Principles of operation of a cerebellar learning circuit

Abstract
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Abstract

We provide behavioral evidence using monkey smooth pursuit eye movements for four principles of cerebellar learning. Using a circuit-level model of the cerebellum, we link behavioral data to learning's neural implementation. The four principles are: (1) early, fast, acquisition driven by climbing fiber inputs to the cerebellar cortex, with poor retention; (2) learned responses of Purkinje cells guide transfer of learning from the cerebellar cortex to the deep cerebellar nucleus, with excellent retention; (3) functionally different neural signals are subject to learning in the cerebellar cortex versus the deep cerebellar nuclei; and (4) negative feedback from the cerebellum to the inferior olive reduces the magnitude of the teaching signal in climbing fibers and limits learning. Our circuit-level model, based on these four principles, explains behavioral data obtained by strategically manipulating the signals responsible for acquisition and recall of direction learning in smooth pursuit eye movements across multiple timescales.

Data availability

The data for each figure is included in a Figure Composer FYP file and can be viewed, exported, and further analyzed using the freely available Figure Composer tool (https://sites.google.com/a/srscicomp.com/datanav/figure-composer). This tool is platform agnostic and runs on Windows, Mac, and Linux systems. The source code used to generate the cerebellar model results (Figure 10) is included as a Jupyter notebook. This source code makes use of Julia but can be viewed without installing Julia.

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Author details

David J Herzfeld

Department of Neurobiology, Duke University School of Medicine, Durham, United States

For correspondence
david.herzfeld@duke.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-9910-0658
Nathan J Hall

Department of Neurobiology, Duke University School of Medicine, Durham, United States

Competing interests
The authors declare that no competing interests exist.
Marios Tringides

Department of Neurobiology, Duke University School of Medicine, Durham, United States

Competing interests
The authors declare that no competing interests exist.
Stephen G Lisberger

Department of Neurobiology, Duke University School of Medicine, Durham, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7859-4361

Funding

National Institute of Neurological Disorders and Stroke (R01NS092623)

Stephen G Lisberger

National Institute of Neurological Disorders and Stroke (F32NS103216)

Nathan J Hall

National Eye Institute (K99-EY030528)

David J Herzfeld

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experimental procedures were performed in accordance with the Guide for the Care and Use of Laboratory Animals (1997) and had been approved in advance by the Institutional Animal Care and Use Committee at Duke University (Protocol A085-18-04).

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.