IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38418-4.html
   My bibliography  Save this article

Task-specific modulation of corticospinal neuron activity during motor learning in mice

Author

Listed:
  • Najet Serradj

    (Burke Neurological Institute)

  • Francesca Marino

    (University of California)

  • Yunuen Moreno-López

    (Burke Neurological Institute)

  • Amanda Bernstein

    (Burke Neurological Institute)

  • Sydney Agger

    (HAVAS Production Studios)

  • Marwa Soliman

    (Burke Neurological Institute)

  • Andrew Sloan

    (Vulintus, Inc.)

  • Edmund Hollis

    (Burke Neurological Institute
    Feil Family Brain and Mind Research Institute, Weill Cornell Medicine)

Abstract

Motor skill learning relies on the plasticity of the primary motor cortex as task acquisition drives cortical motor network remodeling. Large-scale cortical remodeling of evoked motor outputs occurs during the learning of corticospinal-dependent prehension behavior, but not simple, non-dexterous tasks. Here we determine the response of corticospinal neurons to two distinct motor training paradigms and assess the role of corticospinal neurons in the execution of a task requiring precise modulation of forelimb movement and one that does not. In vivo calcium imaging in mice revealed temporal coding of corticospinal activity coincident with the development of precise prehension movements, but not more simplistic movement patterns. Transection of the corticospinal tract and optogenetic regulation of corticospinal activity show the necessity for patterned corticospinal network activity in the execution of precise movements but not simplistic ones. Our findings reveal a critical role for corticospinal network modulation in the learning and execution of precise motor movements.

Suggested Citation

  • Najet Serradj & Francesca Marino & Yunuen Moreno-López & Amanda Bernstein & Sydney Agger & Marwa Soliman & Andrew Sloan & Edmund Hollis, 2023. "Task-specific modulation of corticospinal neuron activity during motor learning in mice," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38418-4
    DOI: 10.1038/s41467-023-38418-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38418-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38418-4?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. Maria Soledad Esposito & Paolo Capelli & Silvia Arber, 2014. "Brainstem nucleus MdV mediates skilled forelimb motor tasks," Nature, Nature, vol. 508(7496), pages 351-356, April.
    2. Andrew J. Peters & Simon X. Chen & Takaki Komiyama, 2014. "Emergence of reproducible spatiotemporal activity during motor learning," Nature, Nature, vol. 510(7504), pages 263-267, June.
    3. Min Fu & Xinzhu Yu & Ju Lu & Yi Zuo, 2012. "Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo," Nature, Nature, vol. 483(7387), pages 92-95, March.
    Full references (including those not matched with items on IDEAS)

    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. Sravani Kondapavulur & Stefan M. Lemke & David Darevsky & Ling Guo & Preeya Khanna & Karunesh Ganguly, 2022. "Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Zhiwei Xu & Erez Geron & Luis M. Pérez-Cuesta & Yang Bai & Wen-Biao Gan, 2023. "Generalized extinction of fear memory depends on co-allocation of synaptic plasticity in dendrites," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Hong Yu & Xinkuan Xiang & Zongming Chen & Xu Wang & Jiaqi Dai & Xinxin Wang & Pengcheng Huang & Zheng-dong Zhao & Wei L. Shen & Haohong Li, 2021. "Periaqueductal gray neurons encode the sequential motor program in hunting behavior of mice," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    4. Thomas E. Chater & Maximilian F. Eggl & Yukiko Goda & Tatjana Tchumatchenko, 2024. "Competitive processes shape multi-synapse plasticity along dendritic segments," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Jasleen Gundh & Awaneesh Singh & R K Brojen Singh, 2015. "Ordering Dynamics in Neuron Activity Pattern Model: An Insight to Brain Functionality," PLOS ONE, Public Library of Science, vol. 10(10), pages 1-16, October.
    6. Masakazu Agetsuma & Issei Sato & Yasuhiro R. Tanaka & Luis Carrillo-Reid & Atsushi Kasai & Atsushi Noritake & Yoshiyuki Arai & Miki Yoshitomo & Takashi Inagaki & Hiroshi Yukawa & Hitoshi Hashimoto & J, 2023. "Activity-dependent organization of prefrontal hub-networks for associative learning and signal transformation," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    7. Ravi Pancholi & Lauren Ryan & Simon Peron, 2023. "Learning in a sensory cortical microstimulation task is associated with elevated representational stability," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. Masashi Hasegawa & Ziyan Huang & Ricardo Paricio-Montesinos & Jan Gründemann, 2024. "Network state changes in sensory thalamus represent learned outcomes," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Ojasee Bapat & Tejas Purimetla & Sarah Kruessel & Monil Shah & Ruolin Fan & Christina Thum & Fiona Rupprecht & Julian D. Langer & Vidhya Rangaraju, 2024. "VAP spatially stabilizes dendritic mitochondria to locally support synaptic plasticity," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    10. Joanna C. Chang & Matthew G. Perich & Lee E. Miller & Juan A. Gallego & Claudia Clopath, 2024. "De novo motor learning creates structure in neural activity that shapes adaptation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. Weiwei Guo & Sijia Fan & Dan Xiao & Hui Dong & Guangwei Xu & Zhikun Wan & Yuqian Ma & Zhen Wang & Tian Xue & Yifeng Zhou & Yulong Li & Wei Xiong, 2021. "A Brainstem reticulotegmental neural ensemble drives acoustic startle reflexes," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    12. Harman Ghuman & Kyungsoo Kim & Sapeeda Barati & Karunesh Ganguly, 2023. "Emergence of task-related spatiotemporal population dynamics in transplanted neurons," Nature Communications, Nature, vol. 14(1), pages 1-15, 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:14:y:2023:i:1:d:10.1038_s41467-023-38418-4. 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.