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

Teppei Ebina, Akitaka Sasagawa, Dokyeong Hong, Rieko Setsuie, Keitaro Obara, Yoshito Masamizu, Masashi Kondo, Shin-Ichiro Terada, Katsuya Ozawa, Masato Uemura, Masafumi Takaji, Akiya Watakabe, Kenta Kobayashi, Kenichi Ohki, Tetsuo Yamamori, Masanori Murayama and Masanori Matsuzaki ()
Additional contact information
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
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
Akiya Watakabe: RIKEN Center for Brain Science
Kenta Kobayashi: National Institute for Physiological Sciences
Kenichi Ohki: The University of Tokyo
Tetsuo Yamamori: RIKEN Center for Brain Science
Masanori Murayama: RIKEN Center for Brain Science
Masanori Matsuzaki: The University of Tokyo

Nature Communications, 2024, vol. 15, issue 1, 1-21

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-51425-3

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