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A cortico-cerebellar loop for motor planning

Author

Listed:
  • Zhenyu Gao

    (Erasmus MC)

  • Courtney Davis

    (Baylor College of Medicine)

  • Alyse M. Thomas

    (Baylor College of Medicine)

  • Michael N. Economo

    (Janelia Research Campus)

  • Amada M. Abrego

    (Baylor College of Medicine)

  • Karel Svoboda

    (Janelia Research Campus)

  • Chris I. Zeeuw

    (Erasmus MC
    Netherlands Institute for Neuroscience)

  • Nuo Li

    (Baylor College of Medicine
    Janelia Research Campus)

Abstract

Persistent and ramping neural activity in the frontal cortex anticipates specific movements1–6. Preparatory activity is distributed across several brain regions7,8, but it is unclear which brain areas are involved and how this activity is mediated by multi-regional interactions. The cerebellum is thought to be primarily involved in the short-timescale control of movement9–12; however, roles for this structure in cognitive processes have also been proposed13–16. In humans, cerebellar damage can cause defects in planning and working memory13. Here we show that persistent representation of information in the frontal cortex during motor planning is dependent on the cerebellum. Mice performed a sensory discrimination task in which they used short-term memory to plan a future directional movement. A transient perturbation in the medial deep cerebellar nucleus (fastigial nucleus) disrupted subsequent correct responses without hampering movement execution. Preparatory activity was observed in both the frontal cortex and the cerebellar nuclei, seconds before the onset of movement. The silencing of frontal cortex activity abolished preparatory activity in the cerebellar nuclei, and fastigial activity was necessary to maintain cortical preparatory activity. Fastigial output selectively targeted the behaviourally relevant part of the frontal cortex through the thalamus, thus closing a cortico-cerebellar loop. Our results support the view that persistent neural dynamics during motor planning is maintained by neural circuits that span multiple brain regions17, and that cerebellar computations extend beyond online motor control13–15,18.

Suggested Citation

  • Zhenyu Gao & Courtney Davis & Alyse M. Thomas & Michael N. Economo & Amada M. Abrego & Karel Svoboda & Chris I. Zeeuw & Nuo Li, 2018. "A cortico-cerebellar loop for motor planning," Nature, Nature, vol. 563(7729), pages 113-116, November.
  • Handle: RePEc:nat:nature:v:563:y:2018:i:7729:d:10.1038_s41586-018-0633-x
    DOI: 10.1038/s41586-018-0633-x
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    Citations

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    Cited by:

    1. Ken-ichi Okada & Ryuji Takeya & Masaki Tanaka, 2022. "Neural signals regulating motor synchronization in the primate deep cerebellar nuclei," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Huee Ru Chong & Yadollah Ranjbar-Slamloo & Malcolm Zheng Hao Ho & Xuan Ouyang & Tsukasa Kamigaki, 2023. "Functional alterations of the prefrontal circuit underlying cognitive aging in mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Alyse Thomas & Weiguo Yang & Catherine Wang & Sri Laasya Tipparaju & Guang Chen & Brennan Sullivan & Kylie Swiekatowski & Mahima Tatam & Charles Gerfen & Nuo Li, 2023. "Superior colliculus bidirectionally modulates choice activity in frontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    4. A. Barri & M. T. Wiechert & M. Jazayeri & D. A. DiGregorio, 2022. "Synaptic basis of a sub-second representation of time in a neural circuit model," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    5. 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.
    6. Eric A. Kirk & Keenan T. Hope & Samuel J. Sober & Britton A. Sauerbrei, 2024. "An output-null signature of inertial load in motor cortex," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    7. Ellen Boven & Joseph Pemberton & Paul Chadderton & Richard Apps & Rui Ponte Costa, 2023. "Cerebro-cerebellar networks facilitate learning through feedback decoupling," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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