3
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      A multi-scale cortical wiring space links cellular architecture and functional dynamics in the human brain

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          The vast net of fibres within and underneath the cortex is optimised to support the convergence of different levels of brain organisation. Here, we propose a novel coordinate system of the human cortex based on an advanced model of its connectivity. Our approach is inspired by seminal, but so far largely neglected models of cortico–cortical wiring established by postmortem anatomical studies and capitalises on cutting-edge in vivo neuroimaging and machine learning. The new model expands the currently prevailing diffusion magnetic resonance imaging (MRI) tractography approach by incorporation of additional features of cortical microstructure and cortico–cortical proximity. Studying several datasets and different parcellation schemes, we could show that our coordinate system robustly recapitulates established sensory-limbic and anterior–posterior dimensions of brain organisation. A series of validation experiments showed that the new wiring space reflects cortical microcircuit features (including pyramidal neuron depth and glial expression) and allowed for competitive simulations of functional connectivity and dynamics based on resting-state functional magnetic resonance imaging (rs-fMRI) and human intracranial electroencephalography (EEG) coherence. Our results advance our understanding of how cell-specific neurobiological gradients produce a hierarchical cortical wiring scheme that is concordant with increasing functional sophistication of human brain organisation. Our evaluations demonstrate the cortical wiring space bridges across scales of neural organisation and can be easily translated to single individuals.

          Abstract

          This study proposes a novel coordinate system of the human cortex based on an expanded model of structural connectivity, and demonstrates that this system can visualize salient dimensions of brain organization, and reflects specific cytoarchitectural and cellular features. Functional neuroimaging and intracranial recordings show that the coordinate system can be used to make robust predictions of functional connectivity and brain dynamics.

          Related collections

          Most cited references130

          • Record: found
          • Abstract: not found
          • Article: not found

          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

            Bookmark
            • Record: found
            • Abstract: not found
            • Article: not found

            Regression Shrinkage and Selection Via the Lasso

              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest.

              In this study, we have assessed the validity and reliability of an automated labeling system that we have developed for subdividing the human cerebral cortex on magnetic resonance images into gyral based regions of interest (ROIs). Using a dataset of 40 MRI scans we manually identified 34 cortical ROIs in each of the individual hemispheres. This information was then encoded in the form of an atlas that was utilized to automatically label ROIs. To examine the validity, as well as the intra- and inter-rater reliability of the automated system, we used both intraclass correlation coefficients (ICC), and a new method known as mean distance maps, to assess the degree of mismatch between the manual and the automated sets of ROIs. When compared with the manual ROIs, the automated ROIs were highly accurate, with an average ICC of 0.835 across all of the ROIs, and a mean distance error of less than 1 mm. Intra- and inter-rater comparisons yielded little to no difference between the sets of ROIs. These findings suggest that the automated method we have developed for subdividing the human cerebral cortex into standard gyral-based neuroanatomical regions is both anatomically valid and reliable. This method may be useful for both morphometric and functional studies of the cerebral cortex as well as for clinical investigations aimed at tracking the evolution of disease-induced changes over time, including clinical trials in which MRI-based measures are used to examine response to treatment.
                Bookmark

                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Writing – review & editing
                Role: Formal analysisRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Writing – review & editing
                Role: ConceptualizationRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Writing – review & editing
                Role: Data curationRole: Resources
                Role: Investigation
                Role: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                30 November 2020
                November 2020
                30 November 2020
                : 18
                : 11
                : e3000979
                Affiliations
                [1 ] Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada
                [2 ] Developmental Neurogenomics Unit, National Institute of Mental Health, Bethesda, Maryland, United States of America
                [3 ] Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada
                [4 ] Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom
                [5 ] York Neuroimaging Center, University of York, York, United Kingdom
                Oxford University, UNITED KINGDOM
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0002-8164-7476
                https://orcid.org/0000-0002-4448-8998
                https://orcid.org/0000-0002-0714-0685
                https://orcid.org/0000-0001-5701-1307
                https://orcid.org/0000-0003-0574-6576
                https://orcid.org/0000-0002-2917-1212
                https://orcid.org/0000-0001-9256-6041
                Article
                PBIOLOGY-D-20-00780
                10.1371/journal.pbio.3000979
                7728398
                33253185
                cd772188-50c4-4359-b915-c041a9e86ce1
                © 2020 Paquola et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 26 March 2020
                : 2 November 2020
                Page count
                Figures: 6, Tables: 0, Pages: 31
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100000034, Institute of Neurosciences, Mental Health and Addiction;
                Award ID: CIHR FDN-154298
                Award Recipient :
                CP and RC were funded through a postdoctoral fellowship of the Fonds de la Recherche due Quebec – Santé (FRQ-S). OB was funded by a Healthy Brains for Healthy Lives (HBHL) postdoctoral fellowship. JR was supported by a Canadian Open Neuroscience Platform (CONP) fellowship. JS was supported by the European Research Council (WANDERINGMINDS-ERC646927). BB acknowledges research support from the National Science and Engineering Research Council of Canada (NSERC Discovery-1304413), the Canadian Institutes of Health Research (CIHR FDN-154298), SickKids Foundation (NI17-039), BrainCanada, Azrieli Center for Autism Research (ACAR-TACC), Helmholtz International BigBrain Analytics Learning Laboratory (HIBALL), FRQ-S, and the Tier-2 Canada Research Chairs program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Physical Sciences
                Mathematics
                Algebra
                Linear Algebra
                Eigenvectors
                Physical Sciences
                Materials Science
                Materials Physics
                Microstructure
                Physical Sciences
                Physics
                Materials Physics
                Microstructure
                Biology and Life Sciences
                Genetics
                Gene Expression
                Computer and Information Sciences
                Software Engineering
                Preprocessing
                Engineering and Technology
                Software Engineering
                Preprocessing
                Biology and Life Sciences
                Neuroscience
                Brain Mapping
                Brain Morphometry
                Diffusion Tensor Imaging
                Tractography
                Medicine and Health Sciences
                Diagnostic Medicine
                Diagnostic Radiology
                Magnetic Resonance Imaging
                Brain Morphometry
                Diffusion Tensor Imaging
                Tractography
                Research and Analysis Methods
                Imaging Techniques
                Diagnostic Radiology
                Magnetic Resonance Imaging
                Brain Morphometry
                Diffusion Tensor Imaging
                Tractography
                Medicine and Health Sciences
                Radiology and Imaging
                Diagnostic Radiology
                Magnetic Resonance Imaging
                Brain Morphometry
                Diffusion Tensor Imaging
                Tractography
                Research and Analysis Methods
                Imaging Techniques
                Neuroimaging
                Brain Morphometry
                Diffusion Tensor Imaging
                Tractography
                Biology and Life Sciences
                Neuroscience
                Neuroimaging
                Brain Morphometry
                Diffusion Tensor Imaging
                Tractography
                Biology and Life Sciences
                Neuroscience
                Brain Mapping
                Research and Analysis Methods
                Bioassays and Physiological Analysis
                Electrophysiological Techniques
                Brain Electrophysiology
                Electroencephalography
                Biology and Life Sciences
                Physiology
                Electrophysiology
                Neurophysiology
                Brain Electrophysiology
                Electroencephalography
                Biology and Life Sciences
                Neuroscience
                Neurophysiology
                Brain Electrophysiology
                Electroencephalography
                Biology and Life Sciences
                Neuroscience
                Brain Mapping
                Electroencephalography
                Medicine and Health Sciences
                Clinical Medicine
                Clinical Neurophysiology
                Electroencephalography
                Research and Analysis Methods
                Imaging Techniques
                Neuroimaging
                Electroencephalography
                Biology and Life Sciences
                Neuroscience
                Neuroimaging
                Electroencephalography
                Medicine and Health Sciences
                Diagnostic Medicine
                Diagnostic Radiology
                Magnetic Resonance Imaging
                Research and Analysis Methods
                Imaging Techniques
                Diagnostic Radiology
                Magnetic Resonance Imaging
                Medicine and Health Sciences
                Radiology and Imaging
                Diagnostic Radiology
                Magnetic Resonance Imaging
                Custom metadata
                vor-update-to-uncorrected-proof
                2020-12-10
                The human connectome project dataset is openly available on https://db.humanconnectome.org/. The BrainSpace toolbox is available under https://github.com/MICA-MNI/BrainSpace. Preprocessed group-level matrices, normative manifold maps, and integral scripts are openly available at https://git.io/JTg1l; instructions on how to access the main datafiles and how to reproduce the figures is available in the readme file of that repository.

                Life sciences
                Life sciences

                Comments

                Comment on this article