1. Neuroscience
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Reconfiguration of functional brain networks and metabolic cost converge during task performance

  1. Andreas Hahn  Is a corresponding author
  2. Michael Breakspear
  3. Lucas Rischka
  4. Wolfgang Wadsak
  5. Godber M Godbersen
  6. Verena Pichler
  7. Paul Michenthaler
  8. Thomas Vanicek
  9. Marcus Hacker
  10. Siegfried Kasper
  11. Rupert Lanzenberger
  12. Luca Cocchi
  1. Medical University of Vienna, Austria
  2. QIMR Berghofer Medical Research Institute, Australia
Research Article
  • Cited 8
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Cite this article as: eLife 2020;9:e52443 doi: 10.7554/eLife.52443

Abstract

The ability to solve cognitive tasks depends upon adaptive changes in the organization of whole-brain functional networks. However, the link between task-induced network reconfigurations and their underlying energy demands is poorly understood. We address this by multimodal network analyses integrating functional and molecular neuroimaging acquired concurrently during a complex cognitive task. Task engagement elicited a marked increase in the association between glucose consumption and functional brain network reorganization. This convergence between metabolic and neural processes was specific to feedforward connections linking the visual and dorsal attention networks, in accordance with task requirements of visuo-spatial reasoning. Further increases in cognitive load above initial task engagement did not affect the relationship between metabolism and network reorganization but only modulated existing interactions. Our findings show how the upregulation of key computational mechanisms to support cognitive performance unveils the complex, interdependent changes in neural metabolism and neuro-vascular responses.

Data availability

We cannot publicly share raw data for reasons of data protection; processed data have been deposited to Dryad Digital Repository under the DOI 10.5061/dryad.zcrjdfn7p

The following data sets were generated

Article and author information

Author details

  1. Andreas Hahn

    Department of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria
    For correspondence
    andreas.hahn@meduniwien.ac.at
    Competing interests
    Andreas Hahn, This research was supported by a grant from the Austrian Science Fund to A. Hahn (FWF KLI 610)..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9727-7580
  2. Michael Breakspear

    Systems Neuroscience Group, QIMR Berghofer Medical Research Institute, Brisbane, Australia
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4943-3969
  3. Lucas Rischka

    Department of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria
    Competing interests
    Lucas Rischka, L. Rischka is recipient of a DOC Fellowship of the Austrian Academy of Sciences at the Department of Psychiatry and Psychotherapy, Medical University of Vienna..
  4. Wolfgang Wadsak

    Department of Biomedical Imaging and Image-guided Therapy, Division of Nuclear Medicine, Medical University of Vienna, Vienna, Austria
    Competing interests
    Wolfgang Wadsak, W.W. declares to having received speaker honoraria from the GE Healthcare and research grants from Ipsen Pharma, Eckert-Ziegler AG, Scintomics, and ITG; and working as a part time employee of CBmed Ltd. (Center for Biomarker Research in Medicine, Graz, Austria)..
  5. Godber M Godbersen

    Department of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  6. Verena Pichler

    Department of Biomedical Imaging and Image-guided Therapy, Division of Nuclear Medicine, Medical University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  7. Paul Michenthaler

    Department of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  8. Thomas Vanicek

    Department of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  9. Marcus Hacker

    Department of Biomedical Imaging and Image-guided Therapy, Division of Nuclear Medicine, Medical University of Vienna, Vienna, Austria
    Competing interests
    Marcus Hacker, M.H. received consulting fees and/or honoraria from Bayer Healthcare BMS, Eli Lilly, EZAG, GE Healthcare, Ipsen, ITM, Janssen, Roche, and Siemens Healthineers..
  10. Siegfried Kasper

    Department of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria
    Competing interests
    Siegfried Kasper, S.K. received grants/research support, consulting fees and/or honoraria within the last three years from Angelini, AOP Orphan Pharmaceuticals AG, Celgene GmbH, Eli Lilly, Janssen-Cilag Pharma GmbH, KRKA-Pharma, Lundbeck A/S, Mundipharma, Neuraxpharm, Pfizer, Sage, Sanofi, Schwabe, Servier, Shire, Sumitomo Dainippon Pharma Co. Ltd., Sun Pharmaceutical Industries Ltd. and Takeda..
  11. Rupert Lanzenberger

    Department of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria
    Competing interests
    Rupert Lanzenberger, R.L. received conference speaker honorarium within the last three years from Shire and support from Siemens Healthcare regarding clinical research using PET/MR. He is shareholder of BM Health GmbH since 2019..
  12. Luca Cocchi

    Systems Neuroscience Group, QIMR Berghofer Medical Research Institute, Brisbane, Australia
    Competing interests
    Luca Cocchi, L. Cocchi is supported by the Australian National Health Medical Research Council (L.C. 1099082 and 1138711)..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3651-2676

Funding

Austrian Science Fund (FWF KLI 610)

  • Andreas Hahn

Austrian Academy of Sciences

  • Lucas Rischka

Australian National Health Medical Research Council (1099082 and 1138711)

  • Luca Cocchi

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

Ethics

Human subjects: After detailed explanation of the study protocol, all participants gave written informed consent. The study was approved by the Ethics Committee (ethics number: 1479/2015) of the Medical University of Vienna and procedures were carried out in accordance with the Declaration of Helsinki.

Reviewing Editor

  1. Thomas Yeo, National University of Singapore, Singapore

Publication history

  1. Received: October 4, 2019
  2. Accepted: April 7, 2020
  3. Accepted Manuscript published: April 21, 2020 (version 1)
  4. Version of Record published: April 22, 2020 (version 2)

Copyright

© 2020, Hahn 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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