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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
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    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.
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    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.

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