)90073-g · Cited by 487
Self-citationWILLIAMS, J. (1992) · Hormones and Behavior · doi:10.1016/0018-506x(92)90004-f · Cited by 471
Getz, L. L., Carter, C. S., & Gavish, L. (1981) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00299829 · Cited by 466
Self-citationKruszynski, M., Lammek, B., Manning, M., Seto, J., Haldar, J., & Sawyer, W. H. (1980) · Journal of Medicinal Chemistry · doi:10.1021/jm00178a003 · Cited by 450
Modulation of social memory in male rats by neurohypophyseal peptides
Dantzer, R., Bluthe, R. M., Koob, G. F., & Le Moal, M. (1987) · Psychopharmacology · doi:10.1007/bf00518192 · Cited by 423
Changes in oxytocin and vasopressin secretion during sexual activity in men
MURPHY, M. R., SECKL, J. R., BURTON, S., CHECKLEY, S. A., & LIGHTMAN, S. L. (1987) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-65-4-738 · Cited by 318
Vasopressin injected into the hypothalamus triggers a stereotypic behavior in golden hamsters
Ferris, C. F., Albers, H. E., Wesolowski, S. M., Goldman, B. D., & Luman, S. E. (1984) · Science · doi:10.1126/science.6538700 · Cited by 255
Flagged first, then by citations
Research works printed but not linked: 3
- Dewsbury, D. A. in American Zoology Nebraska Symposium on Motivation (ed. Leger, D. W.) 1–50 (Univ. Nebraska Press, Lincoln, 1988).
- Jannett, F. J. Biologist 62, 3–19 (1980).
- Bamshad, M., Novak, M. & deVries, G. Soc. Neurosci. Abstr. 18, 152.10 (Soc. for Neuroscience, Anaheim, California, 1992).
Cited by
Sorted by citations
The oxytocin receptor system: structure, function, and regulation
Gimpl, G., & Fahrenholz, F. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.629 · Cited by 3,089
The neurobiology of pair bonding.
Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523
“Likewise, central AVP infusion facilitates pair-bond formation in male prairie voles without matin”
The neural correlates of maternal and romantic love
Bartels, A., & Zeki, S. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.11.003 · Cited by 1,497
Neuroendocrine perspectives on social attachment and love
Sue Carter, C. (1998) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00055-9 · Cited by 1,425
“Both male and female prairie voles become aggressive following sexual experience (Getz et al., 1981; Winslow et al., 1993), however, the onset of postcopulatory aggression is less predictable and slower in females.”
The neurobiology of attachment
Insel, T. R., & Young, L. J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35053579 · Cited by 1,173
“Indeed, all of the major behavioural aspects of monogamy can be facilitated in the prairie vole by central injections of either oxytocin or vasopressin, even in voles that do not have the opportunity to mat”
BackgroundSelf-citation
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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