Oxytocin modulates female sociosexual behavior through a specific class of prefrontal cortical interneurons

Nakajima, Miho; Görlich, Andreas; Heintz, Nathaniel

doi:10.1016/j.cell.2014.09.020

Cited by 262Neuroendocrine regulation and behaviorOlfactory and Sensory Function StudiesNeurotransmitter Receptor Influence on Behavior

Oxytocin modulates female sociosexual behavior through a specific class of prefrontal cortical interneurons

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Nakajima, Miho, Görlich, Andreas, Heintz, Nathaniel·2014·Cell

DOI 10.1016/j.cell.2014.09.020PMC PMC4206218

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Abstract

Human imaging studies have revealed that intranasal administration of the "prosocial" hormone oxytocin (OT) activates the frontal cortex, and this action of OT correlates with enhanced brain function in autism. Here, we report the discovery of a population of somatostatin (Sst)-positive, regular spiking interneurons that express the oxytocin receptor (OxtrINs). Silencing of OxtrINs in the medial prefrontal cortex (mPFC) of female mice resulted in loss of social interest in male mice specifically during the sexually receptive phase of the estrous cycle. This sociosexual deficit was also present in mice in which the Oxtr gene was conditionally deleted from the mPFC and in control mice infused with an Oxtr antagonist. Our data demonstrate a gender-, cell type-, and state-specific role for OT/Oxtr signaling in the mPFC and identify a latent cortical circuit element that may modulate other complex social behaviors in response to OT.

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Cortical oxytocin receptors are found primarily on parvalbumin-positive or somatostatin-positive inhibitory interneurons, including at inhibitory synaptic terminals.
“Cortical oxytocin receptors are found primarily on parvalbumin-positive or somatostatin-positive inhibitory interneurons”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Nakajima et al. 2014
The Results section (“An Oxtr Cre driver line targeting a specific population of cortical interneurons”; page unavailable) reports that Oxtr and Sst are enriched in the receptor-expressing interneurons. It also reports that Pvalb is not detected or is depleted in those cells, so the cited paper does not support the claim that cortical oxytocin receptors are found primarily on parvalbumin-positive or somatostatin-positive interneurons. (LLM, conf=0.88)
Experimental — accuracy not yet measured
A small subpopulation of Sst neurons in prefrontal cortex express oxytocin receptors, and this expression is critical for the modulation of sociosexual behavior by oxytocin.
“a small subpopulation of Sst neurons in prefrontal cortex express oxytocin receptors, and this expression is critical to the modulation of sociosexual behavior by this hormone (Nakajima et al., 2014).”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Nakajima et al., 2014
Sex-specific differences in the effects of activating oxytocin receptor positive medial prefrontal cortex interneurons have been reported, with activation inducing anxiety in males but promoting social behavior in females.
“For example, sex-specific differences in the effects of activating OXT receptor positive mPFC interneurons have been reported with activation inducing anxiety in males, but promoting social behavior in females [68,69].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [68]
Oxytocin is involved in homeostatic regulation of reflexes such as parturition and lactation.
“Oxytocin is involved not only in homeostatic regulation of reflexes such as parturition and lactation, but it is crucial part of other aspects of motherhood such as care and protection of the offspring (Marlin et al., 2015; Nakajima et al., 2014; Sabihi et al., 2014).”
From Neuromodulation of maternal circuits by oxytocin (2019) · cites this paper as Nakajima et al., 2014
Oxytocin is crucial for other aspects of motherhood such as care and protection of the offspring.
“Oxytocin is involved not only in homeostatic regulation of reflexes such as parturition and lactation, but it is crucial part of other aspects of motherhood such as care and protection of the offspring (Marlin et al., 2015; Nakajima et al., 2014; Sabihi et al., 2014).”
From Neuromodulation of maternal circuits by oxytocin (2019) · cites this paper as Nakajima et al., 2014

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GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits
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“Instead, somatostatin-positive interneurons are the main cell type expressing oxytocin receptors in medial prefrontal cortex (Nakajima et al. 2014).”
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Sex differences in anxiety and depression: circuits and mechanisms
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A distributed network for social cognition enriched for oxytocin receptors
Mitre, M., Marlin, B. J., Schiavo, J. K., Morina, E., Norden, S. E., Hackett, T. A., Aoki, C. J., Chao, M. V., & Froemke, R. C. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2409-15.2016 · Cited by 305 · see citing works
Hippocampal oxytocin receptors are necessary for discrimination of social stimuli
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Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice
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A rapidly acting glutamatergic ARC→PVH satiety circuit postsynaptically regulated by α-MSH
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A Cortical Circuit for Sexually Dimorphic Oxytocin-Dependent Anxiety Behaviors
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Oxytocin and vasopressin: linking pituitary neuropeptides and their receptors to social neurocircuits
Baribeau, D. A., & Anagnostou, E. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00335 · Cited by 229 · see citing works
Neuroanatomical Substrates of Rodent Social Behavior: The Medial Prefrontal Cortex and Its Projection Patterns
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Oxytocin Signaling in the Central Amygdala Modulates Emotion Discrimination in Mice
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Prefrontal somatostatin interneurons encode fear memory
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Somatostatin interneurons in the prefrontal cortex control affective state discrimination in mice
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The Neurobiology Shaping Affective Touch: Expectation, Motivation, and Meaning in the Multisensory Context
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Norepinephrine versus dopamine and their interaction in modulating synaptic function in the prefrontal cortex
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Distinct and Dynamic ON and OFF Neural Ensembles in the Prefrontal Cortex Code Social Exploration
Liang, B., Zhang, L., Barbera, G., Fang, W., Zhang, J., Chen, X., Chen, R., Li, Y., & Lin, D. (2018) · Neuron · doi:10.1016/j.neuron.2018.08.043 · Cited by 170 · see citing works
Oxytocin transforms firing mode of CA2 hippocampal neurons
Tirko, N. N., Eyring, K. W., Carcea, I., Mitre, M., Chao, M. V., Froemke, R. C., & Tsien, R. W. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.008 · Cited by 157 · see citing works
Age and sex differences in oxytocin and vasopressin V1a receptor binding densities in the rat brain: focus on the social decision-making network
Smith, C. J. W., Poehlmann, M. L., Li, S., Ratnaseelan, A. M., Bredewold, R., & Veenema, A. H. (2017) · Brain Structure and Function · doi:10.1007/s00429-016-1260-7 · Cited by 143 · see citing works
Oxytocin signaling in the medial amygdala is required for sex discrimination of social cues
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Complementary networks of cortical somatostatin interneurons enforce layer specific control
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Sex differences in the regulation of social and anxiety-related behaviors: insights from vasopressin and oxytocin brain systems
Bredewold, R., & Veenema, A. H. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.011 · Cited by 144 · see citing works
Social circuits and their dysfunction in autism spectrum disorder
Sato, M., Nakai, N., Fujima, S., Choe, K. Y., & Takumi, T. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02201-0 · Cited by 142 · see citing works
<scp>O</scp>xytocin modulation of neural circuits for social behavior
Marlin, B. J., & Froemke, R. C. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22452 · Cited by 130 · see citing works
Reconstruction of the Hypothalamo-Neurohypophysial System and Functional Dissection of Magnocellular Oxytocin Neurons in the Brain
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Sex differences in fear extinction
Velasco, E. R., Florido, A., Milad, M. R., & Andero, R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.05.020 · Cited by 125 · see citing works
Hypomethylation of miR-142 promoter and upregulation of microRNAs that target the oxytocin receptor gene in the autism prefrontal cortex
Mor, M., Nardone, S., Sams, D. S., & Elliott, E. (2015) · Molecular Autism · doi:10.1186/s13229-015-0040-1 · Cited by 118 · see citing works
Oxytocin Receptors Are Expressed by Glutamatergic Prefrontal Cortical Neurons That Selectively Modulate Social Recognition
Tan, Y., Singhal, S. M., Harden, S. W., Cahill, K. M., Nguyen, D.-T. M., Colón-Pérez, L. M., Sahagian, T. J., Thinschmidt, J. S., de Kloet, A. D., Febo, M., et al. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2944-18.2019 · Cited by 118 · see citing works
Oxytocin receptors modulate a social salience neural network in male prairie voles
Johnson, Z. V., Walum, H., Xiao, Y., Riefkohl, P. C., & Young, L. J. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.10.009 · Cited by 113 · see citing works
Quantitative cellular-resolution map of the oxytocin receptor in postnatally developing mouse brains
Newmaster, K. T., Nolan, Z. T., Chon, U., Vanselow, D. J., Weit, A. R., Tabbaa, M., Hidema, S., Nishimori, K., Hammock, E. A. D., & Kim, Y. (2020) · Nature Communications · doi:10.1038/s41467-020-15659-1 · Cited by 109 · see citing works
Oxytocin administration in neonates shapes hippocampal circuitry and restores social behavior in a mouse model of autism
Bertoni, A., Schaller, F., Tyzio, R., Gaillard, S., Santini, F., Xolin, M., Diabira, D., Vaidyanathan, R., Matarazzo, V. A., Medina, I., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01227-6 · Cited by 110 · see citing works
The long and the short of it – a perspective on peptidergic regulation of circuits and behaviour
Jékely, G., Melzer, S., Beets, I., Kadow, I. C. G., Koene, J. M., Haddad, S., & Holden-Dye, L. M. (2018) · Journal of Experimental Biology · doi:10.1242/jeb.166710 · Cited by 102 · see citing works
Social Decision-Making and the Brain: A Comparative Perspective
Tremblay, S., Sharika, K. M., & Platt, M. L. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.01.007 · Cited by 105 · 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
Role of oxytocin in the control of stress and food intake
Onaka, T., & Takayanagi, Y. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12700 · Cited by 98 · see citing works
Oxytocin receptor signaling in the hippocampus: Role in regulating neuronal excitability, network oscillatory activity, synaptic plasticity and social memory
Lin, Y.-T., & Hsu, K. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.10.003 · Cited by 97 · see citing works
Oxytocin and Parental Behaviors
Yoshihara, C., Numan, M., & Kuroda, K. O. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_11 · Cited by 102 · see citing works
Adolescent sleep shapes social novelty preference in mice
Bian, W.-J., Brewer, C. L., Kauer, J. A., & de Lecea, L. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01076-8 · Cited by 96 · see citing works
Species and cell-type properties of classically defined human and rodent neurons and glia
Xu, X., Stoyanova, E. I., Patriotis, A. L., Xing, J., Mash, D. C., & Heintz, N. (2018) · eLife · doi:10.7554/elife.37551 · Cited by 90 · see citing works
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Rapid Molecular Profiling of Defined Cell Types Using Viral TRAP
Nectow, A. R., Moya, M. V., Ekstrand, M. I., Mousa, A., McGuire, K. L., Sferrazza, C. E., Field, B. C., Rabinowitz, G. S., Sawicka, K., Liang, Y., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.03.048 · Cited by 92 · see citing works
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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
Oxytocin and Stress: Neural Mechanisms, Stress-Related Disorders, and Therapeutic Approaches
Matsushita, H., Latt, H. M., Koga, Y., Nishiki, T., & Matsui, H. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.07.046 · Cited by 92 · see citing works
The role of social cognition in parasite and pathogen avoidance
Kavaliers, M., & Choleris, E. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2017.0206 · Cited by 85 · see citing works
Increased anxiety and decreased sociability induced by paternal deprivation involve the PVN-PrL OTergic pathway
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Oxytocin normalizes altered circuit connectivity for social rescue of the Cntnap2 knockout mouse
Choe, K. Y., Bethlehem, R. A. I., Safrin, M., Dong, H., Salman, E., Li, Y., Grinevich, V., Golshani, P., DeNardo, L. A., Peñagarikano, O., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.11.031 · Cited by 77 · see citing works
Oxytocin in the medial prefrontal cortex attenuates anxiety: Anatomical and receptor specificity and mechanism of action
Sabihi, S., Dong, S. M., Maurer, S., Goodpaster, C. M., & Leuner, B. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.06.024 · Cited by 84 · see citing works
Transcriptomic correlates of neuron electrophysiological diversity
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Neural coding of sex-specific social information in the mouse brain
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Bombesin-Like Peptide Recruits Disinhibitory Cortical Circuits and Enhances Fear Memories
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The social dilemma: prefrontal control of mammalian sociability
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Oxytocin promotes prefrontal population activity via the PVN-PFC pathway to regulate pain
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Control of fear by discrete prefrontal GABAergic populations encoding valence-specific information
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Oxytocin and Serotonin Brain Mechanisms in the Nonhuman Primate
Lefèvre, A., Richard, N., Jazayeri, M., Beuriat, P.-A., Fieux, S., Zimmer, L., Duhamel, J., & Angela Sirigu, B. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0659-17.2017 · Cited by 71 · see citing works
Neural circuits regulating prosocial behaviors
Walsh, J. J., Christoffel, D. J., & Malenka, R. C. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-022-01348-8 · Cited by 72 · see citing works
Oxytocin and Vasopressin Receptor Gene Polymorphisms: Role in Social and Psychiatric Traits
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Oxytocin and Rodent Models of Addiction
Leong, K.-C., Cox, S. S., King, C. E., Becker, H. C., & Reichel, C. M. (2018) · International review of neurobiology · doi:10.1016/bs.irn.2018.07.007 · Cited by 69 · see citing works
The role of oxytocin in alcohol and drug abuse
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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
The role of the prefrontal cortex in social interactions of animal models and the implications for autism spectrum disorder
Mohapatra, A. N., & Wagner, S. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1205199 · Cited by 67 · see citing works
Ethanol facilitates socially evoked memory recall in mice by recruiting pain-sensitive anterior cingulate cortical neurons
Sakaguchi, T., Iwasaki, S., Okada, M., Okamoto, K., & Ikegaya, Y. (2018) · Nature Communications · doi:10.1038/s41467-018-05894-y · Cited by 63 · see citing works
Oxytocin facilitates adaptive fear and attenuates anxiety responses in animal models and human studies—potential interaction with the corticotropin-releasing factor (CRF) system in the bed nucleus of the stria terminalis (BNST)
Janeček, M., & Dabrowska, J. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2889-8 · Cited by 61 · see citing works
Oxytocin attenuates deficits in social interaction but not recognition memory in a prenatal valproic acid-induced mouse model of autism
Hara, Y., Ago, Y., Higuchi, M., Hasebe, S., Nakazawa, T., Hashimoto, H., Matsuda, T., & Takuma, K. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.09.013 · Cited by 61 · see citing works
Oxytocin and Memory of Emotional Stimuli: Some Dance to Remember, Some Dance to Forget
Maroun, M., & Wagner, S. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.07.016 · Cited by 61 · see citing works
The Role of Hypothalamic Neuropeptides in Neurogenesis and Neuritogenesis
Bakoš, J., Zatkova, M., Bačová, Z., & Ostatníková, D. (2016) · Neural Plasticity · doi:10.1155/2016/3276383 · Cited by 61 · see citing works
Molecular and neural control of sexually dimorphic social behaviors
Yang, T., & Shah, N. M. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.04.015 · Cited by 61 · see citing works
Mate-choice copying, social information processing, and the roles of oxytocin
Kavaliers, M., Matta, R., & Choleris, E. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.003 · Cited by 60 · see citing works
The effects of intranasal oxytocin on reward circuitry responses in children with autism spectrum disorder
Greene, R. K., Spanos, M., Alderman, C., Walsh, E., Bizzell, J., Mosner, M. G., Kinard, J. L., Stuber, G. D., Chandrasekhar, T., Politte, L. C., et al. (2018) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-018-9228-y · Cited by 55 · see citing works
The modulation of emotional and social behaviors by oxytocin signaling in limbic network
Triana-Del Rio, R., Ranade, S., Guardado, J., LeDoux, J., Klann, E., & Shrestha, P. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1002846 · Cited by 58 · see citing works
Translating Oxytocin Neuroscience to the Clinic: A National Institute of Mental Health Perspective
Insel, T. R. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.02.002 · Cited by 56 · see citing works
Neuromodulation of maternal circuits by oxytocin
Valtcheva, S., & Froemke, R. C. (2019) · Cell and Tissue Research · doi:10.1007/s00441-018-2883-1 · Cited by 54 · see citing works
Involvement of oxytocin and GABA in consolation behavior elicited by socially defeated individuals in mandarin voles
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From classic ethology to modern neuroethology: overcoming the three biases in social behavior research
Zilkha, N., Sofer, Y., Beny, Y., & Kimchi, T. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.04.014 · Cited by 51 · see citing works
Oxytocin attenuates stress-induced reinstatement of alcohol seeking behavior in male and female mice
King, C. E., & Becker, H. C. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05233-z · Cited by 53 · see citing works
Oxytocin and excitation/inhibition balance in social recognition
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Hormones and Female Sexual Dysfunction: Beyond Estrogens and Androgens—Findings From the Fourth International Consultation on Sexual Medicine
Worsley, R., Santoro, N. F., Miller, K. K., Parish, S. J., & Davis, S. R. (2016) · The Journal of Sexual Medicine · doi:10.1016/j.jsxm.2015.12.014 · Cited by 50 · see citing works
Inhibitory microcircuit modules in hippocampal learning
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Implication of the social function of excessive self-grooming behavior in BTBR T+ltpr3tf/J mice as an idiopathic model of autism
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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
Oxytocin Exerts Antidepressant-like effect by potentiating dopaminergic synaptic transmission in the mPFC
Li, Q., Zhang, B., Cao, H., Liu, W., Guo, F., Shen, F., Ye, B., Liu, H., Li, Y., & Liu, Z. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107836 · Cited by 47 · see citing works
Neurobiological Aspects of Face Recognition: The Role of Oxytocin
Lopatina, O. L., Komleva, Y. K., Gorina, Y. V., Higashida, H., & Salmina, A. B. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00195 · Cited by 49 · see citing works
Convergent neuroendocrine mechanisms of social buffering and stress contagion
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Ascending Control of Arousal and Motivation: Role of Nucleus Incertus and its Peptide Neuromodulators in Behavioural Responses to Stress
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Intranasal oxytocin and OXTR genotype effects on resting state functional connectivity: A systematic review
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Self-citation
Oxytocin Receptors are expressed on Neurons within the Prefrontal Cortex that Control Preference for Social Novelty
Tan, Y., Singhal, S. M., Hiller, H., Nguyen, D.-T. M., Colón-Pérez, L. M., Febo, M., Wang, L. A., de Kloet, A. D., Frazier, C. J., & Krause, E. G. (2017) · The FASEB Journal · doi:10.1096/fasebj.31.1_supplement.1076.13 · Cited by 1 · see citing works

Authors: Nakajima, M., Görlich, A., & Heintz, N.
Affiliations: Howard Hughes Medical Institute (US)
Corresponding author: Heintz, Nathaniel
ORCID: Heintz, Nathaniel
Venue: Cell
Publisher: Elsevier BV
Published: 2014-10
Volume: 159
Issue: 2
Pages: 295-305
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2014.09.020
PMC: PMC4206218
OpenAlex: W2162459454
Cited by: 262
References: 80
Citations by year: 2026: 16 · 2025: 18 · 2024: 17 · 2023: 16 · 2022: 23 · 2021: 21 · 2020: 24 · 2019: 20 · 2018: 40 · 2017: 25 · 2016: 26 · 2015: 14 · 2014: 2
FWCI: 33.04
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 373 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Howard Hughes Medical Institute
National Institutes of Health
National Institute of Mental Health (P50MH090963, MH090963)
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, oxytocin receptor, medial prefrontal cortex, somatostatin interneurons, sociosexual behavior, female sexual behavior, estrous cycle, social behavior, conditional gene deletion, autism spectrum disorder
MeSH terms: Animals, Female, Interneurons, Male, Oxytocin, Sexual Behavior, Animal, Sex Characteristics, Social Behavior, Prefrontal Cortex, Receptors, Oxytocin, Estrous Cycle, Mice

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Oxytocin modulates female sociosexual behavior through a specific class of prefrontal cortical interneurons

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