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A cortical filter that learns to suppress the acoustic consequences of movement

Author

Listed:
  • David M. Schneider

    (Duke University School of Medicine
    Center for Neural Science, New York University)

  • Janani Sundararajan

    (Duke University School of Medicine)

  • Richard Mooney

    (Duke University School of Medicine)

Abstract

Sounds can arise from the environment and also predictably from many of our own movements, such as vocalizing, walking, or playing music. The capacity to anticipate these movement-related (reafferent) sounds and distinguish them from environmental sounds is essential for normal hearing1,2, but the neural circuits that learn to anticipate the often arbitrary and changeable sounds that result from our movements remain largely unknown. Here we developed an acoustic virtual reality (aVR) system in which a mouse learned to associate a novel sound with its locomotor movements, allowing us to identify the neural circuit mechanisms that learn to suppress reafferent sounds and to probe the behavioural consequences of this predictable sensorimotor experience. We found that aVR experience gradually and selectively suppressed auditory cortical responses to the reafferent frequency, in part by strengthening motor cortical activation of auditory cortical inhibitory neurons that respond to the reafferent tone. This plasticity is behaviourally adaptive, as aVR-experienced mice showed an enhanced ability to detect non-reafferent tones during movement. Together, these findings describe a dynamic sensory filter that involves motor cortical inputs to the auditory cortex that can be shaped by experience to selectively suppress the predictable acoustic consequences of movement.

Suggested Citation

  • David M. Schneider & Janani Sundararajan & Richard Mooney, 2018. "A cortical filter that learns to suppress the acoustic consequences of movement," Nature, Nature, vol. 561(7723), pages 391-395, September.
    • Handle: RePEc:nat:nature:v:561:y:2018:i:7723:d:10.1038_s41586-018-0520-5
    DOI: 10.1038/s41586-018-0520-5
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    Cited by:

    1. Zhaoran Zhang & Edward Zagha, 2023. "Motor cortex gates distractor stimulus encoding in sensory cortex," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Omid A. Zobeiri & Kathleen E. Cullen, 2024. "Cerebellar Purkinje cells combine sensory and motor information to predict the sensory consequences of active self-motion in macaques," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Matthew F. Tang & Ehsan Kheradpezhouh & Conrad C. Y. Lee & J. Edwin Dickinson & Jason B. Mattingley & Ehsan Arabzadeh, 2023. "Expectation violations enhance neuronal encoding of sensory information in mouse primary visual cortex," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Joji Tsunada & Xiaoqin Wang & Steven J. Eliades, 2024. "Multiple processes of vocal sensory-motor interaction in primate auditory cortex," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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