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).

Reviewing Editor

  1. Timothy Verstynen, Carnegie Mellon University, United States

Publication history

  1. Received: June 25, 2018
  2. Accepted: March 16, 2019
  3. Accepted Manuscript published: March 18, 2019 (version 1)
  4. Version of Record published: April 12, 2019 (version 2)

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

  • 1,673
    Page views
  • 347
    Downloads
  • 25
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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

Further reading

    1. Computational and Systems Biology
    2. Neuroscience
    Jamie D Costabile, Kaarthik A Balakrishnan ... Martin Haesemeyer
    Research Article

    Brains are not engineered solutions to a well-defined problem but arose through selective pressure acting on random variation. It is therefore unclear how well a model chosen by an experimenter can relate neural activity to experimental conditions. Here we developed 'Model identification of neural encoding (MINE)'. MINE is an accessible framework using convolutional neural networks (CNN) to discover and characterize a model that relates aspects of tasks to neural activity. Although flexible, CNNs are difficult to interpret. We use Taylor decomposition approaches to understand the discovered model and how it maps task features to activity. We apply MINE to a published cortical dataset as well as experiments designed to probe thermoregulatory circuits in zebrafish. MINE allowed us to characterize neurons according to their receptive field and computational complexity, features which anatomically segregate in the brain. We also identified a new class of neurons that integrate thermosensory and behavioral information which eluded us previously when using traditional clustering and regression-based approaches.

    1. Developmental Biology
    2. Neuroscience
    Simone Rey, Henrike Ohm ... Christian Klämbt
    Research Article

    Neuronal information conductance often involves the transmission of action potentials. The spreading of action potentials along the axonal process of a neuron is based on three physical parameters: The axial resistance of the axon, the axonal insulation by glial membranes, and the positioning of voltage-gated ion channels. In vertebrates, myelin and channel clustering allow fast saltatory conductance. Here we show that in Drosophila melanogaster voltage-gated sodium and potassium channels, Para and Shal, co-localize and cluster in an area resembling the axon initial segment. The local enrichment of Para but not of Shal localization depends on the presence of peripheral wrapping glial cells. In larvae, relatively low levels of Para channels are needed to allow proper signal transduction and nerves are simply wrapped by glial cells. In adults, the concentration of Para increases and is prominently found at the axon initial segment of motor neurons. Concomitantly, these axon domains are covered by a mesh of glial processes forming a lacunar structure that possibly serves as an ion reservoir. Directly flanking this domain glial processes forming the lacunar area appear to collapse and closely apposed stacks of glial cell processes can be detected, resembling a myelin-like insulation. Thus, Drosophila development may reflect the evolution of myelin which forms in response to increased levels of clustered voltage-gated ion channels.