Diversity and evolution of cerebellar folding in mammals

  1. Katja Heuer  Is a corresponding author
  2. Nicolas Traut
  3. Alexandra Allison de Sousa
  4. Sofie Louise Valk
  5. Julien Clavel
  6. Roberto Toro  Is a corresponding author
  1. Institut Pasteur, Falkland Islands (Malvinas)
  2. Institut Pasteur, France
  3. Bath Spa University, United Kingdom
  4. Max Planck Institute for Human Cognitive and Brain Sciences, Germany
  5. Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023, France

Abstract

The process of brain folding is thought to play an important role in the development and organisation of the cerebrum and the cerebellum. The study of cerebellar folding is challenging due to the small size and abundance of its folia. In consequence, little is known about its anatomical diversity and evolution. We constituted an open collection of histological data from 56 mammalian species and manually segmented the cerebrum and the cerebellum. We developed methods to measure the geometry of cerebellar folia and to estimate the thickness of the molecular layer. We used phylogenetic comparative methods to study the diversity and evolution of cerebellar folding and its relationship with the anatomy of the cerebrum. Our results show that the evolution of cerebellar and cerebral anatomy follows a stabilising selection process. We observed 2 groups of phenotypes changing concertedly through evolution: a group of 'diverse' phenotypes - varying over several orders of magnitude together with body size, and a group of 'stable' phenotypes varying over less than 1 order of magnitude across species. Our analyses confirmed the strong correlation between cerebral and cerebellar volumes across species, and showed in addition that large cerebella are disproportionately more folded than smaller ones. Compared with the extreme variations in cerebellar surface area, folial anatomy and molecular layer thickness varied only slightly, showing a much smaller increase in the larger cerebella. We discuss how these findings could provide new insights into the diversity and evolution of cerebellar folding, the mechanisms of cerebellar and cerebral folding, and their potential influence on the organisation of the brain across species.

Data availability

All data analysed during this study is openly available at https://microdraw.pasteur.fr/project/brainmuseum-cb. Code for reproducing our analyses and our figures is openly available at https://github.com/neuroanatomy/comp-cb-folding

The following data sets were generated

Article and author information

Author details

  1. Katja Heuer

    Institut Pasteur, France, Falkland Islands (Malvinas)
    For correspondence
    katjaqheuer@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7237-0196
  2. Nicolas Traut

    Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Alexandra Allison de Sousa

    Bath Spa University, Bath, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Sofie Louise Valk

    Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2998-6849
  5. Julien Clavel

    Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023, Villeurbanne, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Roberto Toro

    Institut Pasteur, Paris, France
    For correspondence
    rto@pasteur.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6671-858X

Funding

European Commission (101033485)

  • Katja Heuer

Agence Nationale de la Recherche (ANR-19-DATA-0025)

  • Katja Heuer
  • Nicolas Traut
  • Roberto Toro

Agence Nationale de la Recherche (ANR-21-CE45-0016)

  • Katja Heuer
  • Nicolas Traut
  • Roberto Toro

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

Ethics

Human subjects: The human dataset used has been made openly available through the BigBrain project.

Copyright

© 2023, Heuer et al.

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.

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  1. Katja Heuer
  2. Nicolas Traut
  3. Alexandra Allison de Sousa
  4. Sofie Louise Valk
  5. Julien Clavel
  6. Roberto Toro
(2023)
Diversity and evolution of cerebellar folding in mammals
eLife 12:e85907.
https://doi.org/10.7554/eLife.85907

Share this article

https://doi.org/10.7554/eLife.85907

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