Septal oxytocin administration impairs peer affiliation via V1a receptors in female meadow voles
Open accessAbstract
The peptide hormone oxytocin (OT) plays an important role in social behaviors, including social bond formation. In different contexts, however, OT is also associated with aggression, social selectivity, and reduced affiliation. Female meadow voles form social preferences for familiar same-sex peers under short, winter-like day lengths in the laboratory, and provide a means of studying affiliation outside the context of reproductive pair bonds. Multiple lines of evidence suggest that the actions of OT in the lateral septum (LS) may decrease affiliative behavior, including greater density of OT receptors in the LS of meadow voles that huddle less. We infused OT into the LS of female meadow voles immediately prior to cohabitation with a social partner to determine its effects on partner preference formation. OT prevented the formation of preferences for the partner female. Co-administration of OT with a specific OT receptor antagonist did not reverse the effect, but co-administration of OT with a specific vasopressin 1a receptor (V1aR) antagonist did, indicating that OT in the LS likely acted through V1aRs to decrease partner preference. Receptor autoradiography revealed dense V1aR binding in the LS of female meadow voles. These results suggest that the LS is a brain region that may be responsible for inhibitory effects of OT administration on affiliation, which will be important to consider in therapeutic administrations of OT.
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In female meadow voles housed in winter-like conditions, injection of OT into the lateral septum prevents the formation of partner preferences, an effect blocked by co-administration of OT with a V1aR but not an OTR antagonist.
“When housed in winter-like conditions female voles form partner preferences for other females. Injection of OT into the lateral septum prevents the formation of these partner preferences, an effect that is blocked by co-administration of OT with a V1aR but not an OTR antagonist.”
From Cross-talk among oxytocin and arginine-vasopressin receptors: Relevance for basic and clinical studies of the brain and periphery (2018) · cites this paper as [54]
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Cites
NEWMAN, S. W. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09271.x · Cited by 1,189 · see citing works
The Neuropeptide Oxytocin Regulates Parochial Altruism in Intergroup Conflict Among Humans
De Dreu, C. K. W., Greer, L. L., Handgraaf, M. J. J., Shalvi, S., Van Kleef, G. A., Baas, M., Ten Velden, F. S., Van Dijk, E., & Feith, S. W. W. (2010) · Science · doi:10.1126/science.1189047 · Cited by 1,148 · see citing works
Social amnesia in mice lacking the oxytocin gene
Ferguson, J. N., Young, L. J., Hearn, E. F., Matzuk, M. M., Insel, T. R., & Winslow, J. T. (2000) · Nature Genetics · doi:10.1038/77040 · Cited by 1,130 · see citing works
Oxytocin in the Medial Amygdala is Essential for Social Recognition in the Mouse
Ferguson, J. N., Aldag, J. M., Insel, T. R., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-20-08278.2001 · Cited by 1,043 · see citing works
Oxytocin promotes human ethnocentrism
De Dreu, C. K. W., Greer, L. L., Van Kleef, G. A., Shalvi, S., & Handgraaf, M. J. J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015316108 · Cited by 838 · cited 1× · see citing works
“…on a variety of factors including social target (group member versus perceived outsider), prior history, sex, and target region within the brain (see Beery, 2015 for review; De Dreu et al., 2010, 2011; Declerck et al., 2014; Goodson and Thompson, 2010; Scheele et al., 2014; Sheng et al., 2013).”
The vertebrate social behavior network: Evolutionary themes and variations
Goodson, J. L. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.02.003 · Cited by 771 · see citing works
Oxytocin pathways and the evolution of human behavior
Carter, C. S. (2014) · Annual Review of Psychology · doi:10.1146/annurev-psych-010213-115110 · Cited by 714 · see citing works
Liu, Y., & Wang, Z. X. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00555-4 · Cited by 580 · cited 2× · see citing works
“…bond formation: in female prairie voles, partner preference for an opposite-sex mate relies on OT binding to OTRs in the nucleus accumbens (Liu and Wang, 2003; Young et al., 2001); in meadow voles, however, OTR density in the nucleus accumbens is not related to same-sex (Beery and Zucker,…”
Cellular Mechanisms of Social Attachment
Young, L. J., Lim, M. M., Gingrich, B., & Insel, T. R. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1691 · Cited by 523 · see citing works
WILLIAMS, J. (1992) · Hormones and Behavior · doi:10.1016/0018-506x(92)90004-f · Cited by 471 · see citing works
Insel, T., Wang, Z., & Ferris, C. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-09-05381.1994 · Cited by 454 · see citing works
Oxytocin and Vasopressin Agonists and Antagonists as Research Tools and Potential Therapeutics
Manning, M., Misicka, A., Olma, A., Bankowski, K., Stoev, S., Chini, B., Durroux, T., Mouillac, B., Corbani, M., & Guillon, G. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2012.02303.x · Cited by 423 · see citing works
Sala, M., Braida, D., Lentini, D., Busnelli, M., Bulgheroni, E., Capurro, V., Finardi, A., Donzelli, A., Pattini, L., Rubino, T., et al. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.12.022 · Cited by 375 · see citing works
Landgraf, R., Gerstberger, R., Montkowski, A., Probst, J., Wotjak, C., Holsboer, F., & Engelmann, M. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-06-04250.1995 · Cited by 341 · see citing works
Ross, 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
De Vries, G. J., Buds, R. M., & Swaab, D. F. (1981) · Brain Research · doi:10.1016/0006-8993(81)90989-6 · Cited by 319 · cited 1× · see citing works
“Vasopressin immunoreactivity in the LS is testosterone-dependent, and typically lower in females than in males (Bamshad et al., 1993; de Vries et al., 1981; De Vries et al., 1992; Wang and Devries, 1993), but may also play a role in activating V1aRs in female meadow voles.”
Liu, Y., Curtis, J. T., & Wang, Z. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.4.910 · Cited by 282 · see citing works
Bales, K. L., Perkeybile, A. M., Conley, O. G., Lee, M. H., Guoynes, C. D., Downing, G. M., Yun, C. R., Solomon, M., Jacob, S., & Mendoza, S. P. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.08.025 · Cited by 265 · see citing works
Nonapeptide mechanisms of social cognition, behavior and species-specific social systems
Goodson, J. L., & Thompson, R. R. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.08.020 · Cited by 261 · see citing works
Olazábal, D. E., & Young, L. J. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.010 · Cited by 230 · see citing works
Life in groups: the roles of oxytocin in mammalian sociality
Anacker, A. M. J., & Beery, A. K. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00185 · Cited by 216 · see citing works
Self-citationFear-enhancing effects of septal oxytocin receptors
Guzmán, Y. F., Tronson, N. C., Jovasevic, V., Sato, K., Guedea, A. L., Mizukami, H., Nishimori, K., & Radulovic, J. (2013) · Nature Neuroscience · doi:10.1038/nn.3465 · Cited by 215 · see citing works
Lukas, M., Toth, I., Veenema, A. H., & Neumann, I. D. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.09.018 · Cited by 211 · see citing works
Brain oxytocin in social fear conditioning and its extinction: involvement of the lateral septum
Zoicas, I., Slattery, D. A., & Neumann, I. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.156 · Cited by 189 · see citing works
Oxytocin-Induced Analgesia and Scratching Are Mediated by the Vasopressin-1A Receptor in the Mouse
Schorscher-Petcu, A., Sotocinal, S., Ciura, S., Dupre, A., Ritchie, J., Sorge, R. E., Crawley, J. N., Hu, S.-B., Nishimori, K., Young, L. J., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1594-10.2010 · Cited by 189 · see citing works
Veenema, A. H., Beiderbeck, D. I., Lukas, M., & Neumann, I. D. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.006 · Cited by 180 · see citing works
Bamshad, M., Novak, M. A., & De Vries, G. J. (1993) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1993.tb00480.x · Cited by 175 · see citing works
Goodson, & Adkins‐Regan (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00284.x · Cited by 171 · see citing works
Neurobiological mechanisms of social attachment and pair bonding
Johnson, Z. V., & Young, L. J. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.01.009 · Cited by 169 · see citing works
Bredewold, R., Smith, C. J. W., Dumais, K. M., & Veenema, A. H. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00216 · Cited by 157 · see citing works
Madison, D. M., FitzGerald, R. W., & McShea, W. J. (1984) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00310209 · Cited by 150 · see citing works
Keebaugh, A. C., Barrett, C. E., Laprairie, J. L., Jenkins, J. J., & Young, L. J. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1040893 · Cited by 150 · see citing works
Beery, A. K., Lacey, E. A., & Francis, D. D. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21638 · Cited by 144 · see citing works
Self-citationGur, R., Tendler, A., & Wagner, S. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.03.022 · Cited by 144 · see citing works
Mating system of the meadow vole, Microtus pennsylvanicus
Boonstra, R., Xia, X., & Pavone, L. V. (1993) · Behavioral Ecology · doi:10.1093/beheco/4.1.83 · Cited by 140 · see citing works
Oxytocin modulates the racial Bias in neural responses to others' suffering
Sheng, F., Liu, Y., Zhou, B., Zhou, W., & Han, S. (2013) · Biological Psychology · doi:10.1016/j.biopsycho.2012.11.018 · Cited by 139 · cited 2× · see citing works
“…on a variety of factors including social target (group member versus perceived outsider), prior history, sex, and target region within the brain (see Beery, 2015 for review; De Dreu et al., 2010, 2011; Declerck et al., 2014; Goodson and Thompson, 2010; Scheele et al., 2014; Sheng et al., 2013).”
Veenema, A. H., Bredewold, R., & De Vries, G. J. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.10.002 · Cited by 129 · see citing works
Wang, Z., & Vries, G. J. D. (1993) · Brain Research · doi:10.1016/0006-8993(93)91203-5 · Cited by 129 · see citing works
Opposing effects of oxytocin on moral judgment in males and females
Scheele, D., Striepens, N., Kendrick, K. M., Schwering, C., Noelle, J., Wille, A., Schlaepfer, T. E., Maier, W., & Hurlemann, R. (2014) · Human Brain Mapping · doi:10.1002/hbm.22605 · Cited by 112 · see citing works
Song, Z., McCann, K. E., McNeill, J. K., Larkin, T. E., Huhman, K. L., & Albers, H. E. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.08.005 · Cited by 111 · see citing works
Oxytocin and same-sex social behavior in female meadow voles
Beery, A. K., & Zucker, I. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.05.023 · Cited by 108 · see citing works
Self-citationCaughey, S. D., Klampfl, S. M., Bishop, V. R., Pfoertsch, J., Neumann, I. D., Bosch, O. J., & Meddle, S. L. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02224.x · Cited by 107 · see citing works
Manning, M., Miteva, K., Pancheva, S. N., STOEV, S., Wo, N. C., & Chan, W. Y. (1995) · International journal of peptide & protein research · doi:10.1111/j.1399-3011.1995.tb00596.x · Cited by 99 · see citing works
Declerck, C. H., Boone, C., & Kiyonari, T. (2014) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst040 · Cited by 96 · see citing works
Curley, J. P., Jensen, C. L., Franks, B., & Champagne, F. A. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.013 · Cited by 90 · see citing works
The many faces of oxytocin: Implications for psychiatry
Zik, J. B., & Roberts, D. L. (2014) · Psychiatry Research · doi:10.1016/j.psychres.2014.11.048 · Cited by 85 · see citing works
McShea, W. J. (1990) · Animal Behaviour · doi:10.1016/s0003-3472(05)80880-2 · Cited by 83 · see citing works
Parker, K. J., Kinney, L. F., Phillips, K. M., & Lee, T. M. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.6.1341 · Cited by 82 · see citing works
Neuroscience: The hard science of oxytocin
Shen, H. H. (2015) · Nature · doi:10.1038/522410a · Cited by 80 · see citing works
Evaluation of two automated metrics for analyzing partner preference tests
Ahern, T. H., Modi, M. E., Burkett, J. P., & Young, L. J. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.06.010 · Cited by 79 · see citing works
Ferkin, M. H., & Zucker, I. (1991) · Reproduction · doi:10.1530/jrf.0.0920433 · Cited by 77 · see citing works
Antisocial oxytocin: Complex effects on social behavior
Beery, A. K. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.11.006 · Cited by 74 · see citing works
Self-citationDumais, K. M., Alonso, A. G., Immormino, M. A., Bredewold, R., & Veenema, A. H. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.11.007 · Cited by 72 · see citing works
Social Structure and Aggressive Behavior in a Population of Microtus pennsylvanicus
Getz, L. L. (1972) · Journal of Mammalogy · doi:10.2307/1379167 · Cited by 71 · see citing works
Qiu, F., Qiu, C., Cai, H., Liu, T., Qu, Z., Yang, Z., Li, J., Zhou, Q., & Hu, W. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12635 · Cited by 67 · see citing works
Beyond “oxytocin = good”: neural complexities and the flipside of social bonds
van Anders, S. M., Goodson, J. L., & Kingsbury, M. A. (2013) · Archives of Sexual Behavior · doi:10.1007/s10508-013-0134-9 · Cited by 52 · see citing works
Day length and estradiol affect same-sex affiliative behavior in the female meadow vole
Beery, A. K., Loo, T. J., & Zucker, I. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.02.007 · Cited by 50 · see citing works
Self-citationSame-sex social behavior in meadow voles: Multiple and rapid formation of attachments
Beery, A. K., Routman, D. M., & Zucker, I. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.01.020 · Cited by 47 · see citing works
Self-citationFemale meadow voles (Microtus pennsylvanicus) demonstrate same-sex partner preferences.
Parker, K. J., & Lee, T. M. (2003) · Journal of comparative psychology · doi:10.1037/0735-7036.117.3.283 · Cited by 40 · see citing works
Gonadal Steroid Modulation of Vasopressin Pathwaysa
Vries, G. J. D., Crenshaw, B. J., & AL‐SHAMMA, H. A. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34369.x · Cited by 38 · see citing works
Chan, W. Y., Wo, N. C., Cheng, L., & Manning, M. (1996) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)12959-5 · Cited by 31 · see citing works
Corticotropin-releasing factor receptor densities vary with photoperiod and sociality
Beery, A. K., Vahaba, D. M., & Grunberg, D. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.08.014 · Cited by 30 · see citing works
Self-citationStress impairs new but not established relationships in seasonally social voles
Anacker, A. M. J., Reitz, K. M., Goodwin, N. L., & Beery, A. K. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.01.004 · Cited by 29 · see citing works
Self-citationLEONARD, S., ALIZADEHNADERI, R., STOKES, K., et al. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.05.011 · Cited by 26 · see citing works
Ondrasek, N. R., Wade, A., Burkhard, T. T., Hsu, K., Nguyen, T., Post, J., & Zucker, I. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.12.021 · Cited by 20 · see citing works
Yong, E. (2012) · The New Scientist · doi:10.1016/s0262-4079(12)60377-7 · Cited by 15 · see citing works
LEONARD, S., & Ferkin, M. H. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00161-4 · Cited by 13 · see citing works
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Resendez, S. L., Namboodiri, V. M. K., Otis, J. M., Eckman, L. E. H., Rodriguez-Romaguera, J., Ung, R. L., Basiri, M. L., Kosyk, O., Rossi, M. A., Dichter, G. S., et al. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.1515-18.2020 · Cited by 142 · see citing works
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- Authors
- Anacker, A. M. J., Christensen, J. D., LaFlamme, E. M., Grunberg, D. M., & Beery, A. K.
- Affiliations
- Smith College (US)
- Corresponding author
- Beery, Annaliese K.
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2016-06
- Volume
- 68
- Pages
- 156-162
- ISSN
- 0306-4530 (ISSN-L)
- PMC
- PMC4851907
- OpenAlex
- W2285705771
- Cited by
- 44
- References
- 67
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 4 · 2023: 6 · 2022: 4 · 2021: 6 · 2020: 5 · 2019: 4 · 2018: 6 · 2017: 2 · 2016: 1
- FWCI
- 6.81
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (am, 283 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Psychoneuroendocrinology (acceptedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Smith ScholarWorks (Smith College) (submittedVersion, cc-by)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Science Foundation (#1257162)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- oxytocin, vasopressin V1a receptor, lateral septum, social affiliation, mate preferences, Microtus pennsylvanicus, female social behavior, social selectivity, receptor antagonists, huddling behavior
- MeSH terms
- Animals, Autoradiography, Brain, Arvicolinae, Female, Oxytocin, Pair Bond, Peer Group, Septal Nuclei, Sexual Behavior, Animal, Social Behavior, Receptors, Vasopressin, Receptors, Oxytocin
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