Oxytocin signaling in the medial amygdala is required for sex discrimination of social cues

Yao, Shenqin; Bergan, Joseph; Lanjuin, Anne; Dulac, Catherine

doi:10.7554/elife.31373

Cited by 151Neuroendocrine regulation and behaviorOlfactory and Sensory Function StudiesHypothalamic control of reproductive hormones

Oxytocin signaling in the medial amygdala is required for sex discrimination of social cues

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Yao, Shenqin, Bergan, Joseph, Lanjuin, Anne, Dulac, Catherine·2017·eLife

DOI 10.7554/elife.31373PMC PMC5768418

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Abstract

The neural control of social behaviors in rodents requires the encoding of pheromonal cues by the vomeronasal system. Here we show that the typical preference of male mice for females is eliminated in mutants lacking oxytocin, a neuropeptide modulating social behaviors in many species. Ablation of the oxytocin receptor in aromatase-expressing neurons of the medial amygdala (MeA) fully recapitulates the elimination of female preference in males. Further, single-unit recording in the MeA uncovered significant changes in the sensory representation of conspecific cues in the absence of oxytocin signaling. Finally, acute manipulation of oxytocin signaling in adults is sufficient to alter social interaction preferences in males as well as responses of MeA neurons to chemosensory cues. These results uncover the critical role of oxytocin signaling in a molecularly defined neuronal population in order to modulate the behavioral and physiological responses of male mice to females on a moment-to-moment basis.

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Ablating OXTR expression in aromatase-positive neurons in the medial amygdala abolishes male mouse preferences for females.
“Ablating OXTR expression in aromatase-positive neurons in the MeA abolishes male mouse preferences for females (96).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [96]
OXTRs in the medial amygdala receive oxytocin input from the paraventricular nucleus that help discriminate between sex and individual cues.
“OXTRs in the MeA receive OXT input from the PVN that help discriminate between sexand individual cues (53,74,96).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [96]

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Oxytocin, Neural Plasticity, and Social Behavior
Froemke, R. C., & Young, L. J. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-102320-102847 · Cited by 487 · see citing works
“This discrimination is impaired in males either if oxytocin signaling is systemically blocked (Li et al. 2017) or by selectively deleting oxytocin receptors from aromatase-positive neurons of the medial amygdala (Yao et al. 2017).”
Background
Functional circuit architecture underlying parental behaviour
Kohl, J., Babayan, B. M., Rubinstein, N. D., Autry, A. E., Marin-Rodriguez, B., Kapoor, V., Miyamichi, K., Zweifel, L. S., Luo, L., Uchida, N., et al. (2018) · Nature · doi:10.1038/s41586-018-0027-0 · Cited by 459 · see citing works
Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice
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Prefrontal–amygdala circuits in social decision-making
Gangopadhyay, P., Chawla, M., Monte, O. D., & Chang, S. W. C. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00738-9 · Cited by 247 · see citing works
Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities
Rigney, N., de Vries, G. J., Petrulis, A., & Young, L. J. (2022) · Endocrinology · doi:10.1210/endocr/bqac111 · Cited by 191 · see citing works
Responses and functions of dopamine in nucleus accumbens core during social behaviors
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An amygdala-to-hypothalamus circuit for social reward
Hu, R. K., Zuo, Y., Ly, T., Wang, J., Meera, P., Wu, Y. E., & Hong, W. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00828-2 · Cited by 174 · see citing works
A functional cellular framework for sex and estrous cycle-dependent gene expression and behavior
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Neural and Hormonal Control of Sexual Behavior
Jennings, K. J., & de Lecea, L. (2020) · Endocrinology · doi:10.1210/endocr/bqaa150 · Cited by 146 · see citing works
The neural circuitry of social homeostasis: Consequences of acute versus chronic social isolation
Lee, C. R., Chen, A., & Tye, K. M. (2021) · Cell · doi:10.1016/j.cell.2021.02.028 · Cited by 138 · see citing works
Interplay between Oxytocin and Sensory Systems in the Orchestration of Socio-Emotional Behaviors
Grinevich, V., & Stoop, R. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.016 · Cited by 139 · see citing works
Organization of neural circuits underlying social behavior: A consideration of the medial amygdala
Raam, T., & Hong, W. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.02.008 · Cited by 134 · see citing works
Limbic Neurons Shape Sex Recognition and Social Behavior in Sexually Naive Males
Bayless, D. W., Yang, T., Mason, M. M., Susanto, A. A. T., Lobdell, A., & Shah, N. M. (2019) · Cell · doi:10.1016/j.cell.2018.12.041 · Cited by 131 · see citing works
An insular view of the social decision-making network
Rogers-Carter, M. M., & Christianson, J. P. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.06.005 · Cited by 121 · see citing works
The zebrafish subcortical social brain as a model for studying social behavior disorders
Geng, Y., & Peterson, R. T. (2019) · Disease Models & Mechanisms · doi:10.1242/dmm.039446 · Cited by 111 · see citing works
Valence coding in amygdala circuits
Pignatelli, M., & Beyeler, A. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.10.010 · Cited by 120 · see citing works
Detection, processing and reinforcement of social cues: regulation by the oxytocin system
Menon, R., & Neumann, I. D. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00759-w · Cited by 100 · see citing works
Molecular Mechanisms of Oxytocin Signaling at the Synaptic Connection
Bakos, J., Srancikova, A., Havranek, T., & Bacova, Z. (2018) · Neural Plasticity · doi:10.1155/2018/4864107 · Cited by 104 · see citing works
Cortical Representations of Conspecific Sex Shape Social Behavior
Kingsbury, L., Huang, S., Raam, T., Ye, L. S., Don, W., Hu, R. K., Li, Y., & Hong, W. (2020) · Neuron · doi:10.1016/j.neuron.2020.06.020 · Cited by 86 · see citing works
The Neural Mechanisms of Sexually Dimorphic Aggressive Behaviors
Hashikawa, K., Hashikawa, Y., Lischinsky, J. E., & Lin, D. (2018) · Trends in Genetics · doi:10.1016/j.tig.2018.07.001 · Cited by 89 · see citing works
Insular cortex projections to nucleus accumbens core mediate social approach to stressed juvenile rats
Rogers-Carter, M. M., Djerdjaj, A., Gribbons, K. B., Varela, J. A., & Christianson, J. P. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.0316-19.2019 · Cited by 79 · see citing works
Neural coding of sex-specific social information in the mouse brain
Li, Y., & Dulac, C. G. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.07.005 · Cited by 73 · see citing works
What Is Health?
Sterling, P. (2020) · The MIT Press eBooks · doi:10.7551/mitpress/11472.001.0001 · Cited by 117 · see citing works
In the mood for sex: neural circuits for reproduction
Lenschow, C., & Lima, S. Q. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.12.001 · Cited by 71 · see citing works
Neuronal diversity of the amygdala and the bed nucleus of the stria terminalis
Beyeler, A., & Dabrowska, J. (2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-815134-1.00003-9 · Cited by 65 · see citing works
Mapping Central Projection of Oxytocin Neurons in Unmated Mice Using Cre and Alkaline Phosphatase Reporter
Liao, P., Chiu, Y.-M., Yu, J., & Chen, S. (2020) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2020.559402 · Cited by 68 · see citing works
Oxytocin and sex differences in behavior
Caldwell, H. K. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.02.002 · Cited by 64 · see citing works
Neural systems that facilitate the representation of social rank
Dwortz, M. F., Curley, J. P., Tye, K. M., & Padilla-Coreano, N. (2022) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2020.0444 · Cited by 64 · see citing works
Estrogen receptor 2b is the major determinant of sex-typical mating behavior and sexual preference in medaka
Nishiike, Y., Miyazoe, D., Togawa, R., Yokoyama, K., Nakasone, K., Miyata, M., Kikuchi, Y., Kamei, Y., Todo, T., Ishikawa‐Fujiwara, T., et al. (2021) · Current Biology · doi:10.1016/j.cub.2021.01.089 · Cited by 62 · see citing works
Oxytocin and Food Intake Control: Neural, Behavioral, and Signaling Mechanisms
Liu, C. M., Spaulding, M. O., Rea, J. J., Noble, E. E., & Kanoski, S. E. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910859 · Cited by 53 · see citing works
Neural circuits regulating sexual behaviors via the olfactory system in mice
Ishii, K. K., & Touhara, K. (2018) · Neuroscience Research · doi:10.1016/j.neures.2018.10.009 · Cited by 53 · see citing works
Brain circuits that regulate social behavior
Li, H., Zhao, Z., Jiang, S., & Wu, H. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03037-6 · Cited by 57 · see citing works
Sexually dimorphic control of affective state processing and empathic behaviors
Fang, S., Luo, Z.-Y., Wei, Z., Qin, Y., Zheng, J., Zhang, H., Jin, J., Li, J., Miao, C., Yang, S., et al. (2024) · Neuron · doi:10.1016/j.neuron.2024.02.001 · Cited by 45 · see citing works
Reviving-like prosocial behavior in response to unconscious or dead conspecifics in rodents
Sun, W., Zhang, G., Huang, J., Tao, C., Seo, M. B., Tao, H. W., & Zhang, L. I. (2025) · Science · doi:10.1126/science.adq2677 · Cited by 40 · see citing works
Human Primary Olfactory Amygdala Subregions Form Distinct Functional Networks, Suggesting Distinct Olfactory Functions
Noto, T., Zhou, G., Yang, Q., Lane, G., & Zelano, C. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.752320 · Cited by 38 · see citing works
Oxytocin signaling in the posterior hypothalamus prevents hyperphagic obesity in mice
Inada, K., Tsujimoto, K., Yoshida, M., Nishimori, K., & Miyamichi, K. (2022) · eLife · doi:10.7554/elife.75718 · Cited by 39 · see citing works
Neural circuit control of innate behaviors
Wei, X., Jiao, Z., Senol, E., Yao, J., Zhao, M., Zhao, Z., Chen, X., Cao, P., Fu, Y., Gao, Z., et al. (2021) · Science China Life Sciences · doi:10.1007/s11427-021-2043-2 · Cited by 38 · see citing works
Brain functional networks associated with social bonding in monogamous voles
López-Gutiérrez, M. F., Gracia-Tabuenca, Z., Ortiz, J. J., Camacho, F., Young, L. J., Paredes, R. G., Díaz, N. F., Portillo, W., & Alcauter, S. (2021) · eLife · doi:10.7554/elife.55081 · Cited by 40 · see citing works
Intertwined associations between oxytocin, immune system and major depressive disorder
Jiang, J., Yang, M., Tian, M., Chen, Z., Xiao, L., & Gong, Y. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114852 · Cited by 36 · see citing works
PDF-1 neuropeptide signaling regulates sexually dimorphic gene expression in shared sensory neurons of C. elegans
Hilbert, Z. A., & Kim, D. H. (2018) · eLife · doi:10.7554/elife.36547 · Cited by 32 · see citing works
Indispensable role of the oxytocin receptor for allogrooming toward socially distressed cage mates in female mice
Matsumoto, M., Yoshida, M., Jayathilake, B. W., Inutsuka, A., Nishimori, K., Takayanagi, Y., & Onaka, T. (2021) · Journal of Neuroendocrinology · doi:10.1111/jne.12980 · Cited by 32 · see citing works
Fish as a model in social neuroscience: conservation and diversity in the social brain network
Ogawa, S., Pfaff, D. W., & Parhar, I. S. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12689 · Cited by 31 · see citing works
Neural Circuits Underlying Rodent Sociality: A Comparative Approach
Lee, N. S., & Beery, A. K. (2019) · Current topics in behavioral neurosciences · doi:10.1007/7854_2018_77 · Cited by 31 · see citing works
Structure and function of the medial amygdala
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Oxytocin as an Anti-obesity Treatment
Niu, J., Tong, J., & Blevins, J. E. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.743546 · Cited by 30 · see citing works
Sexual Differentiation and Sex Differences in Neural Development
Turano, A., Osborne, B. F., & Schwarz, J. M. (2018) · Current topics in behavioral neurosciences · doi:10.1007/7854_2018_56 · Cited by 29 · see citing works
Mapping the neural circuitry of predator fear in the nonhuman primate
Montardy, Q., Kwan, W. C., Mundiñano, I.-C., Fox, D. M., Wang, L., Gross, C. T., & Bourne, J. A. (2020) · Brain Structure and Function · doi:10.1007/s00429-020-02176-6 · Cited by 28 · see citing works
Neural control of sexually dimorphic social behaviors
McKinsey, G. L., Ahmed, O. M., & Shah, N. M. (2018) · Current Opinion in Physiology · doi:10.1016/j.cophys.2018.08.003 · Cited by 26 · see citing works
Neural mechanisms of comforting: Prosocial touch and stress buffering
Lim, K. Y., & Hong, W. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105391 · Cited by 29 · see citing works
Social modulation of fear: Facilitation vs buffering
Morozov, A., & Ito, W. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12491 · Cited by 27 · see citing works
Neural activation associated with outgroup helping in adolescent rats
Breton, J., Eisner, J. S., Gandhi, V. S., Musick, N., Zhang, A., Long, K. L. P., Perloff, O. S., Hu, K. Y., Pham, C. M., Lalchandani, P., et al. (2022) · iScience · doi:10.1016/j.isci.2022.104412 · Cited by 26 · see citing works
A combinatorial modulation of synaptic plasticity in the rat medial amygdala by oxytocin, urocortin3 and estrogen
Frankiensztajn, L. M., Gur-Pollack, R., & Wagner, S. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.04.006 · Cited by 27 · see citing works
Synaptic Connections of Aromatase Circuits in the Medial Amygdala Are Sex Specific
Billing, A., Correia, M. H., Kelly, D. A., Li, G., & Bergan, J. F. (2020) · eNeuro · doi:10.1523/eneuro.0489-19.2020 · Cited by 25 · see citing works
The paraventricular nucleus of the hypothalamus: a key node in the control of behavioural states
Iremonger, K. J., & Power, E. M. (2025) · The Journal of Physiology · doi:10.1113/jp288366 · Cited by 33 · see citing works
Peripheral oxytocin injection modulates vomeronasal sensory activity and reduces pup-directed aggression in male mice
Nakahara, T. S., Camargo, A. P., Magalhães, P. H. M., Souza, M. A. A., Ribeiro, P. G., Netto, P. H. M., Carvalho, V. M. D. A., José, J., & Papes, F. (2020) · Scientific Reports · doi:10.1038/s41598-020-77061-7 · Cited by 24 · see citing works
Neural circuit mechanisms that govern inter-male attack in mice
Zha, X., & Xu, X. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03956-x · Cited by 24 · see citing works
A neural circuit perspective on brain aromatase
Spool, J. A., Bergan, J. F., & Remage‐Healey, L. (2021) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2021.100973 · Cited by 25 · see citing works
Representation of sex-specific social memory in ventral CA1 neurons
Watarai, A., Tao, K., & Okuyama, T. (2025) · Science · doi:10.1126/science.adp3814 · Cited by 22 · see citing works
Pharmacological modulation of AMPA receptors rescues specific impairments in social behavior associated with the A350V Iqsec2 mutation
Jabarin, R., Levy, N. S., Abergel, Y., Berman, J. H., Zag, A., Netser, S., Levy, A. P., & Wagner, S. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01347-1 · Cited by 21 · see citing works
A neural basis for prosocial behavior toward unresponsive individuals
Sun, F., Wu, Y. E., & Hong, W. (2025) · Science · doi:10.1126/science.adq2679 · Cited by 21 · see citing works
A sex‐specific feedback projection from aromatase‐expressing neurons in the medial amygdala to the accessory olfactory bulb
Inbar, T., Davis, R. A., & Bergan, J. F. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25236 · Cited by 22 · see citing works
Somatosensorimotor and Odor Modification, Along with Serotonergic Processes Underlying the Social Deficits in BTBR T+ Itpr3tf/J and BALB/cJ Mouse Models of Autism
Arakawa, H. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.02.002 · Cited by 20 · see citing works
Distinct medial amygdala oxytocin receptor neurons projections respectively control consolation or aggression in male mandarin voles
Qu, Y., Zhang, L., Hou, W., Liu, L., Liu, J., Li, L., Guo, X., Yin, L., Huang, C., He, Z., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-51652-8 · Cited by 21 · see citing works
Neural and Hormonal Basis of Opposite-Sex Preference by Chemosensory Signals
Kondo, Y., & Hayashi, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158311 · Cited by 18 · see citing works
Sex Differences in Biophysical Signatures across Molecularly Defined Medial Amygdala Neuronal Subpopulations
Matos, H. Y., Hernandez‐Pineda, D., Charpentier, C. M., Rusk, A., Corbin, J. G., & Jones, K. S. (2020) · eNeuro · doi:10.1523/eneuro.0035-20.2020 · Cited by 19 · see citing works
Leptin enhances social motivation and reverses chronic unpredictable stress-induced social anhedonia during adolescence
Lei, Y., Wang, D., Bai, Y., Nougaisse, J., Weintraub, N. L., Guo, M., & Lu, X. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01778-2 · Cited by 18 · see citing works
Silencing and stimulating the medial amygdala impairs ejaculation but not sexual incentive motivation in male rats
Huijgens, P. T., Heijkoop, R., & Snoeren, E. M. S. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113206 · Cited by 17 · see citing works
Phosphorylation-dependent positive feedback on the oxytocin receptor through the kinase PKD1 contributes to long-term social memory
Wang, F., Yin, X.-S., Lu, J., Cen, C., & Wang, Y. (2022) · Science Signaling · doi:10.1126/scisignal.abd0033 · Cited by 15 · see citing works
Distinct Dynamics of Theta and Gamma Rhythmicity during Social Interaction Suggest Differential Mode of Action in the Medial Amygdala of Sprague Dawley Rats and C57BL/6J Mice
John, S. R., Dagash, W., Mohapatra, A. N., Netser, S., & Wagner, S. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.04.020 · Cited by 16 · see citing works
Near-infrared nanosensors enable optical imaging of oxytocin with selectivity over vasopressin in acute mouse brain slices
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Authors: Yao, S., Bergan, J., Lanjuin, A., & Dulac, C.
Affiliations: Allen Institute for Brain Science (US)
Howard Hughes Medical Institute (US)
Corresponding author: Dulac, Catherine
ORCID: Yao, Shenqin
Bergan, Joseph
Lanjuin, Anne
Dulac, Catherine
Venue: eLife
Publisher: eLife Sciences Publications, Ltd
Published: 2017-12-12
Volume: 6
ISSN: 2050-084X (ISSN-L)
DOI: 10.7554/elife.31373
PMC: PMC5768418
OpenAlex: W2746264266
Cited by: 151
References: 108
Citations by year: 2026: 13 · 2025: 18 · 2024: 15 · 2023: 16 · 2022: 19 · 2021: 27 · 2020: 17 · 2019: 10 · 2018: 15 · 2017: 1
FWCI: 16.83
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
creativecommons.org/licenses/by/4.0/ (am)
creativecommons.org/licenses/by/4.0/ (tdm)
Locations: eLife (publishedVersion, cc-by)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders: Howard Hughes Medical Institute
National Institute on Deafness and Other Communication Disorders (R01DC013087)
Simons Foundation (Simons Foundation Autism Research Initiative - 308094)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Keywords: oxytocin signaling, medial amygdala, gender discrimination, social behavior, vomeronasal system, oxytocin receptor, female preference, social interaction, mice
MeSH terms: Amygdala, Animals, Cells, Cultured, Cues, Discrimination, Psychological, Female, Male, Mice, Inbred C57BL, Oxytocics, Oxytocin, Sensory Receptor Cells, Sexual Behavior, Animal, Social Behavior, Receptors, Oxytocin, Mice, Knockout, Mice

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Oxytocin signaling in the medial amygdala is required for sex discrimination of social cues

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