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Sensory cortex plasticity supports auditory social learning

Author

Listed:
  • Nihaad Paraouty

    (Center for Neural Science New York University)

  • Justin D. Yao

    (Rutgers University)

  • Léo Varnet

    (PSL University)

  • Chi-Ning Chou

    (Simons Foundation
    Harvard University)

  • SueYeon Chung

    (Center for Neural Science New York University
    Simons Foundation)

  • Dan H. Sanes

    (Center for Neural Science New York University
    New York University
    New York University
    NYU Langone Medical Center)

Abstract

Social learning (SL) through experience with conspecifics can facilitate the acquisition of many behaviors. Thus, when Mongolian gerbils are exposed to a demonstrator performing an auditory discrimination task, their subsequent task acquisition is facilitated, even in the absence of visual cues. Here, we show that transient inactivation of auditory cortex (AC) during exposure caused a significant delay in task acquisition during the subsequent practice phase, suggesting that AC activity is necessary for SL. Moreover, social exposure induced an improvement in AC neuron sensitivity to auditory task cues. The magnitude of neural change during exposure correlated with task acquisition during practice. In contrast, exposure to only auditory task cues led to poorer neurometric and behavioral outcomes. Finally, social information during exposure was encoded in the AC of observer animals. Together, our results suggest that auditory SL is supported by AC neuron plasticity occurring during social exposure and prior to behavioral performance.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41641-8
    DOI: 10.1038/s41467-023-41641-8
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    References listed on IDEAS

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    1. Caroline A. Runyan & Eugenio Piasini & Stefano Panzeri & Christopher D. Harvey, 2017. "Distinct timescales of population coding across cortex," Nature, Nature, vol. 548(7665), pages 92-96, August.
    2. Uri Cohen & SueYeon Chung & Daniel D. Lee & Haim Sompolinsky, 2020. "Separability and geometry of object manifolds in deep neural networks," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    3. Gül Dölen & Ayeh Darvishzadeh & Kee Wui Huang & Robert C. Malenka, 2013. "Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin," Nature, Nature, vol. 501(7466), pages 179-184, September.
    4. Gagan Narula & Joshua A. Herbst & Joerg Rychen & Richard H. R. Hahnloser, 2018. "Learning auditory discriminations from observation is efficient but less robust than learning from experience," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    5. Petr Znamenskiy & Anthony M. Zador, 2013. "Corticostriatal neurons in auditory cortex drive decisions during auditory discrimination," Nature, Nature, vol. 497(7450), pages 482-485, May.
    6. Masashi Tanaka & Fangmiao Sun & Yulong Li & Richard Mooney, 2018. "A mesocortical dopamine circuit enables the cultural transmission of vocal behaviour," Nature, Nature, vol. 563(7729), pages 117-120, November.
    7. 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.
    8. Ioana Carcea & Naomi López Caraballo & Bianca J. Marlin & Rumi Ooyama & Justin S. Riceberg & Joyce M. Mendoza Navarro & Maya Opendak & Veronica E. Diaz & Luisa Schuster & Maria I. Alvarado Torres & Ha, 2021. "Oxytocin neurons enable social transmission of maternal behaviour," Nature, Nature, vol. 596(7873), pages 553-557, August.
    9. Stephen M. Town & Katherine C. Wood & Jennifer K. Bizley, 2018. "Sound identity is represented robustly in auditory cortex during perceptual constancy," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    Full references (including those not matched with items on IDEAS)

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