The relationship between spatial configuration and functional connectivity of brain regions

  1. Janine Diane Bijsterbosch  Is a corresponding author
  2. Mark W Woolrich
  3. Matthew F Glasser
  4. Emma C Robinson
  5. Christian F Beckmann
  6. David C Van Essen
  7. Samuel J Harrison
  8. Stephen M Smith
  1. University of Oxford, United Kingdom
  2. Washington University in St. Louis, United States
  3. King's College London, United Kingdom
  4. Radboud University Medical Centre, Netherlands

Abstract

Brain connectivity is often considered in terms of the communication between functionally distinct brain regions. Many studies have investigated the extent to which patterns of coupling strength between multiple neural populations relates to behaviour. For example, studies have used 'functional connectivity fingerprints' to characterise individuals' brain activity. Here, we investigate the extent to which the exact spatial arrangement of cortical regions interacts with measures of brain connectivity. We find that the shape and exact location of brain regions interact strongly with the modelling of brain connectivity, and present evidence that the spatial arrangement of functional regions is strongly predictive of non-imaging measures of behaviour and lifestyle. We believe that, in many cases, cross-subject variations in the spatial configuration of functional brain regions are being interpreted as changes in functional connectivity. Therefore, a better understanding of these effects is important when interpreting the relationship between functional imaging data and cognitive traits.

Data availability

The following previously published data sets were used
    1. WU-Minn HCP consortium Principal Investigators: David Van Essen and Kamil Ugurbil
    (2017) Human Connectome Project
    Freely available upon agreeing with Open Access Data Use Terms and Restricted Data Use Terms ( https://www.humanconnectome.org/study/hcp-young-adult/document/quick-reference-open-access-vs-restricted-data).

Article and author information

Author details

  1. Janine Diane Bijsterbosch

    Centre for Functional MRI of the Brain (FMRIB), Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
    For correspondence
    Janine.Bijsterbosch@ndcn.ox.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1385-9178
  2. Mark W Woolrich

    Oxford Centre for Human Brain Activity (OHBA), Wellcome Centre for Integrative NeuroImaging, Department of Psychiatry, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
  3. Matthew F Glasser

    Department of Neuroscience, School of Medicine, Washington University in St. Louis, St Louis, United States
    Competing interests
    No competing interests declared.
  4. Emma C Robinson

    Department of Biomedical Engineering, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
    Competing interests
    No competing interests declared.
  5. Christian F Beckmann

    Donders Institute, Radboud University Medical Centre, Nijmegen, Netherlands
    Competing interests
    No competing interests declared.
  6. David C Van Essen

    Department of Neuroscience, School of Medicine, Washington University in St. Louis, St Louis, United States
    Competing interests
    David C Van Essen, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7044-4721
  7. Samuel J Harrison

    Centre for Functional MRI of the Brain (FMRIB), Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5886-2389
  8. Stephen M Smith

    Centre for Functional MRI of the Brain (FMRIB), Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.

Funding

National Institutes of Health (1U54MH091657)

  • David C Van Essen

Wellcome (098369/Z/12/Z)

  • Stephen M Smith

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (864-12-003)

  • Christian F Beckmann

Wellcome (091509/Z/10/Z)

  • Stephen M Smith

Wellcome (203139/Z/16/Z)

  • Stephen M Smith

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

Ethics

Human subjects: HCP data were acquired using protocols approved by the Washington University institutional review board. Informed consent was obtained from subjects. Anonymised data are publicly available from ConnectomeDB (db.humanconnectome.org; Hodge et al., 2016). Certain parts of the dataset used in this study, such as the age of the subjects, are available subject to restricted data usage terms, requiring researchers to ensure that the anonymity of subjects is protected (Van Essen et al., 2013).

Copyright

© 2018, Bijsterbosch 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

  • 6,850
    views
  • 1,143
    downloads
  • 204
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Janine Diane Bijsterbosch
  2. Mark W Woolrich
  3. Matthew F Glasser
  4. Emma C Robinson
  5. Christian F Beckmann
  6. David C Van Essen
  7. Samuel J Harrison
  8. Stephen M Smith
(2018)
The relationship between spatial configuration and functional connectivity of brain regions
eLife 7:e32992.
https://doi.org/10.7554/eLife.32992

Share this article

https://doi.org/10.7554/eLife.32992

Further reading

  1. The exact location of certain brain regions is linked to intelligence, life satisfaction and other behavioural factors.

    1. Neuroscience
    Gáspár Oláh, Rajmund Lákovics ... Gábor Tamás
    Research Article

    Human-specific cognitive abilities depend on information processing in the cerebral cortex, where the neurons are significantly larger and their processes longer and sparser compared to rodents. We found that, in synaptically connected layer 2/3 pyramidal cells (L2/3 PCs), the delay in signal propagation from soma to soma is similar in humans and rodents. To compensate for the longer processes of neurons, membrane potential changes in human axons and/or dendrites must propagate faster. Axonal and dendritic recordings show that the propagation speed of action potentials (APs) is similar in human and rat axons, but the forward propagation of excitatory postsynaptic potentials (EPSPs) and the backward propagation of APs are 26 and 47% faster in human dendrites, respectively. Experimentally-based detailed biophysical models have shown that the key factor responsible for the accelerated EPSP propagation in human cortical dendrites is the large conductance load imposed at the soma by the large basal dendritic tree. Additionally, larger dendritic diameters and differences in cable and ion channel properties in humans contribute to enhanced signal propagation. Our integrative experimental and modeling study provides new insights into the scaling rules that help maintain information processing speed albeit the large and sparse neurons in the human cortex.