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Cerebro-cerebellar networks facilitate learning through feedback decoupling

Author

Listed:
  • Ellen Boven

    (University of Bristol
    University of Bristol)

  • Joseph Pemberton

    (University of Bristol)

  • Paul Chadderton

    (University of Bristol)

  • Richard Apps

    (University of Bristol)

  • Rui Ponte Costa

    (University of Bristol)

Abstract

Behavioural feedback is critical for learning in the cerebral cortex. However, such feedback is often not readily available. How the cerebral cortex learns efficiently despite the sparse nature of feedback remains unclear. Inspired by recent deep learning algorithms, we introduce a systems-level computational model of cerebro-cerebellar interactions. In this model a cerebral recurrent network receives feedback predictions from a cerebellar network, thereby decoupling learning in cerebral networks from future feedback. When trained in a simple sensorimotor task the model shows faster learning and reduced dysmetria-like behaviours, in line with the widely observed functional impact of the cerebellum. Next, we demonstrate that these results generalise to more complex motor and cognitive tasks. Finally, the model makes several experimentally testable predictions regarding cerebro-cerebellar task-specific representations over learning, task-specific benefits of cerebellar predictions and the differential impact of cerebellar and inferior olive lesions. Overall, our work offers a theoretical framework of cerebro-cerebellar networks as feedback decoupling machines.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-022-35658-8
    DOI: 10.1038/s41467-022-35658-8
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    References listed on IDEAS

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    1. Valerio Mante & David Sussillo & Krishna V. Shenoy & William T. Newsome, 2013. "Context-dependent computation by recurrent dynamics in prefrontal cortex," Nature, Nature, vol. 503(7474), pages 78-84, November.
    2. Martha L. Streng & Laurentiu S. Popa & Timothy J. Ebner, 2018. "Modulation of sensory prediction error in Purkinje cells during visual feedback manipulations," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    3. Mark J. Wagner & Tony Hyun Kim & Joan Savall & Mark J. Schnitzer & Liqun Luo, 2017. "Cerebellar granule cells encode the expectation of reward," Nature, Nature, vol. 544(7648), pages 96-100, April.
    4. 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.
    5. Volodymyr Mnih & Koray Kavukcuoglu & David Silver & Andrei A. Rusu & Joel Veness & Marc G. Bellemare & Alex Graves & Martin Riedmiller & Andreas K. Fidjeland & Georg Ostrovski & Stig Petersen & Charle, 2015. "Human-level control through deep reinforcement learning," Nature, Nature, vol. 518(7540), pages 529-533, February.
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