Cerebellar re-encoding of self-generated head movements

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Abstract

Head movements are primarily sensed in a reference frame tied to the head, yet they are used to calculate self-orientation relative to the world. This requires to re-encode head kinematic signals into a reference frame anchored to earth-centered landmarks such as gravity, through computations whose neuronal substrate remains to be determined. Here, we studied the encoding of self-generated head movements in the rat caudal cerebellar vermis, an area essential for graviceptive functions. We found that, contrarily to peripheral vestibular inputs, most Purkinje cells exhibited a mixed sensitivity to head rotational and gravitational information and were differentially modulated by active and passive movements. In a subpopulation of cells, this mixed sensitivity underlay a tuning to rotations about an axis defined relative to gravity. Therefore, we show that the caudal vermis hosts a re-encoded, gravitationally-polarized representation of self-generated head kinematics in freely moving rats.

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Guillaume P Dugué

Neurophysiology of Brain Circuits Team, Institut de Biologie de l'École Normale Supérieure, Inserm U1024, CNRS UMR8197, Paris, France

Competing interests
The authors declare that no competing interests exist.
Matthieu Tihy

Neurophysiology of Brain Circuits Team, Institut de Biologie de l'École Normale Supérieure, Inserm U1024, CNRS UMR8197, Paris, France

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-9314-4657
Boris Gourévitch

Genetics and Physiology of Hearing Laboratory, Inserm UMR1120, University Paris 6, Institut Pasteur, Paris, France

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6742-8739
Clément Léna

Neurophysiology of Brain Circuits Team, Institut de Biologie de l'École Normale Supérieure, Inserm U1024, CNRS UMR8197, Paris, France

For correspondence
lena@biologie.ens.fr

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-1431-7717

Funding

Agence Nationale de la Recherche (ANR-12-BSV4-0027)

Clément Léna

Agence Nationale de la Recherche (ANR-15- CE37-0007)

Boris Gourévitch

Agence Nationale de la Recherche (ANR-10-LABX-54 MEMO LIFE)

Clément Léna

Agence Nationale de la Recherche (ANR-11-IDEX-0001-02 PSL Research University)

Clément Léna

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

Ethics

Animal experimentation: Experimental procedures were conducted in strict conformity with the institutional guidelines and in compliance with French national and European laws and policies. All procedures were approved by the "Charles Darwin" Ethics Committee (project number 1334).

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.