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A motor cortex circuit for motor planning and movement

Author

Listed:
  • Nuo Li

    (Janelia Research Campus, Howard Hughes Medical Institute)

  • Tsai-Wen Chen

    (Janelia Research Campus, Howard Hughes Medical Institute)

  • Zengcai V. Guo

    (Janelia Research Campus, Howard Hughes Medical Institute)

  • Charles R. Gerfen

    (Laboratory of Systems Neuroscience, National Institute of Mental Health)

  • Karel Svoboda

    (Janelia Research Campus, Howard Hughes Medical Institute)

Abstract

Activity in motor cortex predicts specific movements seconds before they occur, but how this preparatory activity relates to upcoming movements is obscure. We dissected the conversion of preparatory activity to movement within a structured motor cortex circuit. An anterior lateral region of the mouse cortex (a possible homologue of premotor cortex in primates) contains equal proportions of intermingled neurons predicting ipsi- or contralateral movements, yet unilateral inactivation of this cortical region during movement planning disrupts contralateral movements. Using cell-type-specific electrophysiology, cellular imaging and optogenetic perturbation, we show that layer 5 neurons projecting within the cortex have unbiased laterality. Activity with a contralateral population bias arises specifically in layer 5 neurons projecting to the brainstem, and only late during movement planning. These results reveal the transformation of distributed preparatory activity into movement commands within hierarchically organized cortical circuits.

Suggested Citation

  • Nuo Li & Tsai-Wen Chen & Zengcai V. Guo & Charles R. Gerfen & Karel Svoboda, 2015. "A motor cortex circuit for motor planning and movement," Nature, Nature, vol. 519(7541), pages 51-56, March.
    • Handle: RePEc:nat:nature:v:519:y:2015:i:7541:d:10.1038_nature14178
    DOI: 10.1038/nature14178
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    Cited by:

    1. Christopher M. Kim & Arseny Finkelstein & Carson C. Chow & Karel Svoboda & Ran Darshan, 2023. "Distributing task-related neural activity across a cortical network through task-independent connections," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    2. Yanjie Wang & Zhaonan Chen & Guofen Ma & Lizhao Wang & Yanmei Liu & Meiling Qin & Xiang Fei & Yifan Wu & Min Xu & Siyu Zhang, 2023. "A frontal transcallosal inhibition loop mediates interhemispheric balance in visuospatial processing," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    3. Ignacio Alonso & Irina Scheer & Mélanie Palacio-Manzano & Noémie Frézel-Jacob & Antoine Philippides & Mario Prsa, 2023. "Peripersonal encoding of forelimb proprioception in the mouse somatosensory cortex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Sebastian Reinartz & Arash Fassihi & Maria Ravera & Luciano Paz & Francesca Pulecchi & Marco Gigante & Mathew E. Diamond, 2024. "Direct contribution of the sensory cortex to the judgment of stimulus duration," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    5. Yanmei Liu & Jiahe Zhang & Zhishan Jiang & Meiling Qin & Min Xu & Siyu Zhang & Guofen Ma, 2024. "Organization of corticocortical and thalamocortical top-down inputs in the primary visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    6. Xuandi Hou & Jianing Jing & Yizhou Jiang & Xiaohui Huang & Quanxiang Xian & Ting Lei & Jiejun Zhu & Kin Fung Wong & Xinyi Zhao & Min Su & Danni Li & Langzhou Liu & Zhihai Qiu & Lei Sun, 2024. "Nanobubble-actuated ultrasound neuromodulation for selectively shaping behavior in mice," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. Bowen Dempsey & Selvee Sungeelee & Phillip Bokiniec & Zoubida Chettouh & Séverine Diem & Sandra Autran & Evan R. Harrell & James F. A. Poulet & Carmen Birchmeier & Harry Carey & Auguste Genovesio & Si, 2021. "A medullary centre for lapping in mice," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    8. 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.
    9. Tristano Pancani & Michelle Day & Tatiana Tkatch & David L. Wokosin & Patricia González-Rodríguez & Jyothisri Kondapalli & Zhong Xie & Yu Chen & Vahri Beaumont & D. James Surmeier, 2023. "Cholinergic deficits selectively boost cortical intratelencephalic control of striatum in male Huntington’s disease model mice," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. Tanner C Dixon & Christina M Merrick & Joni D Wallis & Richard B Ivry & Jose M Carmena, 2021. "Hybrid dedicated and distributed coding in PMd/M1 provides separation and interaction of bilateral arm signals," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-35, November.
    11. Daniel G. Taub & Qiufen Jiang & Francesca Pietrafesa & Junfeng Su & Aloe Carroll & Caitlin Greene & Michael R. Blanchard & Aakanksha Jain & Mahmoud El-Rifai & Alexis Callen & Katherine Yager & Clara C, 2024. "The secondary somatosensory cortex gates mechanical and heat sensitivity," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    12. Laura D'Angelo & Antonio Canale & Zhaoxia Yu & Michele Guindani, 2023. "Bayesian nonparametric analysis for the detection of spikes in noisy calcium imaging data," Biometrics, The International Biometric Society, vol. 79(2), pages 1370-1382, June.
    13. Koun Onodera & Hiroyuki K. Kato, 2022. "Translaminar recurrence from layer 5 suppresses superficial cortical layers," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    14. Daigo Takeuchi & Dheeraj Roy & Shruti Muralidhar & Takashi Kawai & Andrea Bari & Chanel Lovett & Heather A. Sullivan & Ian R. Wickersham & Susumu Tonegawa, 2022. "Cingulate-motor circuits update rule representations for sequential choice decisions," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

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