Intranasal oxytocin drives coordinated social approach.

Administration, Intranasal Aggression / drug effects Animals Female Male Mice Oxytocin / pharmacology Pair Bond Sexual Behavior, Animal / drug effects Social Behavior

Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
09 09 2021
Historique:
received: 15 06 2021
accepted: 24 08 2021
entrez: 10 9 2021
pubmed: 11 9 2021
medline: 16 11 2021
Statut: epublish

Résumé

Coordinated responses to challenge are essential to survival for bonded monogamous animals and may depend on behavioral compatibility. Oxytocin (OT) context-dependently regulates social affiliation and vocal communication, but its role in pair members' decision to jointly respond to challenge is unclear. To test for OT effects, California mouse females received an intranasal dose of OT (IN-OT) or saline after bonding with males either matched or mismatched in their approach response to an aggressive vocal challenge. Pair mates were re-tested jointly for approach response, time spent together, and vocalizations. Females and males converged in their approach after pairing, but mismatched pairs with females given a single dose of IN-OT displayed a greater convergence that resulted from behavioral changes by both pair members. Unpaired females given IN-OT did not change their approach, indicating a social partner was necessary for effects to emerge. Moreover, IN-OT increased time spent approaching together, suggesting behavioral coordination beyond a further increase in bonding. This OT-induced increase in joint approach was associated with a decrease in the proportion of sustained vocalizations, a type of vocalization that can be associated with intra-pair conflict. Our results expand OT's effects on behavioral coordination and underscore the importance of emergent social context.

Identifiants

DOI: 10.1038/s41598-021-97468-0 PMID: 34504242 PMC: PMC8429717
pubmed: 34504242
doi: 10.1038/s41598-021-97468-0
pii: 10.1038/s41598-021-97468-0
pmc: PMC8429717
doi:

Substances chimiques

Oxytocin 50-56-6

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

17923

Informations de copyright

© 2021. The Author(s).

Références

Dillard, J. R. & Westneat, D. F. Disentangling the correlated evolution of monogamy and cooperation. Trends Ecol. Evol. 31(7), 503–513 (2016).
pubmed: 27156754 doi: 10.1016/j.tree.2016.03.009
French, J. A., Cavanaugh, J., Mustoe, A. & Carp, S. Social monogamy in nonhuman primates: phylogeny, phenotype, and physiology. J. Sex Res. 55(4–5), 410–434 (2018).
pubmed: 28704071 doi: 10.1080/00224499.2017.1339774
Klug, H. Why monogamy? A review of potential ultimate drivers. Front Ecol Evol. 6, 30 (2018).
doi: 10.3389/fevo.2018.00030
Mayer, M., Zedrosser, A. & Rosell, F. Extra-territorial movements differ between territory holders and subordinates in a large, monogamous rodent. Sci. Rep. 7(1), 1–10 (2017).
doi: 10.1038/s41598-017-15540-0
Dally, J. M., Emery, N. J. & Clayton, N. S. The SOCIAL SUPPRESSION OF CACHING IN WESTERN Scrub-Jays (Aphelocoma californica). Behaviour 142(7), 961–977 (2005).
doi: 10.1163/1568539055010084
Borries, C., Savini, T. & Koenig, A. Social monogamy and the threat of infanticide in larger mammals. Behav. Ecol. Sociobiol. 65(4), 685–693 (2011).
doi: 10.1007/s00265-010-1070-5
Both, C. & Visser, M. E. Breeding territory size affects fitness: an experimental study on competition at the individual level. J. Anim. Ecol. 69(6), 1021–1030 (2000).
doi: 10.1046/j.1365-2656.2000.00458.x
Thomas, D. W., Blondel, J., Perret, P., Lambrechts, M. M. & Speakman, J. R. Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science 291(5513), 2598–2600 (2001).
pubmed: 11283370 doi: 10.1126/science.1057487
Agrell, J., Wolff, J. O. & Ylönen, H. Counter-strategies to infanticide in mammals: costs and consequences. Oikos 83(3), 507–517 (1998).
doi: 10.2307/3546678
Rogers, W. Parental investment and division of labor in the midas cichlid (Cichlasoma citrinellum). Ethology 79(2), 126–142 (1988).
doi: 10.1111/j.1439-0310.1988.tb00706.x
Brotherton, P. N. M., Pemberton, J. M., Komers, P. E. & Malarky, G. Genetic and behavioural evidence of monogamy in a mammal, Kirk’s dik-dik (Madoqua kirkii). Proc. R. Soc. B Biol. Sci. 264(1382), 675–681 (1997).
doi: 10.1098/rspb.1997.0096
Thomas, J. A. & Birney, E. C. Parental care and mating system of the prairie vole, Microtus ochrogaster. Behav. Ecol. Sociobiol. 5(2), 171–186 (1979).
doi: 10.1007/BF00293304
Ahern, T. H., Hammock, E. A. D. & Young, L. J. Parental division of labor, coordination, and the effects of family structure on parenting in monogamous prairie voles (Microtus ochrogaster). Dev. Psychobiol. 53(2), 118–131 (2011).
pubmed: 20945408 doi: 10.1002/dev.20498
Frazier, C. R. M. M., Trainor, B. C., Cravens, C. J., Whitney, T. K. & Marler, C. A. Paternal behavior influences development of aggression and vasopressin expression in male California mouse offspring. Horm. Behav. 50(5), 699–707 (2006).
pubmed: 16934808 doi: 10.1016/j.yhbeh.2006.06.035
Marler, C. A, Trainor, B. C., Gleason, E. D., Bester-Meredith, J.K. & Becker, E. A. The Effects of Paternal Behavior on Offspring Aggression and Hormones in the Biparental California Mouse. Neurobiol. Parent Brain. 435–448 (Elsevier, California, 2008).
Rieger, N. S. & Marler, C. A. The function of ultrasonic vocalizations during territorial defence by pair-bonded male and female California mice. Anim. Behav. 135, 97–108 (2018).
doi: 10.1016/j.anbehav.2017.11.008
Olff, M. et al. The role of oxytocin in social bonding, stress regulation and mental health: an update on the moderating effects of context and interindividual differences. Psychoneuroendocrinology 38(9), 1883–1894 (2013).
pubmed: 23856187 doi: 10.1016/j.psyneuen.2013.06.019
Ditzen, B. et al. Intranasal oxytocin increases positive communication and reduces cortisol levels during couple conflict. Biol. Psychiatry. 65(9), 728–731 (2009).
pubmed: 19027101 doi: 10.1016/j.biopsych.2008.10.011
Williams, A. V. et al. Social approach and social vigilance are differentially regulated by oxytocin receptors in the nucleus accumbens. Neuropsychopharmacology 45(9), 1423–1430 (2020).
pubmed: 32198453 pmcid: 7360746 doi: 10.1038/s41386-020-0657-4
Eckstein, M. et al. Oxytocin facilitates the sensation of social stress. Hum. Brain Mapp. 35(9), 4741–4750 (2014).
pubmed: 24659430 pmcid: 6869318 doi: 10.1002/hbm.22508
Shamay-Tsoory, S. G. et al. Intranasal administration of oxytocin increases envy and schadenfreude (gloating). Biol. Psychiatry. 66(9), 864–870 (2009).
pubmed: 19640508 doi: 10.1016/j.biopsych.2009.06.009
DeWall, C. N. et al. When the love hormone leads to violence: oxytocin increases intimate partner violence inclinations among high trait aggressive people. Soc. Psychol. Personal. Sci. 5(6), 691–697 (2014).
doi: 10.1177/1948550613516876
De Dreu, C. K. W. et al. Oxytocin promotes human ethnocentrism. Proc. Natl. Acad. Sci. 108(4), 1262–1266 (2011).
pubmed: 21220339 pmcid: 3029708 doi: 10.1073/pnas.1015316108
Shamay-Tsoory, S. G. & Abu-Akel, A. The social salience hypothesis of oxytocin. Biol. Psychiatry. 79(3), 194–202 (2016).
pubmed: 26321019 doi: 10.1016/j.biopsych.2015.07.020
Harari-Dahan, O. & Bernstein, A. A general approach—avoidance hypothesis of oxytocin: accounting for social and non-social effects of oxytocin. Neurosci. Biobehav. Rev. 47, 506–519 (2014).
pubmed: 25454355 doi: 10.1016/j.neubiorev.2014.10.007
Kemp, A. H. & Guastella, A. J. The role of oxytocin in human affect: a novel hypothesis. Curr. Dir. Psychol. Sci. 20(4), 222–231 (2011).
doi: 10.1177/0963721411417547
Cavanaugh, J., Mustoe, A., Womack, S. L. & French, J. A. Oxytocin modulates mate-guarding behavior in marmoset monkeys. Horm. Behav. 106, 150–161 (2018).
pubmed: 30342885 pmcid: 6298842 doi: 10.1016/j.yhbeh.2018.10.009
Marsh, N. et al. Oxytocin-enforced norm compliance reduces xenophobic outgroup rejection. Proc. Natl. Acad. Sci. 114(35), 9314–9319 (2017).
pubmed: 28808030 pmcid: 5584433 doi: 10.1073/pnas.1705853114
Wey, T. W., Vrana, P. B. & Mabry, K. E. Mating system as a possible driver of behavioral diversity in Peromyscus. Behav. Ecol. Sociobiol. 71(11), 163 (2017).
doi: 10.1007/s00265-017-2392-3
Merritt, J. F. Peromyscus californicus. Mamm. Species. 85, 1 (1978).
doi: 10.2307/3503909
Gubernick, D. J. & Cully, N. J. Behavioral ecology and sociobiology mechanisms of sexual fidelity in the monogamous California mouse, Peromyscus californicus. Behav. Ecol. Sociobiol. 32, 211–219 (1993).
doi: 10.1007/BF00173779
Trainor, B. C. & Marler, C. A. Testosterone, paternal behavior, and aggression in the monogamous California Mouse (Peromyscus californicus). Horm Behav. 40(1), 32–42 (2001).
pubmed: 11467882 doi: 10.1006/hbeh.2001.1652
Bester-Meredith, J. K., Young, L. J. & Marler, C. A. Species differences in paternal behavior and aggression in Peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm. Behav. 36(1), 25–38 (1999).
pubmed: 10433884 doi: 10.1006/hbeh.1999.1522
Davis, E. S. & Marler, C. A. The progesterone challenge: steroid hormone changes following a simulated territorial intrusion in female Peromyscus californicus. Horm. Behav. 44(3), 185–198 (2003).
pubmed: 14609541 doi: 10.1016/S0018-506X(03)00128-4
Marler, C. A., Oyegbile, T. O. & Marler, C. A. Winning fights elevates testosterone levels in California mice and enhances future ability to win fights. Horm. Behav. 48(3), 259–267 (2005).
pubmed: 15979073 doi: 10.1016/j.yhbeh.2005.04.007
Fuxjager, M. J., Mast, G., Becker, E. A. & Marler, C. A. The “home advantage” is necessary for a full winner effect and changes in post-encounter testosterone. Horm. Behav. 56(2), 214–219 (2009).
pubmed: 19426733 doi: 10.1016/j.yhbeh.2009.04.009
Rieger, N. S., Stanton, E. H. & Marler, C. A. Division of labour in territorial defence and pup retrieval by pair-bonded California mice, Peromyscus californicus. Anim. Behav. 156, 67–78 (2019).
doi: 10.1016/j.anbehav.2019.05.023
Rieger, N. S., Monari, P. K., Hartfield, K., Schefelker, J. & Marler, C. A. Pair-bonding leads to convergence in approach behavior to conspecific vocalizations in California mice (Peromyscus californicus). Plos one. 16(8), e0255295 (2021).
pubmed: 34383820 pmcid: 8360543 doi: 10.1371/journal.pone.0255295
Kalcounis-Rueppell, M. C., Pultorak, J. D. & Marler, C. A. Ultrasonic vocalizations of mice in the genus Peromyscus. Handb. Behav. Neurosci. 25, 227–235 (2018).
doi: 10.1016/B978-0-12-809600-0.00022-6
Guoynes, C. D. & Marler, C. A. An acute dose of intranasal oxytocin rapidly increases maternal communication and maintains maternal care in primiparous postpartum California mice. Plos one. 16(4), e0244033 (2021).
pubmed: 33886559 pmcid: 8061985 doi: 10.1371/journal.pone.0244033
Steinman, M. Q. et al. Sex-specific effects of stress on oxytocin neurons correspond with responses to intranasal oxytocin. Biol. Psychiatry. 80(5), 406–414 (2016).
pubmed: 26620251 doi: 10.1016/j.biopsych.2015.10.007
Duque-Wilckens, N. et al. Extrahypothalamic oxytocin neurons drive stress-induced social vigilance and avoidance. Proc. Natl. Acad. Sci. 117(42), 26406–26413 (2020).
pubmed: 33020267 pmcid: 7585015 doi: 10.1073/pnas.2011890117
Laubu, C., Dechaume-Moncharmont, F. X. X., Motreuil, S. & Schweitzer, C. Mismatched partners that achieve postpairing behavioral similarity improve their reproductive success. Sci. Adv. 2(3), e1501013 (2016).
pubmed: 26973869 pmcid: 4783125 doi: 10.1126/sciadv.1501013
Arueti, M. et al. When two become one: the role of oxytocin in interpersonal coordination and cooperation. J. Cogn. Neurosci. 25(9), 1418–1427 (2013).
pubmed: 23574582 doi: 10.1162/jocn_a_00400
Trainor, B. C., Bird, I. M. & Marler, C. A. Opposing hormonal mechanisms of aggression revealed through short-lived testosterone manipulations and multiple winning experiences. Horm. Behav. 45(2), 115–121 (2004).
pubmed: 15019798 doi: 10.1016/j.yhbeh.2003.09.006
Oyegbile, T. O. & Marler, C. A. Weak winner effect in a less aggressive mammal: correlations with corticosterone but not testosterone. Physiol. Behav. 89(2), 171–179 (2006).
pubmed: 16859719 doi: 10.1016/j.physbeh.2006.05.044
Kalcounis-Rueppell, M. C., Metheny, J. D. & Vonhof, M. J. Production of ultrasonic vocalizations by Peromyscus mice in the wild. Front. Zool. 3(1), 1–12 (2006).
doi: 10.1186/1742-9994-3-3
Pultorak, J. D., Alger, S. J., Loria, S. O., Johnson, A. M. & Marler, C. A. Changes in behavior and ultrasonic vocalizations during pair bonding and in response to an infidelity challenge in monogamous California mice. Front. Ecol. Evol. 6, 125 (2018).
doi: 10.3389/fevo.2018.00125
Gubernick, D. J. Reproduction in the California mouse, Peromyscus californicus. J. Mammal. 69(4), 857–860 (1988).
doi: 10.2307/1381649
Bales, K. L. et al. Long-term exposure to intranasal oxytocin in a mouse autism model. Transl. Psychiatry. 4(11), 480 (2014).
doi: 10.1038/tp.2014.117
Leppanen, J., Ng, K. W., Tchanturia, K. & Treasure, J. Meta-analysis of the effects of intranasal oxytocin on interpretation and expression of emotions. Neurosci. Biobehav. Rev. 78, 125–144 (2017).
pubmed: 28467893 doi: 10.1016/j.neubiorev.2017.04.010
Guoynes, C. D. et al. Chronic intranasal oxytocin has dose-dependent effects on central oxytocin and vasopressin systems in prairie voles (Microtus ochrogaster). Neuroscience 369, 292–302 (2018).
pubmed: 29183825 doi: 10.1016/j.neuroscience.2017.11.037
Smith, A. S., Korgan, A. C. & Young, W. S. Oxytocin delivered nasally or intraperitoneally reaches the brain and plasma of normal and oxytocin knockout mice. Pharmacol Res. 146, 104324 (2019).
pubmed: 31238093 pmcid: 6679720 doi: 10.1016/j.phrs.2019.104324
Duque-Wilckens, N. et al. Oxytocin receptors in the anteromedial bed nucleus of the stria terminalis promote stress-induced social avoidance in female california mice. Biol. Psychiatry. 83(3), 203–213 (2018).
pubmed: 29066224 doi: 10.1016/j.biopsych.2017.08.024
Rieger, N. S., Spool, J.A., Riters, L. V. & Marler, C.A. Unpublished data.
Pultorak, J. D., Matusinec, K. R., Miller, Z. K. & Marler, C. A. Ultrasonic vocalization production and playback predicts intrapair and extrapair social behaviour in a monogamous mouse. Anim. Behav. 125, 13–23 (2017).
doi: 10.1016/j.anbehav.2016.12.023
Timonin, M. E., Kalcounis-Rueppell, M. C. & Marler, C. A. Testosterone pulses at the nest site modify ultrasonic vocalization types in a monogamous and territorial mouse. Ethology 124(11), 804–815 (2018).
doi: 10.1111/eth.12812
Marler, C. A. & Monari, P. K. Neuroendocrine control of vocalizations in rodents. Neuroendocrine Regulation of Animal Vocalization. 201–216. (Academic Press, 2021).
Gleason, E. D. & Marler, C. A. Testosterone response to courtship predicts future paternal behavior in the California mouse, Peromyscus californicus. Horm. Behav. 57(2), 147–154 (2010).
pubmed: 19833131 doi: 10.1016/j.yhbeh.2009.10.006
Underhill, V. et al. Personality and behavioral syndromes in two Peromyscus species: presence, lack of state dependence, and lack of association with home range size. Behav. Ecol. Sociobiol. 75(1), 1–16 (2021).
doi: 10.1007/s00265-020-02951-9
Careau, V., Bininda-Emonds, O. R. P., Thomas, D. W., Réale, D. & Humphries, M. M. Exploration strategies map along fast-slow metabolic and life-history continua in muroid rodents. Funct. Ecol. 23(1), 150–156 (2009).
doi: 10.1111/j.1365-2435.2008.01468.x
Wang, L. et al. Effects of chronic social defeat on social behaviors in adult female mandarin voles (Microtus mandarinus): Involvement of the oxytocin system in the nucleus accumbens. Prog. Neuro-Psychopharmacol. Biol. Psychiatry. 82, 278–288 (2018).
doi: 10.1016/j.pnpbp.2017.11.002
Marazziti, D. et al. A relationship between oxytocin and anxiety of romantic attachment. Clin. Pract. Epidemiol. Ment. Heal. 2(1), 1–6 (2006).
doi: 10.1186/1745-0179-2-1
Laubu, C., Louâpre, P. & Dechaume-Moncharmont, F.X. Pair-bonding influences affective state in a monogamous fish species. Proc. R. Soc. B Biol. Sci. 286(1904), 20190760 (2019).
doi: 10.1098/rspb.2019.0760
Shaver, P. R. & Hazan, C. A biased overview of the study of love. J. Soc. Pers. Relat. 5(4), 473–501 (1988).
doi: 10.1177/0265407588054005
von Zimmermann, J., Vicary, S., Sperling, M., Orgs, G. & Richardson, D. C. The choreography of group affiliation. Top. Cogn. Sci. 10(1), 80–94 (2018).
doi: 10.1111/tops.12320
Ribble, D. O. & Salvioni, M. Social organization and nest co-occupancy in Peromyscus californicus, a monogamous rodent. Behav. Ecol. Sociobiol. 26(1), 9–15 (1990).
doi: 10.1007/BF00174020
Bosch, O. J. & Young, L. J. Oxytocin and social relationships: from attachment to bond disruption. Curr. Top. Behav. Neurosci. 35, 97–117 (2018).
pubmed: 28812266 pmcid: 5815947 doi: 10.1007/7854_2017_10
Webster, M. M. & Ward, A. J. W. Personality and social context. Biol. Rev. 86(4), 759–773 (2011).
pubmed: 21091603 doi: 10.1111/j.1469-185X.2010.00169.x
Réale, D., Reader, S. M., Sol, D., McDougall, P. T. & Dingemanse, N. J. Integrating animal temperament within ecology and evolution. Biol. Rev. 82(2), 291–318 (2007).
pubmed: 17437562 doi: 10.1111/j.1469-185X.2007.00010.x
Ostler, J. Surviving Genocide: Native Nations and the United States from the American Revolution to Bleeding Kansas (Yale University Press, Yale, 2019).
doi: 10.12987/9780300245264

Auteurs

Patrick K Monari (PK)

Department of Psychology, University of Wisconsin-Madison, Madison, WI, USA. monari@wisc.edu.

Nathaniel S Rieger (NS)

Department of Psychology, University of Wisconsin-Madison, Madison, WI, USA.
Department of Psychology and Neuroscience, Boston College, Chestnut Hill, MA, USA.

Juliette Schefelker (J)

Department of Psychology, University of Wisconsin-Madison, Madison, WI, USA.

Catherine A Marler (CA)

Department of Psychology, University of Wisconsin-Madison, Madison, WI, USA.

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Classifications MeSH

questionsmedicales.fr › Thérapeutique › Traitement médicamenteux › Voies d'administration de substances chimiques et des médicaments › Administration par voie topique › Administration par voie muqueuse › Administration par voie nasale › Intranasal oxytocin drives coordinated social approach.
questionsmedicales.fr › Comportement et mécanismes comportementaux › Comportement › Comportement social › Agressivité › Intranasal oxytocin drives coordinated social approach.
questionsmedicales.fr › Eucaryotes › Animaux › Intranasal oxytocin drives coordinated social approach.
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Intranasal oxytocin drives coordinated social approach.
questionsmedicales.fr › Acides aminés, peptides et protéines › Peptides › Hormones peptidiques › Hormones hypophysaires › Hormones post-hypophysaires › Ocytocine › Intranasal oxytocin drives coordinated social approach.
questionsmedicales.fr › Comportement et mécanismes comportementaux › Comportement › Comportement animal › Acte consommatoire › Comportement sexuel chez les animaux › Monogamie › Intranasal oxytocin drives coordinated social approach.
questionsmedicales.fr › Comportement et mécanismes comportementaux › Comportement › Comportement animal › Acte consommatoire › Comportement sexuel chez les animaux › Intranasal oxytocin drives coordinated social approach.
questionsmedicales.fr › Comportement et mécanismes comportementaux › Comportement › Comportement social › Intranasal oxytocin drives coordinated social approach.