Consolidation alters motor sequence-specific distributed representations

  1. Basile Pinsard  Is a corresponding author
  2. Arnaud Boutin
  3. Ella Gabitov
  4. Ovidiu Lungu
  5. Habib Benali
  6. Julien Doyon  Is a corresponding author
  1. Centre de Recherche de l'Institut Universitaire de Gériatrie de Montréal, Canada
  2. Concordia University, Canada
  3. McGill University, Canada

Abstract

FMRI studies investigating the acquisition of sequential motor skills in humans have revealed learning-related functional reorganizations of the cortico-striatal and cortico-cerebellar motor systems accompanied with an initial hippocampal contribution. Yet, the functional significance of these activity level changes remains ambiguous as they convey the evolution of both sequence-specific knowledge and unspecific task ability. Moreover, these changes do not specifically assess the occurrence of learning-related plasticity. To address these issues, we investigated local circuits tuning to sequence-specific information using multivariate distances between patterns evoked by consolidated or newly acquired motor sequences production. The results reveal that representations in dorsolateral striatum, prefrontal and secondary motor cortices are greater when executing consolidated sequences than untrained ones. By contrast, sequence representations in the hippocampus and dorsomedial striatum becomes less engaged. Our findings show, for the first time in humans, that complementary sequence-specific motor representations evolve distinctively during critical phases of skill acquisition and consolidation.

Data availability

Behavioral data analyzed and presented in the article as well as statistical maps of brain representational measure have been deposited on the Open Science Framework with the DOI 10.17605/OSF.IO/EPJ2V

The following data sets were generated

Article and author information

Author details

  1. Basile Pinsard

    Functional Neuroimaging Unit, Centre de Recherche de l'Institut Universitaire de Gériatrie de Montréal, Montréal, Canada
    For correspondence
    basile.pinsard@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4391-3075
  2. Arnaud Boutin

    Functional Neuroimaging Unit, Centre de Recherche de l'Institut Universitaire de Gériatrie de Montréal, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5696-2626
  3. Ella Gabitov

    Functional Neuroimaging Unit, Centre de Recherche de l'Institut Universitaire de Gériatrie de Montréal, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Ovidiu Lungu

    Functional Neuroimaging Unit, Centre de Recherche de l'Institut Universitaire de Gériatrie de Montréal, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Habib Benali

    Perform Center, Concordia University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Julien Doyon

    Montreal Neurological Institute - McConnell Brain Imaging Center, McGill University, Montréal, Canada
    For correspondence
    julien.doyon@mcgill.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3788-4271

Funding

Canadian Institutes of Health Research (MOP 97830)

  • Basile Pinsard
  • Arnaud Boutin
  • Ella Gabitov
  • Julien Doyon

Ministère de l'Education Nationale, de l'Enseignement Superieur et de la Recherche (PhD scholarship)

  • Basile Pinsard

Sorbonne Université (PhD study abroad grant)

  • Basile Pinsard

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

Ethics

Human subjects: All participants provided written informed consent and received financial compensationfor their participation. This study protocol was approved by the Research Ethics Board of the ""Comité mixte d'éthique de la recherche - Regroupement en Neuroimagerie duQuébec"" (CMER-RNQ 13-14-011).

Copyright

© 2019, Pinsard 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.

Metrics

  • 2,007
    views
  • 411
    downloads
  • 906
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Basile Pinsard
  2. Arnaud Boutin
  3. Ella Gabitov
  4. Ovidiu Lungu
  5. Habib Benali
  6. Julien Doyon
(2019)
Consolidation alters motor sequence-specific distributed representations
eLife 8:e39324.
https://doi.org/10.7554/eLife.39324

Share this article

https://doi.org/10.7554/eLife.39324

Further reading

    1. Neuroscience
    Agnieszka Glica, Katarzyna Wasilewska ... Katarzyna Jednoróg
    Research Article

    The neural noise hypothesis of dyslexia posits an imbalance between excitatory and inhibitory (E/I) brain activity as an underlying mechanism of reading difficulties. This study provides the first direct test of this hypothesis using both electroencephalography (EEG) power spectrum measures in 120 Polish adolescents and young adults (60 with dyslexia, 60 controls) and glutamate (Glu) and gamma-aminobutyric acid (GABA) concentrations from magnetic resonance spectroscopy (MRS) at 7T MRI scanner in half of the sample. Our results, supported by Bayesian statistics, show no evidence of E/I balance differences between groups, challenging the hypothesis that cortical hyperexcitability underlies dyslexia. These findings suggest that alternative mechanisms must be explored and highlight the need for further research into the E/I balance and its role in neurodevelopmental disorders.

    1. Biochemistry and Chemical Biology
    2. Neuroscience
    Silvia Galli, Marco Di Antonio
    Insight

    The buildup of knot-like RNA structures in brain cells may be the key to understanding how uncontrolled protein aggregation drives Alzheimer’s disease.