IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51425-3.html
   My bibliography  Save this article

Dynamics of directional motor tuning in the primate premotor and primary motor cortices during sensorimotor learning

Author

Listed:
  • Teppei Ebina

    (The University of Tokyo)

  • Akitaka Sasagawa

    (The University of Tokyo)

  • Dokyeong Hong

    (The University of Tokyo)

  • Rieko Setsuie

    (RIKEN Center for Brain Science)

  • Keitaro Obara

    (RIKEN Center for Brain Science)

  • Yoshito Masamizu

    (RIKEN Center for Brain Science
    Doshisha University)

  • Masashi Kondo

    (The University of Tokyo)

  • Shin-Ichiro Terada

    (The University of Tokyo)

  • Katsuya Ozawa

    (RIKEN Center for Brain Science)

  • Masato Uemura

    (The University of Tokyo)

  • Masafumi Takaji

    (RIKEN Center for Brain Science
    RIKEN Center for Brain Science
    Tokyo Institute of Technology)

  • Akiya Watakabe

    (RIKEN Center for Brain Science
    RIKEN Center for Brain Science)

  • Kenta Kobayashi

    (National Institute for Physiological Sciences)

  • Kenichi Ohki

    (The University of Tokyo
    The University of Tokyo Institutes for Advanced Study
    The University of Tokyo)

  • Tetsuo Yamamori

    (RIKEN Center for Brain Science
    RIKEN Center for Brain Science
    Central Institute of Experimental Animals)

  • Masanori Murayama

    (RIKEN Center for Brain Science)

  • Masanori Matsuzaki

    (The University of Tokyo
    RIKEN Center for Brain Science
    The University of Tokyo Institutes for Advanced Study
    The University of Tokyo)

Abstract

Sensorimotor learning requires reorganization of neuronal activity in the premotor cortex (PM) and primary motor cortex (M1). To reveal PM- and M1-specific reorganization in a primate, we conducted calcium imaging in common marmosets while they learned a two-target reaching (pull/push) task after mastering a one-target reaching (pull) task. Throughout learning of the two-target reaching task, the dorsorostral PM (PMdr) showed peak activity earlier than the dorsocaudal PM (PMdc) and M1. During learning, the reaction time in pull trials increased and correlated strongly with the peak timing of PMdr activity. PMdr showed decreasing representation of newly introduced (push) movement, whereas PMdc and M1 maintained high representation of pull and push movements. Many task-related neurons in PMdc and M1 exhibited a strong preference to either movement direction. PMdc neurons dynamically switched their preferred direction depending on their performance in push trials in the early learning stage, whereas M1 neurons stably retained their preferred direction and high similarity of preferred direction between neighbors. These results suggest that in primate sensorimotor learning, dynamic directional motor tuning in PMdc converts the sensorimotor association formed in PMdr to the stable and specific motor representation of M1.

Suggested Citation

  • Teppei Ebina & Akitaka Sasagawa & Dokyeong Hong & Rieko Setsuie & Keitaro Obara & Yoshito Masamizu & Masashi Kondo & Shin-Ichiro Terada & Katsuya Ozawa & Masato Uemura & Masafumi Takaji & Akiya Wataka, 2024. "Dynamics of directional motor tuning in the primate premotor and primary motor cortices during sensorimotor learning," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51425-3
    DOI: 10.1038/s41467-024-51425-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51425-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-51425-3?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. Teppei Ebina & Yoshito Masamizu & Yasuhiro R. Tanaka & Akiya Watakabe & Reiko Hirakawa & Yuka Hirayama & Riichiro Hira & Shin-Ichiro Terada & Daisuke Koketsu & Kazuo Hikosaka & Hiroaki Mizukami & Atsu, 2018. "Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    2. Keitaro Obara & Teppei Ebina & Shin-Ichiro Terada & Takanori Uka & Misako Komatsu & Masafumi Takaji & Akiya Watakabe & Kenta Kobayashi & Yoshito Masamizu & Hiroaki Mizukami & Tetsuo Yamamori & Kiyoto , 2023. "Change detection in the primate auditory cortex through feedback of prediction error signals," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Shinnosuke Nomura & Shin-Ichiro Terada & Teppei Ebina & Masato Uemura & Yoshito Masamizu & Kenichi Ohki & Masanori Matsuzaki, 2024. "ARViS: a bleed-free multi-site automated injection robot for accurate, fast, and dense delivery of virus to mouse and marmoset cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-23, December.

    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. Shinnosuke Nomura & Shin-Ichiro Terada & Teppei Ebina & Masato Uemura & Yoshito Masamizu & Kenichi Ohki & Masanori Matsuzaki, 2024. "ARViS: a bleed-free multi-site automated injection robot for accurate, fast, and dense delivery of virus to mouse and marmoset cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    2. Keitaro Obara & Teppei Ebina & Shin-Ichiro Terada & Takanori Uka & Misako Komatsu & Masafumi Takaji & Akiya Watakabe & Kenta Kobayashi & Yoshito Masamizu & Hiroaki Mizukami & Tetsuo Yamamori & Kiyoto , 2023. "Change detection in the primate auditory cortex through feedback of prediction error signals," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Jimin Wu & Yuzhi Chen & Ashok Veeraraghavan & Eyal Seidemann & Jacob T. Robinson, 2024. "Mesoscopic calcium imaging in a head-unrestrained male non-human primate using a lensless microscope," Nature Communications, Nature, vol. 15(1), pages 1-14, 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:15:y:2024:i:1:d:10.1038_s41467-024-51425-3. 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.