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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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“, prairie vole, Microtus ochrogaster (Winslow et al. 1993; Young et al. 2008); zebrafinch, Taeniopygia guttata (Goodson and Adkins-Regan 1999); convict cichlid, Amatitlania nigrofasciata (O’Connell et al.”
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“…immediate reproductive context, AVP plays a role in a number of other social behaviors, such as pair-bonding (Winslow, Hastings, Carter, Harbough, & Insel, 1993), parenting (Caldwell, Greer, Johnson, Prange, & Pedersen, 1987; Trainor & Marler, 2001; Wang & De Vries, 1993), and social recognition…”
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“Specifically, the impairment of partner preference displayed by male prairie voles in our study is notably opposite of the acute, facilitatory effects of AVP administration on partner preference formation (55) and social contact (73, 74) demonstrated in other studies.”
ResultEarly experience and the developmental programming of oxytocin and vasopressin
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“For example, OT is necessary for pair bond formation in female prairie voles [248], whereas AVP is necessary for this behavior to occur in males of the same species [249].”
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“in ventral pallidum, a region of reward circuitry that supports pairbond formation.(159,160) Antagonizing these pallidal receptors in prairie voles disrupts pair-bonding in males,(137) while overexpressing these”
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“AVP was first implicated in social bond formation and paternal care in voles [28, 60, 61].”
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López-Gutiérrez, M. F., Mejía-Chávez, S., Alcauter, S., & Portillo, W. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.978344 · Cited by 12
“…voles and NWP consisted of pharmacological manipulation of central OTR and AVPr activity, effectively impairing or enhancing pair-bonding behavior (Winslow et al., 1993; Williams et al., 1994; Insel et al., 1995b, 1998; Insel, 1997; Cho et al., 1999; Donaldson et al., 2010; Smith et al., 2010;…”
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“On the other hand, AVP has been found to facilitate pair bonds (Winslow et al., 1993; Liu et al., 2001; Gobrogge et al., 2009) and paternal caregiving behaviors in males (for a review, see Goodson and Bass, 2001).”
BackgroundCART peptide following social novelty in the prairie vole (Microtus ochrogaster)
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“, 2003) activate D2 receptors, leading to the formation of a pair bond, mating is not required for partner preference formation (Cho et al., 1999; Winslow et al., 1993).”
Forero, S. A., & Ophir, A. G. (2022) · Brain Behavior and Evolution · doi:10.1159/000522109 · Cited by 12
“, 2018] and notably after undergoing the life history transition of becoming pair bonded shortly after mating [Winslow et al., 1993].”
BackgroundHostetler, C. M., & Bales, K. L. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.03.019 · Cited by 11
“, 1997) and mating is not required to form a partner preference (Winslow et al., 1993; Cho et al., 1999).”
BackgroundDumais, K. M., & Veenema, A. H. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-802114-9.00011-1 · Cited by 11
Latzman, R. D., Green, L. M., & Fernandes, M. A. (2017) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2017.30.02.03 · Cited by 11
Detection of social approach in inbred mice
Pratte, M., & Jamon, M. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.04.011 · Cited by 11
Chapter 6 Advances in Vasopressin Receptor Agonists and Antagonists
Ryckmans, T. (2009) · Annual reports in medicinal chemistry · doi:10.1016/s0065-7743(09)04406-6 · Cited by 11
Wallace, K. J., Chun, E. K., Manns, J. R., Ophir, A. G., & Kelly, A. M. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105362 · Cited by 10
“Moreover, sexually experienced prairie vole males often respond to interactions with a novel same-sex conspecific with aggression (Winslow et al., 1993).”
Berendzen, K. M., Bales, K. L., & Manoli, D. S. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105339 · Cited by 10
The output of the hippocampus is inhibited during social behavior in the male rat
Garritano, J., Martinez, C., Grossman, K., Intemann, P., Merritt, K. E., Pfoff, R., & Smock, T. (1996) · Experimental Brain Research · doi:10.1007/bf00229553 · Cited by 10
“Finally, there is evidence that brain vasopressin, or a similar peptide, mediates pair-bond formation in monogamous prairie voles ( Winslow et al. 1993 ).”
BackgroundParker, J. T., Rodriguez, N. A., Lawal, B., Delevan, C. J., & Bamshad, M. (2011) · Behavioural Processes · doi:10.1016/j.beproc.2011.08.010 · Cited by 10
Cis→Trans Isomerization of Pro7 in Oxytocin Regulates Zn2+ Binding
Fuller, D. R., Glover, M. S., Pierson, N. A., Kim, D., Russell, D. H., & Clemmer, D. E. (2016) · Journal of the American Society for Mass Spectrometry · doi:10.1007/s13361-016-1410-4 · Cited by 10
“Oxytocin (OT) is a nine-residue peptide that facilitates labor and lactation [1], and is associated with psychological issues such as trust, fear, anxiety, aggression, and pair bonding [2, 3].”
Thompson, R. R. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104742 · Cited by 10
The Effects of Acute Arginine Vasopressin Administration on Social Cognition in Healthy Males
Kenyon, A. R., Alvares, G. A., Hickie, I. B., & Guastella, A. J. (2013) · Journal of Hormones · doi:10.1155/2013/386306 · Cited by 10
Fatherhood alters gene expression within the MPOA
Seelke, A. M. H., Bond, J. M., Simmons, T. C., Joshi, N., Settles, M. L., Stolzenberg, D. S., Rhemtulla, M., & Bales, K. L. (2018) · Current Zoology · doi:10.1093/eep/dvy026 · Cited by 52
Neuroplasticity and Aggression: An Interaction Between Vasopressin and Serotonin
Ferris, C. F. (2005) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195168761.003.0007 · Cited by 10
Arginine Vasopressin 1a Receptor (AVPR1a) RS3 Repeat Polymorphism Associated with EntrepreneurshipPreprint
Wernerfelt, N., Rand, D. G., Dreber, A., Montgomery, C., & Malhotra, D. K. (2012) · SSRN Electronic Journal · doi:10.2139/ssrn.2141598 · Cited by 11
GOODSON, J. L., EIBACH, R., DUKES, A., FRIEDMAN, M., SAKATA, J., THOMPSON, R., & ADKINS‐REGAN, E. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51956.x · Cited by 10
Horie, K., Blumenthal, S. A., Inoue, K., Yada, S., Nishimori, K., & Young, L. J. (2025) · Hormones and Behavior · doi:10.1016/j.yhbeh.2025.105708 · Cited by 8
“There is some evidence that OXTR signaling may play a sex-specific role in facilitating pair bonding in female prairie voles (Insel and Hulihan, 1995; Winslow et al., 1993), while others suggest a role in both sexes (Cho et al., 1999; Johnson et al., 2016).”
Association between parental behaviors and structural plasticity in the brain of male rodents
Inada, K., & Miyamichi, K. (2023) · Neuroscience Research · doi:10.1016/j.neures.2023.06.007 · Cited by 9
Prairie voles as a model for adaptive reward remodeling following loss of a bonded partner
Sadino, J., & Donaldson, Z. (2024) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.15134 · Cited by 7
Carsten Schradin, A., Larke, R. H., & Bales, K. L. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.02.060 · Cited by 9
“Variation in this receptor has been shown in brain areas of the “social behavior network” (lateral septum, amygdala, ventral pallidum) [6] which are known to regulate social recognition and pair bond formation [7,8].”
Reliability of basal plasma vasopressin concentrations in healthy male adults
Quintana, D. S., Westlye, L. T., Smerud, K. T., Mahmoud, R. A., Djupesland, P. G., & Andreassen, O. A. (2016) · Acta Neuropsychiatrica · doi:10.1017/neu.2016.67 · Cited by 9
“Intriguingly, animal studies have shown more specific socialbehavioural effects with AVP compared with OT administration (3), particularly in males.”
BackgroundSoto, M., Lewis, R. J., & Curtis, J. T. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.02.008 · Cited by 9
Neuroendocrinology and Behavior
Sumiyoshi, T. (2012) · InTech eBooks · doi:10.5772/1666 · Cited by 9
Blondel, D. V., & Phelps, S. M. (2016) · Journal of comparative psychology · doi:10.1037/com0000048 · Cited by 9
“…and pups could be used as stimulus animals for cohabitation followed by preference tests; sexually naïve males generally do not attack each other (Winslow et al., 1993) and can exhibit affiliative behavior towards unrelated pups (Bales et al., 2006; Ophir, Crino, Wilkerson, Wolff, & Phelps,…”
BackgroundMethodInfluentialDevelopment of a radioligand for imaging V 1a vasopressin receptors with PET
Naik, R., Valentine, H., Hall, A., Mathews, W. B., Harris, J. C., Carter, C. S., Dannals, R. F., Wong, D. F., & Horti, A. G. (2017) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2017.08.037 · Cited by 9
“Social attunement is fundamental to sexual behavior, pair-bonding, maternal behavior, mate guarding, social memory and biparental care [4, 5].”
BackgroundSelf-citationPaban, V., Alescio‐Lautier, B., Devigne, C., & Soumireu-Mourat, B. (1998) · European Journal of Pharmacology · doi:10.1016/s0014-2999(98)00704-3 · Cited by 9
Tsuji, C., Tsuji, T., Allchorne, A. J., Leng, G., & Ludwig, M. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12531 · Cited by 8
“The neuropeptide also regulates social behaviours such as aggression (11, 76 12), pair-bonding (13, 14), and parental behaviour (15, 16) and has also been linked to 77 human social behaviours in health (17-19) and during neurological disorders such as 78 autism (20, 21).”
Vasopressin and oxytocin receptors (version 2019.4) in the IUPHAR/BPS Guide to Pharmacology Database
Bichet, D. G., Bouvier, M., Chini, B., Gimpl, G., Guillon, G., Kimura, T., Knepper, M. A., Lolait, S. J., Manning, M., Mouillac, B., et al. (2019) · IUPHAR/BPS Guide to Pharmacology CITE · doi:10.2218/gtopdb/f66/2019.4 · Cited by 8
Medial amygdala ERα expression influences monogamous behaviour of male prairie voles in the field
Lambert, C. T., Lichter, J. B., Perry, A. N., Castillo, S. A., Keane, B., Cushing, B. S., & Solomon, N. G. (2021) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2021.0318 · Cited by 7
Rethinking the Architecture of Attachment: New Insights into the Role for Oxytocin Signaling
Berendzen, K. M., & Manoli, D. S. (2022) · Affective Science · doi:10.1007/s42761-022-00142-5 · Cited by 9
Gingrich, B., HOUT, R. L., Wang, Z., & Insel, T. R. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51952.x · Cited by 8
Self-citationBrains and speciation: Control of behavior
Barker, A. J. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.11.003 · Cited by 7
Carter, C. S., & Porges, S. W. (2010) · Elsevier eBooks · doi:10.1016/b978-0-08-045396-5.00207-4 · Cited by 8
Self-citationNaloxone increases conditioned fear responses during social buffering in male rats
Yamasaki, T., Kiyokawa, Y., Munetomo, A., & Takeuchi, Y. (2024) · European Journal of Neuroscience · doi:10.1111/ejn.16343 · Cited by 7
“Although these neuromodulators mediate affiliative behaviour to a specific familiar conspecific (Insel & Hulihan, 1995; Kendrick et al., 1992; Smith & Wang, 2014; Winslow et al., 1993), social buffering in the present study was induced by unfamiliar conspecifics.”
BackgroundNeuroendocrine mechanisms contributing to the coevolution of sociality and communication
Freiler, M. K., & Smith, G. T. (2023) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2023.101077 · Cited by 8
Mating systems, social behaviour and hormones
Goymann, W., & Hofer, H. (2010) · Springer eBooks · doi:10.1007/978-3-642-02624-9_16 · Cited by 7
Rodriguez, N. A., Legzim, K. M., Aliou, F., Al-Naimi, O. A. S., & Bamshad, M. (2013) · Behavioural Processes · doi:10.1016/j.beproc.2013.10.002 · Cited by 7
Intranasal vasopressin expedites dishonesty in women
Feng, C., Qin, L., Luo, Y., & Xu, P. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104843 · Cited by 7
Neuronal activation in the caudal brainstem associated with mating by voles
Curtis, J. T., Berkley, K. J., & Wang, Z. X. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00175-7 · Cited by 7
“1 mg/day for 3 days) induces sexual receptivity in most female prairie voles [18].”
Differences in Neural Response to Romantic Stimuli in Monogamous and Non-Monogamous Men
Hamilton, L. D., & Meston, C. M. (2017) · Archives of Sexual Behavior · doi:10.1007/s10508-017-1071-9 · Cited by 8
'Friendship' in Macaques : economics and emotions
Massen, J. J. M. (2010) · Utrecht University Repository (Utrecht University) · Cited by 7
Comparative Cognition and Neuroscience
Snowdon, C. T., & Cronin, K. A. (2009) · Wiley eBooks · doi:10.1002/9780470478509.neubb001004 · Cited by 7
Gnanadesikan, G. E., Bray, E. E., Cook, E. N., Levy, K., Douglas, L. E. L. C., Kennedy, B. S., Tecot, S. R., & MacLean, E. L. (2024) · Hormones and Behavior · doi:10.1016/j.yhbeh.2024.105612 · Cited by 6
“These include functions related to pair-bonding (Insel and Shapiro, 1992; Winslow and Insel, 1991; Winslow et al., 1993), parental care (Caldwell et al., 2008; Curley et al., 2012; Finkenwirth et al., 2016; Keverne and Kendrick, 1992; Pederson and Prange, 1979; Saito and Nakamura, 2011; Saltzman…”
Background
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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