Individual behavioral trajectories shape whole-brain connectivity in mice

Abstract

It is widely assumed that our actions shape our brains and that the resulting connections determine who we are. To test this idea in a reductionist setting, in which genes and environment are controlled, we investigated differences in neuroanatomy and structural covariance by ex vivo structural magnetic resonance imaging (MRI) in mice whose behavioral activity was continuously tracked for 3 months in a large, enriched environment. We confirmed that environmental enrichment increases mouse hippocampal volumes. Stratifying the enriched group according to individual longitudinal behavioral trajectories, however, revealed striking differences in mouse brain structural covariance in continuously highly active mice compared to those whose trajectories showed signs of habituating activity. Network-based statistics identified distinct sub-networks of murine structural covariance underlying these differences in behavioral activity. Together, these results reveal that differentiated behavioral trajectories of mice in an enriched environment are associated with differences in brain connectivity.

Data availability

The structural MR images used in this manuscript are publicly available on the OSF platform (https://osf.io/m7gpd/). The volumetric MRI data are found in Supplementary Files 1 (absolute values) and 2 (relative values). The behavioral data from the cage (animal IDs with time-stamped raw antenna contacts) are assessible at Dryad: https://doi.org/10.5061/dryad.bzkh189ds

The following data sets were generated

Article and author information

Author details

  1. Jadna Bogado Lopes

    German Center for Neurodegenerative Diseases, TU Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Anna N Senko

    German Center for Neurodegenerative Diseases, TU Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0885-0440
  3. Klaas Bahnsen

    Faculty of Medicine, TU Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5413-0359
  4. Daniel Geisler

    Faculty of Medicine, TU Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Eugene Kim

    Department of Neuroimaging, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0066-7051
  6. Michel Bernanos

    Department of Neuroimaging, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Diana Cash

    Department of Neuroimaging, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Stefan Ehrlich

    Faculty of Medicine, TU Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Anthony C Vernon

    Department of Basic and Clinical Neuroscience, King's College London, London, United Kingdom
    For correspondence
    anthony.vernon@kcl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7305-1069
  10. Gerd Kempermann

    German Center for Neurodegenerative Diseases, TU Dresden, Dresden, Germany
    For correspondence
    gerd.kempermann@dzne.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5304-4061

Funding

Helmholtz Association (Basic Funding)

  • Anna N Senko
  • Gerd Kempermann

Medizinische Fakultät Carl Gustav Carus, Technische Universität Dresden (Basic Funding)

  • Anna N Senko
  • Gerd Kempermann

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (88881.129646/2016-01)

  • Jadna Bogado Lopes

Joachim Herz Stiftung

  • Jadna Bogado Lopes

Medical Research Council (New Investigator Research Grant MR/N025377/1 (AV); Centre Grant MR/N026063/1)

  • Anthony C Vernon

TransCampus (TransCampus Research Award)

  • Anthony C Vernon
  • Gerd Kempermann

Deutsche Forschungsgemeinschaft (EH 367/7-1)

  • Stefan Ehrlich

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

Ethics

Animal experimentation: The experiment was conducted in accordance with the applicable European and national regulations and approved by the local authority (Landesdirektion Sachsen, file number 7/2016 TVT DD24 5131-365-8-SAC). All analyses were performed in a blinded manner.

Reviewing Editor

  1. Jason P Lerch, University of Oxford, United Kingdom

Publication history

  1. Received: May 18, 2022
  2. Accepted: January 13, 2023
  3. Accepted Manuscript published: January 16, 2023 (version 1)

Copyright

© 2023, Bogado Lopes 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. Jadna Bogado Lopes
  2. Anna N Senko
  3. Klaas Bahnsen
  4. Daniel Geisler
  5. Eugene Kim
  6. Michel Bernanos
  7. Diana Cash
  8. Stefan Ehrlich
  9. Anthony C Vernon
  10. Gerd Kempermann
(2023)
Individual behavioral trajectories shape whole-brain connectivity in mice
eLife 12:e80379.
https://doi.org/10.7554/eLife.80379

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