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Distinct representations of body and head motion are dynamically encoded by Purkinje cell populations in the macaque cerebellum

The ability to accurately control our posture and perceive our spatial orientation during self-motion requires knowledge of the motion of both the head and body. However, while the vestibular sensors and nuclei directly encode head motion, no sensors directly encode body motion. Instead, the integra...

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Detalles Bibliográficos
Autores principales: Zobeiri, Omid A, Cullen, Kathleen E
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9075952/
https://www.ncbi.nlm.nih.gov/pubmed/35467528
http://dx.doi.org/10.7554/eLife.75018
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author Zobeiri, Omid A
Cullen, Kathleen E
author_facet Zobeiri, Omid A
Cullen, Kathleen E
author_sort Zobeiri, Omid A
collection PubMed
description The ability to accurately control our posture and perceive our spatial orientation during self-motion requires knowledge of the motion of both the head and body. However, while 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 transform multiple streams of sensory information into an estimate of body 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 Purkinje cells dynamically encoded an intermediate representation of self-motion between head and body motion. Notably, Purkinje cells responded to both vestibular and neck proprioceptive stimulation with considerable heterogeneity in their response dynamics. Furthermore, their vestibular responses were tuned to head-on-body position. In contrast, targeted neurons in the deep cerebellar nuclei are known to unambiguously encode either head or body motion across conditions. Using a simple population model, we established that combining responses of~40-50 Purkinje cells could explain the responses of these deep cerebellar nuclei neurons across all self-motion conditions. We propose that the observed heterogeneity in Purkinje cell response dynamics 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.
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spelling pubmed-90759522022-05-07 Distinct representations of body and head motion are dynamically encoded by Purkinje cell populations in the macaque cerebellum Zobeiri, Omid A Cullen, Kathleen E eLife Neuroscience The ability to accurately control our posture and perceive our spatial orientation during self-motion requires knowledge of the motion of both the head and body. However, while 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 transform multiple streams of sensory information into an estimate of body 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 Purkinje cells dynamically encoded an intermediate representation of self-motion between head and body motion. Notably, Purkinje cells responded to both vestibular and neck proprioceptive stimulation with considerable heterogeneity in their response dynamics. Furthermore, their vestibular responses were tuned to head-on-body position. In contrast, targeted neurons in the deep cerebellar nuclei are known to unambiguously encode either head or body motion across conditions. Using a simple population model, we established that combining responses of~40-50 Purkinje cells could explain the responses of these deep cerebellar nuclei neurons across all self-motion conditions. We propose that the observed heterogeneity in Purkinje cell response dynamics 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. eLife Sciences Publications, Ltd 2022-04-25 /pmc/articles/PMC9075952/ /pubmed/35467528 http://dx.doi.org/10.7554/eLife.75018 Text en © 2022, Zobeiri and Cullen https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Zobeiri, Omid A
Cullen, Kathleen E
Distinct representations of body and head motion are dynamically encoded by Purkinje cell populations in the macaque cerebellum
title Distinct representations of body and head motion are dynamically encoded by Purkinje cell populations in the macaque cerebellum
title_full Distinct representations of body and head motion are dynamically encoded by Purkinje cell populations in the macaque cerebellum
title_fullStr Distinct representations of body and head motion are dynamically encoded by Purkinje cell populations in the macaque cerebellum
title_full_unstemmed Distinct representations of body and head motion are dynamically encoded by Purkinje cell populations in the macaque cerebellum
title_short Distinct representations of body and head motion are dynamically encoded by Purkinje cell populations in the macaque cerebellum
title_sort distinct representations of body and head motion are dynamically encoded by purkinje cell populations in the macaque cerebellum
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9075952/
https://www.ncbi.nlm.nih.gov/pubmed/35467528
http://dx.doi.org/10.7554/eLife.75018
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