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Structured cerebellar connectivity supports resilient pattern separation

Author

Listed:
  • Tri M. Nguyen

    (Department of Neurobiology, Harvard Medical School)

  • Logan A. Thomas

    (Department of Neurobiology, Harvard Medical School
    University of California Berkeley)

  • Jeff L. Rhoades

    (Department of Neurobiology, Harvard Medical School
    Harvard University)

  • Ilaria Ricchi

    (Department of Neurobiology, Harvard Medical School
    École Polytechnique Fédérale de Lausanne (EPFL))

  • Xintong Cindy Yuan

    (Department of Neurobiology, Harvard Medical School
    Harvard University)

  • Arlo Sheridan

    (HHMI Janelia Research Campus
    Salk Institute for Biological Studies)

  • David G. C. Hildebrand

    (Department of Neurobiology, Harvard Medical School
    The Rockefeller University)

  • Jan Funke

    (HHMI Janelia Research Campus)

  • Wade G. Regehr

    (Department of Neurobiology, Harvard Medical School)

  • Wei-Chung Allen Lee

    (Boston Children’s Hospital, Harvard Medical School)

Abstract

The cerebellum is thought to help detect and correct errors between intended and executed commands1,2 and is critical for social behaviours, cognition and emotion3–6. Computations for motor control must be performed quickly to correct errors in real time and should be sensitive to small differences between patterns for fine error correction while being resilient to noise7. Influential theories of cerebellar information processing have largely assumed random network connectivity, which increases the encoding capacity of the network’s first layer8–13. However, maximizing encoding capacity reduces the resilience to noise7. To understand how neuronal circuits address this fundamental trade-off, we mapped the feedforward connectivity in the mouse cerebellar cortex using automated large-scale transmission electron microscopy and convolutional neural network-based image segmentation. We found that both the input and output layers of the circuit exhibit redundant and selective connectivity motifs, which contrast with prevailing models. Numerical simulations suggest that these redundant, non-random connectivity motifs increase the resilience to noise at a negligible cost to the overall encoding capacity. This work reveals how neuronal network structure can support a trade-off between encoding capacity and redundancy, unveiling principles of biological network architecture with implications for the design of artificial neural networks.

Suggested Citation

  • Tri M. Nguyen & Logan A. Thomas & Jeff L. Rhoades & Ilaria Ricchi & Xintong Cindy Yuan & Arlo Sheridan & David G. C. Hildebrand & Jan Funke & Wade G. Regehr & Wei-Chung Allen Lee, 2023. "Structured cerebellar connectivity supports resilient pattern separation," Nature, Nature, vol. 613(7944), pages 543-549, January.
  • Handle: RePEc:nat:nature:v:613:y:2023:i:7944:d:10.1038_s41586-022-05471-w
    DOI: 10.1038/s41586-022-05471-w
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    Cited by:

    1. Ting-Feng Lin & Silas E. Busch & Christian Hansel, 2024. "Intrinsic and synaptic determinants of receptive field plasticity in Purkinje cells of the mouse cerebellum," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

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