Cerebral chemoarchitecture shares organizational traits with brain structure and function

  1. Benjamin Hänisch
  2. Justine Y Hansen
  3. Boris C Bernhardt
  4. Simon B Eickhoff
  5. Juergen Dukart
  6. Bratislav Misic
  7. Sofie Louise Valk  Is a corresponding author
  1. Forschungszentrum Jülich, Germany
  2. McGill University, Canada
  3. Max Planck Institute for Human Cognitive and Brain Sciences, Germany

Abstract

Chemoarchitecture, the heterogeneous distribution of neurotransmitter transporter and receptor molecules, is a relevant component of structure-function relationships in the human brain. Here, we studied the organization of the receptome, a measure of interareal chemoarchitectural similarity, derived from Positron-Emission Tomography imaging studies of 19 different neurotransmitter transporters and receptors. Nonlinear dimensionality reduction revealed three main spatial gradients of cortical chemoarchitectural similarity - a centro-temporal gradient, an occipito-frontal gradient, and a temporo-occipital gradient. In subcortical nuclei, chemoarchitectural similarity distinguished functional communities and delineated a striato-thalamic axis. Overall, the cortical receptome shared key organizational traits with functional and structural brain anatomy, with node-level correspondence to functional, microstructural, and diffusion MRI-based measures decreasing along a primary-to-transmodal axis. Relative to primary and paralimbic regions, unimodal and heteromodal regions showed higher receptomic diversification, possibly supporting functional flexibility.

Data availability

All data and software used in this study is openly accessible. PET data is available at https://github.com/netneurolab/hansen_receptors. FC, SC and MPC data is available at https://portal.conp.ca/dataset?id=projects/mica-mics. ENIGMA data is available through enigmatoolbox (https://github.com/MICA-MNI/ENIGMA). Meta-analytical functional activation data is available through Neurosynth (https://neurosynth.org/analyses/topics/v5-topics-50). The code used to perform the analyses can be found at https://github.com/CNG-LAB/cngopen/receptor_similarity.

The following previously published data sets were used

Article and author information

Author details

  1. Benjamin Hänisch

    Institute of Neuroscience and Medicine, Brain and Behaviour, Forschungszentrum Jülich, Jülich, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5463-4218
  2. Justine Y Hansen

    Montréal Neurological Institute, 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:" 0000-0003-3142-7480
  3. Boris C Bernhardt

    Montreal Neurological Institute, 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:" 0000-0001-9256-6041
  4. Simon B Eickhoff

    Institute of Neuroscience and Medicine, Brain and Behaviour, Forschungszentrum Jülich, Jülich, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6363-2759
  5. Juergen Dukart

    Institute of Neuroscience and Medicine, Brain and Behaviour, Forschungszentrum Jülich, Jülich, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0492-5644
  6. Bratislav Misic

    Montréal Neurological Institute, 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:" 0000-0003-0307-2862
  7. Sofie Louise Valk

    Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    For correspondence
    s.valk@fz-juelich.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2998-6849

Funding

Max-Planck-Institut für Kognitions- und Neurowissenschaften (Open Access funding)

  • Sofie Louise Valk

FRQ-S

  • Boris C Bernhardt

Tier-2 Canada Research Chairs program

  • Boris C Bernhardt

Human Brain Project

  • Simon B Eickhoff

Max Planck Gesellschaft (Otto Hahn award)

  • Sofie Louise Valk

Helmholtz International Lab grant agreement (InterLabs-0015)

  • Boris C Bernhardt
  • Simon B Eickhoff
  • Sofie Louise Valk

Canada First Research Excellence Fund (CFREF Competition 2,2015-2016)

  • Boris C Bernhardt
  • Simon B Eickhoff
  • Sofie Louise Valk

European Union's Horizon 2020 (No. 826421 TheVirtualBrain-Cloud"")

  • Juergen Dukart

Helmholtz International BigBrain Analytics & Laboratory

  • Justine Y Hansen
  • Boris C Bernhardt
  • Simon B Eickhoff
  • Sofie Louise Valk

Natural Sciences and Engineering Research Council of Canada

  • Justine Y Hansen
  • Boris C Bernhardt
  • Bratislav Misic

Canadian Institutes of Health Research

  • Boris C Bernhardt
  • Bratislav Misic

Brain Canada Foundation Future Leaders Fund

  • Boris C Bernhardt
  • Bratislav Misic

Canada Research Chairs

  • Bratislav Misic

Michael J. Fox Foundation for Parkinson's Research

  • Bratislav Misic

SickKids Foundation (NI17-039)

  • Boris C Bernhardt

Azrieli Center for Autism Research (ACAR-TACC)

  • Boris C Bernhardt

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

Reviewing Editor

  1. Birte U Forstmann, University of Amsterdam, Netherlands

Ethics

Human subjects: The current research complies with all relevant ethical regulations as set by The Independent Research Ethics Committee at the Medical Faculty of the Heinrich-Heine-University of Duesseldorf (study number 2018-317). The current data was based on open access resources, and ethic approvals of the individual datasets are available in the original publications of each data source.

Version history

  1. Preprint posted: August 26, 2022 (view preprint)
  2. Received: September 30, 2022
  3. Accepted: July 12, 2023
  4. Accepted Manuscript published: July 13, 2023 (version 1)
  5. Version of Record published: July 26, 2023 (version 2)

Copyright

© 2023, Hänisch 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. Benjamin Hänisch
  2. Justine Y Hansen
  3. Boris C Bernhardt
  4. Simon B Eickhoff
  5. Juergen Dukart
  6. Bratislav Misic
  7. Sofie Louise Valk
(2023)
Cerebral chemoarchitecture shares organizational traits with brain structure and function
eLife 12:e83843.
https://doi.org/10.7554/eLife.83843

Share this article

https://doi.org/10.7554/eLife.83843

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