IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-64592-8.html
   My bibliography  Save this article

Stage-dependent cerebrocerebellar communication during sensorimotor processing

Author

Listed:
  • Vincenzo Romano

    (Erasmus MC)

  • Matthijs Driessche

    (Erasmus MC)

  • Nathalie Wingerden

    (Erasmus MC)

  • Staf Bauer

    (Erasmus MC)

  • Brendan Boeser

    (Erasmus MC)

  • Jorge F. Mejias

    (University of Amsterdam)

  • Chris I. Zeeuw

    (Erasmus MC
    Royal Dutch Academy of Arts & Sciences)

Abstract

Cerebral cortex and cerebellum are essential for sensorimotor control, but the dynamics of their interactions remain unclear. Here, we investigated which pathways prevail during preparation and execution of spontaneous whisker movements in mice. During preparation, neuronal activity of primary motor (M1) and somatosensory (S1) cortex precede that of cerebellar crus regions, with a lead that is consistent with relaying a copy of motor commands. After movement onset, the phase of the signal inverts, indicating a dominant vector signaling from cerebellum to cerebrum. At this stage, Purkinje cell activity correlates more with S1 than M1, generating a prediction of sensory consequences during motor actions. A computational cerebello-cortical model could replicate the changes in dynamics and directionality. Optogenetic manipulations of pons and thalamus confirm the modeled predictions on stage-dependent dynamics. Together our data point towards a swap in direction of information flow between cerebrum and cerebellum when motor preparation switches to execution.

Suggested Citation

  • Vincenzo Romano & Matthijs Driessche & Nathalie Wingerden & Staf Bauer & Brendan Boeser & Jorge F. Mejias & Chris I. Zeeuw, 2025. "Stage-dependent cerebrocerebellar communication during sensorimotor processing," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-64592-8
    DOI: 10.1038/s41467-025-64592-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-64592-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-025-64592-8?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. Joseph Pemberton & Paul Chadderton & Rui Ponte Costa, 2024. "Cerebellar-driven cortical dynamics can enable task acquisition, switching and consolidation," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. 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.
    3. Jun Takatoh & Vincent Prevosto & P. M. Thompson & Jinghao Lu & Leeyup Chung & Andrew Harrahill & Shun Li & Shengli Zhao & Zhigang He & David Golomb & David Kleinfeld & Fan Wang, 2022. "The whisking oscillator circuit," Nature, Nature, vol. 609(7927), pages 560-568, September.
    4. Leopoldo Petreanu & Tianyi Mao & Scott M. Sternson & Karel Svoboda, 2009. "The subcellular organization of neocortical excitatory connections," Nature, Nature, vol. 457(7233), pages 1142-1145, February.
    5. 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.
    6. Yan Yang & Stephen G. Lisberger, 2014. "Purkinje-cell plasticity and cerebellar motor learning are graded by complex-spike duration," Nature, Nature, vol. 510(7506), pages 529-532, June.
    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. Joseph Pemberton & Paul Chadderton & Rui Ponte Costa, 2024. "Cerebellar-driven cortical dynamics can enable task acquisition, switching and consolidation," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Simon Weiler & Vahid Rahmati & Marcel Isstas & Johann Wutke & Andreas Walter Stark & Christian Franke & Jürgen Graf & Christian Geis & Otto W. Witte & Mark Hübener & Jürgen Bolz & Troy W. Margrie & Kn, 2024. "A primary sensory cortical interareal feedforward inhibitory circuit for tacto-visual integration," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    3. Hironobu Osaki & Moeko Kanaya & Yoshifumi Ueta & Mariko Miyata, 2022. "Distinct nociception processing in the dysgranular and barrel regions of the mouse somatosensory cortex," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Federico Brandalise & Ronan Chéreau & I-Wen Chen & David Oorschot & Claudia Raig & Tanika Bawa & Nandkishor Mule & Stéphane Pagès & Foivos Markopoulos & Anthony Holtmaat, 2025. "Thalamocortical feedback selectively controls pyramidal neuron excitability," Nature Communications, Nature, vol. 16(1), pages 1-20, December.
    5. Sergio Luengo-Sanchez & Isabel Fernaud-Espinosa & Concha Bielza & Ruth Benavides-Piccione & Pedro Larrañaga & Javier DeFelipe, 2018. "3D morphology-based clustering and simulation of human pyramidal cell dendritic spines," PLOS Computational Biology, Public Library of Science, vol. 14(6), pages 1-22, June.
    6. Arco Bast & Jason M. Guest & Rieke Fruengel & Rajeevan T. Narayanan & Christiaan P. J. Kock & Marcel Oberlaender, 2025. "Thalamus enables active dendritic coupling of inputs arriving at different cortical layers," Nature Communications, Nature, vol. 16(1), pages 1-19, December.
    7. Ravi D. Mill & Michael W. Cole, 2025. "Dynamically shifting from compositional to conjunctive brain representations supports cognitive task learning," Nature Communications, Nature, vol. 16(1), pages 1-24, December.
    8. Songren Wei & Meng Luo & Pingping Wang & Rui Chen & Xiyun Jin & Chang Xu & Chenyang Li & Xiaoyu Lin & Zhaochun Xu & Hongxin Liu & Rui Cheng & Wenyi Yang & Yideng Cai & Guangfu Xue & Peng Huang & Zhiga, 2025. "Charting the spatial transcriptome of the human cerebral cortex at single-cell resolution," Nature Communications, Nature, vol. 16(1), pages 1-20, December.
    9. Shan Shen & Xiaolong Jiang & Federico Scala & Jiakun Fu & Paul Fahey & Dmitry Kobak & Zhenghuan Tan & Na Zhou & Jacob Reimer & Fabian Sinz & Andreas S. Tolias, 2022. "Distinct organization of two cortico-cortical feedback pathways," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    10. Yun Gao & Dan Wu & Jie Song & Xueyi Zhang & Bangbang Hou & Hengfa Liu & Junqi Liao & Liang Zhou, 2025. "A wearable obstacle avoidance device for visually impaired individuals with cross-modal learning," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    11. 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.
    12. Solomiia Korchynska & Patrick Rebernik & Marko Pende & Laura Boi & Alán Alpár & Ramon Tasan & Klaus Becker & Kira Balueva & Saiedeh Saghafi & Peer Wulff & Tamas L. Horvath & Gilberto Fisone & Hans-Ulr, 2022. "A hypothalamic dopamine locus for psychostimulant-induced hyperlocomotion in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    13. 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.
    14. 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.
    15. Suma Chinta & Scott R. Pluta, 2023. "Neural mechanisms for the localization of unexpected external motion," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    16. 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.
    17. Dabal Pedamonti & Samia Mohinta & Martin V. Dimitrov & Hugo Malagon-Vina & Stephane Ciocchi & Rui Ponte Costa, 2025. "Hippocampus supports multi-task reinforcement learning under partial observability," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    18. Gabriele Marcassa & Dan Dascenco & Blanca Lorente-Echeverría & Danie Daaboul & Jeroen Vandensteen & Elke Leysen & Lucas Baltussen & Andrew J. M. Howden & Joris Wit, 2025. "Synaptic signatures and disease vulnerabilities of layer 5 pyramidal neurons," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    19. 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.
    20. Yoav Printz & Pritish Patil & Mathias Mahn & Asaf Benjamin & Anna Litvin & Rivka Levy & Max Bringmann & Ofer Yizhar, 2023. "Determinants of functional synaptic connectivity among amygdala-projecting prefrontal cortical neurons in male mice," Nature Communications, Nature, vol. 14(1), pages 1-18, 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:16:y:2025:i:1:d:10.1038_s41467-025-64592-8. 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.