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Oxytocin enables maternal behaviour by balancing cortical inhibition

Author

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  • Bianca J. Marlin

    (Skirball Institute for Biomolecular Medicine, New York University School of Medicine
    Neuroscience Institute, New York University School of Medicine
    New York University School of Medicine
    New York University School of Medicine)

  • Mariela Mitre

    (Skirball Institute for Biomolecular Medicine, New York University School of Medicine
    Neuroscience Institute, New York University School of Medicine
    New York University School of Medicine
    New York University School of Medicine)

  • James A. D’amour

    (Skirball Institute for Biomolecular Medicine, New York University School of Medicine
    Neuroscience Institute, New York University School of Medicine
    New York University School of Medicine
    New York University School of Medicine)

  • Moses V. Chao

    (Skirball Institute for Biomolecular Medicine, New York University School of Medicine
    Neuroscience Institute, New York University School of Medicine
    New York University School of Medicine
    New York University School of Medicine)

  • Robert C. Froemke

    (Skirball Institute for Biomolecular Medicine, New York University School of Medicine
    Neuroscience Institute, New York University School of Medicine
    New York University School of Medicine
    New York University School of Medicine)

Abstract

Oxytocin is important for social interactions and maternal behaviour. However, little is known about when, where and how oxytocin modulates neural circuits to improve social cognition. Here we show how oxytocin enables pup retrieval behaviour in female mice by enhancing auditory cortical pup call responses. Retrieval behaviour required the left but not right auditory cortex, was accelerated by oxytocin in the left auditory cortex, and oxytocin receptors were preferentially expressed in the left auditory cortex. Neural responses to pup calls were lateralized, with co-tuned and temporally precise excitatory and inhibitory responses in the left cortex of maternal but not pup-naive adults. Finally, pairing calls with oxytocin enhanced responses by balancing the magnitude and timing of inhibition with excitation. Our results describe fundamental synaptic mechanisms by which oxytocin increases the salience of acoustic social stimuli. Furthermore, oxytocin-induced plasticity provides a biological basis for lateralization of auditory cortical processing.

Suggested Citation

  • Bianca J. Marlin & Mariela Mitre & James A. D’amour & Moses V. Chao & Robert C. Froemke, 2015. "Oxytocin enables maternal behaviour by balancing cortical inhibition," Nature, Nature, vol. 520(7548), pages 499-504, April.
  • Handle: RePEc:nat:nature:v:520:y:2015:i:7548:d:10.1038_nature14402
    DOI: 10.1038/nature14402
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    Cited by:

    1. Nihaad Paraouty & Justin D. Yao & Léo Varnet & Chi-Ning Chou & SueYeon Chung & Dan H. Sanes, 2023. "Sensory cortex plasticity supports auditory social learning," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Yishan Qu & Lizi Zhang & Wenjuan Hou & Limin Liu & Jing Liu & Lu Li & Xing Guo & Yin Li & Caihong Huang & Zhixiong He & Fadao Tai, 2024. "Distinct medial amygdala oxytocin receptor neurons projections respectively control consolation or aggression in male mandarin voles," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    3. David Wolf & Renée Hartig & Yi Zhuo & Max F. Scheller & Mirko Articus & Marcel Moor & Valery Grinevich & Christiane Linster & Eleonora Russo & Wolfgang Weber-Fahr & Jonathan R. Reinwald & Wolfgang Kel, 2024. "Oxytocin induces the formation of distinctive cortical representations and cognitions biased toward familiar mice," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    4. Allen P. F. Chen & Jeffrey M. Malgady & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Joshua L. Plotkin & Shaoyu Ge & Qiaojie Xiong, 2022. "Nigrostriatal dopamine pathway regulates auditory discrimination behavior," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Masafumi Tsurutani & Teppei Goto & Mitsue Hagihara & Satsuki Irie & Kazunari Miyamichi, 2024. "Selective vulnerability of parvocellular oxytocin neurons in social dysfunction," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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