IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41641-8.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41641-8
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-41641-8?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. Andrea Bonassi & Ilaria Cataldo & Giulio Gabrieli & Moses Tandiono & Jia Nee Foo & Bruno Lepri & Gianluca Esposito, 2022. "The Interaction between Serotonin Transporter Allelic Variation and Maternal Care Modulates Instagram Sociability in a Sample of Singaporean Users," IJERPH, MDPI, vol. 19(9), pages 1-15, April.
    3. Masakazu Agetsuma & Issei Sato & Yasuhiro R. Tanaka & Luis Carrillo-Reid & Atsushi Kasai & Atsushi Noritake & Yoshiyuki Arai & Miki Yoshitomo & Takashi Inagaki & Hiroshi Yukawa & Hitoshi Hashimoto & J, 2023. "Activity-dependent organization of prefrontal hub-networks for associative learning and signal transformation," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    4. Roberto de la Torre-Martinez & Maya Ketzef & Gilad Silberberg, 2023. "Ongoing movement controls sensory integration in the dorsolateral striatum," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Henry W. Kietzman & Gracy Trinoskey-Rice & Sarah A. Blumenthal & Jidong D. Guo & Shannon L. Gourley, 2022. "Social incentivization of instrumental choice in mice requires amygdala-prelimbic cortex-nucleus accumbens connectivity," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    6. Sam Gijsen & Miro Grundei & Robert T Lange & Dirk Ostwald & Felix Blankenburg, 2021. "Neural surprise in somatosensory Bayesian learning," PLOS Computational Biology, Public Library of Science, vol. 17(2), pages 1-36, February.
    7. Julie E Elie & Frédéric E Theunissen, 2019. "Invariant neural responses for sensory categories revealed by the time-varying information for communication calls," PLOS Computational Biology, Public Library of Science, vol. 15(9), pages 1-43, September.
    8. Hyosang Kim & Doyoun Kim & Yisul Cho & Kyungdeok Kim & Junyeop Daniel Roh & Yangsik Kim & Esther Yang & Seong Soon Kim & Sunjoo Ahn & Hyun Kim & Hyojin Kang & Yongchul Bae & Eunjoon Kim, 2022. "Early postnatal serotonin modulation prevents adult-stage deficits in Arid1b-deficient mice through synaptic transcriptional reprogramming," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    9. Ana M. G. Manea & David J.-N. Maisson & Benjamin Voloh & Anna Zilverstand & Benjamin Hayden & Jan Zimmermann, 2024. "Neural timescales reflect behavioral demands in freely moving rhesus macaques," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    10. Kyuhyun Choi & Eugenio Piasini & Edgar Díaz-Hernández & Luigim Vargas Cifuentes & Nathan T. Henderson & Elizabeth N. Holly & Manivannan Subramaniyan & Charles R. Gerfen & Marc V. Fuccillo, 2023. "Distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    11. Hadar Levi-Aharoni & Oren Shriki & Naftali Tishby, 2020. "Surprise response as a probe for compressed memory states," PLOS Computational Biology, Public Library of Science, vol. 16(2), pages 1-21, February.
    12. Shinichiro Kira & Houman Safaai & Ari S. Morcos & Stefano Panzeri & Christopher D. Harvey, 2023. "A distributed and efficient population code of mixed selectivity neurons for flexible navigation decisions," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    13. Roxana Zeraati & Yan-Liang Shi & Nicholas A. Steinmetz & Marc A. Gieselmann & Alexander Thiele & Tirin Moore & Anna Levina & Tatiana A. Engel, 2023. "Intrinsic timescales in the visual cortex change with selective attention and reflect spatial connectivity," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    14. Thomas Akam & Rui Costa & Peter Dayan, 2015. "Simple Plans or Sophisticated Habits? State, Transition and Learning Interactions in the Two-Step Task," PLOS Computational Biology, Public Library of Science, vol. 11(12), pages 1-25, December.
    15. Allen P. F. Chen & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Shaoyu Ge & Qiaojie Xiong, 2023. "Nigrostriatal dopamine modulates the striatal-amygdala pathway in auditory fear conditioning," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    16. Zihao Chen & Yechao Han & Zheng Ma & Xinnian Wang & Surui Xu & Yong Tang & Alexei L. Vyssotski & Bailu Si & Yang Zhan, 2024. "A prefrontal-thalamic circuit encodes social information for social recognition," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    17. Jelena Katic & Yuichi Morohashi & Yoko Yazaki-Sugiyama, 2022. "Neural circuit for social authentication in song learning," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    18. M. E. Flanigan & O. J. Hon & S. D’Ambrosio & K. M. Boyt & L. Hassanein & M. Castle & H. L. Haun & M. M. Pina & T. L. Kash, 2023. "Subcortical serotonin 5HT2c receptor-containing neurons sex-specifically regulate binge-like alcohol consumption, social, and arousal behaviors in mice," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    19. Xin Wei Chia & Jian Kwang Tan & Lee Fang Ang & Tsukasa Kamigaki & Hiroshi Makino, 2023. "Emergence of cortical network motifs for short-term memory during learning," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    20. Matthijs N. Oude Lohuis & Jean L. Pie & Pietro Marchesi & Jorrit S. Montijn & Christiaan P. J. Kock & Cyriel M. A. Pennartz & Umberto Olcese, 2022. "Multisensory task demands temporally extend the causal requirement for visual cortex in perception," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41641-8. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.