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Distinct Representations of Body and Head motion are Dynamically Encoded by Purkinje cell Populations in the Macaque Cerebellum

View ORCID ProfileOmid A. Zobeiri, View ORCID ProfileKathleen E. Cullen
doi: https://doi.org/10.1101/2021.10.25.465748
Omid A. Zobeiri
1Department of Biomedical Engineering, McGill University, Montréal, Canada
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Kathleen E. Cullen
2Department of Biomedical Engineering, Johns Hopkins University, Baltimore, USA
3Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, USA
4Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, USA
5Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, USA
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  • For correspondence: Kathleen.Cullen@jhu.edu
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Abstract

The ability to accurately control our posture and perceive spatial orientation during self-motion requires knowledge of the motion of both the head and body. However, whereas the vestibular sensors and nuclei directly encode head motion, no sensors directly encode body motion. Instead, the integration of vestibular and neck proprioceptive inputs is necessary to transform vestibular information into the body-centric reference frame required for postural control. The anterior vermis of the cerebellum is thought to play a key role in this transformation, yet how its Purkinje cells integrate these inputs or what information they dynamically encode during self-motion remains unknown. Here we recorded the activity of individual anterior vermis Purkinje cells in alert monkeys during passively applied whole-body, body-under-head, and head-on-body rotations. Most neurons dynamically encoded an intermediate representation of self-motion between head and body motion. Notably, these neurons responded to both vestibular and neck proprioceptive stimulation and showed considerable heterogeneity in their response dynamics. Furthermore, their vestibular responses demonstrated tuning in response to changes in head-on-body position. In contrast, a small remaining percentage of neurons sensitive only to vestibular stimulation unambiguously encoded head-in-space motion across conditions. Using a simple population model, we establish that combining responses from 40 Purkinje cells can explain the responses of their target neurons in deep cerebellar nuclei across all self-motion conditions. We propose that the observed heterogeneity in Purkinje cells underlies the cerebellum’s capacity to compute the dynamic representation of body motion required to ensure accurate postural control and perceptual stability in our daily lives.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted October 26, 2021.
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Distinct Representations of Body and Head motion are Dynamically Encoded by Purkinje cell Populations in the Macaque Cerebellum
Omid A. Zobeiri, Kathleen E. Cullen
bioRxiv 2021.10.25.465748; doi: https://doi.org/10.1101/2021.10.25.465748
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Distinct Representations of Body and Head motion are Dynamically Encoded by Purkinje cell Populations in the Macaque Cerebellum
Omid A. Zobeiri, Kathleen E. Cullen
bioRxiv 2021.10.25.465748; doi: https://doi.org/10.1101/2021.10.25.465748

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