1. Neuroscience

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
https://doi.org/10.7554/eLife.32992
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Cite this article
  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
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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).
    https://www.humanconnectome.org/

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).

Reviewing Editor

  1. Chris Honey

Version history

  1. Received: October 20, 2017
  2. Accepted: February 15, 2018
  3. Accepted Manuscript published: February 16, 2018 (version 1)
  4. Version of Record published: March 20, 2018 (version 2)

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.

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  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

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Further reading

    1. Neuroscience

    The relationship between spatial configuration and functional connectivity of brain regions revisited

    Janine Diane Bijsterbosch, Christian F Beckmann ... Samuel J Harrison
    Research Advance Updated

    Previously we showed that network-based modelling of brain connectivity interacts strongly with the shape and exact location of brain regions, such that cross-subject variations in the spatial configuration of functional brain regions are being interpreted as changes in functional connectivity (Bijsterbosch et al., 2018). Here we show that these spatial effects on connectivity estimates actually occur as a result of spatial overlap between brain networks. This is shown to systematically bias connectivity estimates obtained from group spatial ICA followed by dual regression. We introduce an extended method that addresses the bias and achieves more accurate connectivity estimates.

  2. Listen to Janine Bijsterbosch explain how our behaviour is moulded by our brain.

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

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