Cerebellum encodes and influences the initiation, performance, and termination of discontinuous movements in mice

Abstract
Data availability
Article and author information
Metrics

Abstract

The cerebellum is hypothesized to represent timing information important for organizing salient motor events during periodically performed discontinuous movements. To provide functional evidence validating this idea, we measured and manipulated Purkinje cell (PC) activity in the lateral cerebellum of mice trained to volitionally perform periodic bouts of licking for regularly allocated water rewards. Overall, PC simple spiking modulated during task performance, mapping phasic tongue protrusions and retractions, as well as ramping prior to both lick-bout initiation and termination, two important motor events delimiting movement cycles. The ramping onset occurred earlier for the initiation of un-cued exploratory licking that anticipated water availability relative to licking that was reactive to water allocation, suggesting that the cerebellum is engaged differently depending on the movement context. In a subpopulation of PCs, climbing-fiber-evoked responses also increased during lick-bout initiation, but not termination, highlighting differences in how cerebellar input pathways represent task-related information. Optogenetic perturbation of PC activity disrupted the behavior by degrading lick-bout rhythmicity in addition to initiating and terminating licking bouts confirming a causative role in movement organization. Together, these results substantiate that the cerebellum contributes to the initiation and timing of repeated motor actions.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 4, 6 and 7.

Article and author information

Author details

Michael A Gaffield

Max Planck Florida Institute for Neuroscience, Jupiter, United States

Competing interests
The authors declare that no competing interests exist.
Britton A Sauerbrei

School of Medicine, Case Western Reserve University, Cleveland, United States

Competing interests
The authors declare that no competing interests exist.
Jason M Christie

Department of Physiology and Biophysics, University of Colorado School of Medicine, Aurora, United States

For correspondence
jason.m.christie@cuanschutz.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-0276-2554

Funding

National Institute of Neurological Disorders and Stroke (NS1188401)

Jason M Christie

National Institute of Neurological Disorders and Stroke (NS105958)

Jason M Christie

National Institute of Neurological Disorders and Stroke (NS112289)

Jason M Christie

Max Planck Florida Institute for Neuroscience (open access funding)

Michael A Gaffield
Jason M Christie

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 of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols of the Max Planck Florida Institute for Neuroscience (Protocol Number: 18-009) . As detailed in the Methods section, care was taken to minimize animal pain, suffering, and distress.

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.