Convergence of cortical types and functional motifs in the human mesiotemporal lobe

  1. Casey Paquola  Is a corresponding author
  2. Oualid Benkarim
  3. Jordan DeKraker
  4. Sara Lariviere
  5. Stefan Frässle
  6. Jessica Royer
  7. Shahin Tavakol
  8. Sofie Valk
  9. Andrea Bernasconi
  10. Neda Bernasconi
  11. Ali Khan
  12. Alan C Evans
  13. Adeel Razi
  14. Jonathan Smallwood
  15. Boris Bernhardt  Is a corresponding author
  1. McGill University, Canada
  2. University of Western Ontario, Canada
  3. ETH Zurich, Switzerland
  4. Max Planck Institute Leipzig, Germany
  5. Monash University, Australia
  6. University of York, United Kingdom

Abstract

The mesiotemporal lobe (MTL) is implicated in many cognitive processes, is compromised in numerous brain disorders, and exhibits a gradual cytoarchitectural transition from six-layered parahippocampal isocortex to three-layered hippocampal allocortex. Leveraging an ultra-high-resolution histological reconstruction of a human brain, our study showed that the dominant axis of MTL cytoarchitectural differentiation follows the iso-to-allocortical transition and depth-specific variations in neuronal density. Projecting the histology-derived MTL model to in-vivo functional MRI, we furthermore determined how its cytoarchitecture underpins its intrinsic effective connectivity and association to large-scale networks. Here, the cytoarchitectural gradient was found to underpin intrinsic effective connectivity of the MTL, but patterns differed along the anterior-posterior axis. Moreover, while the iso-to-allocortical gradient parametrically represented the multiple-demand relative to task-negative networks, anterior-posterior gradients represented transmodal versus unimodal networks. Our findings establish that the combination of micro- and macrostructural features allow the MTL to represent dominant motifs of whole-brain functional organization.

Data availability

Code and data related to this specific project are openly available under https://github.com/MICA-MNI/micaopen/tree/master/cortical_confluence, BigBrain related information are openly available under https://bigbrain.loris.ca/main.php. The human connectome project dataset is available under https://db.humanconnectome.org/.

Article and author information

Author details

  1. Casey Paquola

    Neurology and Neurosurgery, McGill University, Montreal, Canada
    For correspondence
    casey.paquola@mcgill.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0190-4103
  2. Oualid Benkarim

    Neurology and Neurosurgery, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Jordan DeKraker

    Brain and Mind Institute, University of Western Ontario, London, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Sara Lariviere

    Neurology and Neurosurgery, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5701-1307
  5. Stefan Frässle

    Biomedical, ETH Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8011-2226
  6. Jessica Royer

    Neurology and Neurosurgery, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  7. Shahin Tavakol

    Neurology and Neurosurgery, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  8. Sofie Valk

    Cognitive Neurogenetics, Max Planck Institute Leipzig, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Andrea Bernasconi

    Neurology and Neurosurgery, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  10. Neda Bernasconi

    Neurology and Neurosurgery, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  11. Ali Khan

    Brain and Mind Institute, University of Western Ontario, London, Canada
    Competing interests
    The authors declare that no competing interests exist.
  12. Alan C Evans

    Montreal Neurological Institute and Hospital, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  13. Adeel Razi

    Monash University, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0779-9439
  14. Jonathan Smallwood

    Department of Psychology, University of York, York, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  15. Boris Bernhardt

    Neurology and Neurosurgery, McGill University, Montreal, Canada
    For correspondence
    boris.bernhardt@mcgill.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9536-7862

Funding

Canadian HIV Trials Network, Canadian Institutes of Health Research (CIHR FDN-154298)

  • Boris Bernhardt

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

Ethics

Human subjects: Participants gave informed consent and the study was approved by the local Research Ethics Board of the Montreal Neurological Institute and Hospital (2018-3469).

Reviewing Editor

  1. Morgan Barense, University of Toronto, Canada

Publication history

  1. Received: July 3, 2020
  2. Accepted: November 3, 2020
  3. Accepted Manuscript published: November 4, 2020 (version 1)
  4. Version of Record published: November 17, 2020 (version 2)

Copyright

© 2020, Paquola 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. Casey Paquola
  2. Oualid Benkarim
  3. Jordan DeKraker
  4. Sara Lariviere
  5. Stefan Frässle
  6. Jessica Royer
  7. Shahin Tavakol
  8. Sofie Valk
  9. Andrea Bernasconi
  10. Neda Bernasconi
  11. Ali Khan
  12. Alan C Evans
  13. Adeel Razi
  14. Jonathan Smallwood
  15. Boris Bernhardt
(2020)
Convergence of cortical types and functional motifs in the human mesiotemporal lobe
eLife 9:e60673.
https://doi.org/10.7554/eLife.60673