Microstructural organization of human insula is linked to its macrofunctional circuitry and predicts cognitive control

  1. Vinod Menon  Is a corresponding author
  2. Guillermo Gallardo
  3. Mark A Pinsk
  4. Van-Dang Nguyen
  5. Jing-Rebecca Li
  6. Weidong Cai
  7. Demian Wassermann  Is a corresponding author
  1. Stanford University School of Medicine, United States
  2. Max Planck Institute for Human Cognitive and Brain Sciences, Germany
  3. Princeton University, United States
  4. Royal Institute of Technology in Stockholm, Sweden
  5. Inria Centre de Recherche Saclay Île-de-France, France

Abstract

The human insular cortex is a heterogeneous brain structure which plays an integrative role in guiding behavior. The cytoarchitectonic organization of the human insula has been investigated over the last century using postmortem brains but there has been little progress in noninvasive in vivo mapping of its microstructure and large-scale functional circuitry. Quantitative modeling of multi-shell diffusion MRI data from 413 participants revealed that human insula microstructure differs significantly across subdivisions that serve distinct cognitive and affective functions. Insular microstructural organization was mirrored in its functionally interconnected circuits with the anterior cingulate cortex that anchors the salience network, a system important for adaptive switching of cognitive control systems. Furthermore, insular microstructural features, confirmed in Macaca mulatta, were linked to behavior and predicted individual differences in cognitive control ability. Our findings open new possibilities for probing psychiatric and neurological disorders impacted by insular cortex dysfunction, including autism, schizophrenia, and fronto-temporal dementia.

Data availability

All data used in this study is available in open-source databases. The human data comes from the Human Connectome Project, the primate data is available at the INDI Primate Data Exchange, and the three-dimensional neuronal models are available from the NeuroMorpho website. All custom code is available on GitHub accesible through the Zenodo DOI: 10.5281/zenodo.3759708. All code was developed based on open-source, publicly available software packages.

The following data sets were generated

Article and author information

Author details

  1. Vinod Menon

    Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Palo Alto, United States
    For correspondence
    menon@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Guillermo Gallardo

    Department of Neuropsychology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Mark A Pinsk

    Scully Center for the Neuroscience of Mind & Behavior Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Van-Dang Nguyen

    Computer Science, Royal Institute of Technology in Stockholm, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  5. Jing-Rebecca Li

    Defi, Inria Centre de Recherche Saclay Île-de-France, Palaiseau, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Weidong Cai

    Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Palo Alto, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Demian Wassermann

    Parietal, Inria Centre de Recherche Saclay Île-de-France, Palaiseau, France
    For correspondence
    demian.wassermann@inria.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5194-6056

Funding

European Commission (NeuroLang -- 757672)

  • Demian Wassermann

National Institutes of Health (HD094623,HD059205,MH084164)

  • Vinod Menon

National Institutes of Health (MH105625)

  • Weidong Cai

Inria (LargeBrainNets)

  • Demian Wassermann

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

Ethics

Animal experimentation: Animal data was obtained from the INDI-Prime primate data exchange database collection (http://fcon_1000.projects.nitrc.org/indi/indiPRIME.html) . All methods and procedures were approved by the Princeton University IACUC

Human subjects: Data was obtained from the HCP database. Informed consent for this study was not explicitly required. However, subjects signed a written informed consent when the database was constituted. IRB approval was obtained for the database construction with the following details: Mapping the Human Connectome: Structure, Function, and HeritabilityIRB # 201204036

Reviewing Editor

  1. Timothy E Behrens, University of Oxford, United Kingdom

Publication history

  1. Received: November 9, 2019
  2. Accepted: June 3, 2020
  3. Accepted Manuscript published: June 4, 2020 (version 1)
  4. Version of Record published: June 22, 2020 (version 2)

Copyright

© 2020, Menon 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. Vinod Menon
  2. Guillermo Gallardo
  3. Mark A Pinsk
  4. Van-Dang Nguyen
  5. Jing-Rebecca Li
  6. Weidong Cai
  7. Demian Wassermann
(2020)
Microstructural organization of human insula is linked to its macrofunctional circuitry and predicts cognitive control
eLife 9:e53470.
https://doi.org/10.7554/eLife.53470

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