Task-evoked metabolic demands of the posteromedial default mode network are shaped by dorsal attention and frontoparietal control networks

  1. Godber M Godbersen
  2. Sebastian Klug
  3. Wolfgang Wadsak
  4. Verena Pichler
  5. Julia Raitanen
  6. Anna Rieckmann
  7. Lars Stiernman
  8. Luca Cocchi
  9. Mike Breakspears
  10. Marcus Hacker
  11. Rupert Lanzenberger
  12. Andreas Hahn  Is a corresponding author
  1. Medical University of Vienna, Austria
  2. University of Vienna, Austria
  3. Umeå University, Sweden
  4. QIMR Berghofer Medical Research Institute, Australia
  5. University of Newcastle Australia, Australia

Abstract

External tasks evoke characteristic fMRI BOLD signal deactivations in the default mode network (DMN). However, for the corresponding metabolic glucose demands both decreases and increases have been reported. To resolve this discrepancy, functional PET/MRI data from 50 healthy subjects performing Tetris® were combined with previously published data sets of working memory, visual and motor stimulation. We show that the glucose metabolism of the posteromedial DMN is dependent on the metabolic demands of the correspondingly engaged task-positive networks. Specifically, the dorsal attention and frontoparietal network shape the glucose metabolism of the posteromedial DMN in opposing directions. While tasks that mainly require an external focus of attention lead to a consistent downregulation of both metabolism and the BOLD signal in the posteromedial DMN, cognitive control during working memory requires a metabolically expensive BOLD suppression. This indicates that two types of BOLD deactivations with different-oxygen-to-glucose index may occur in this region. We further speculate that consistent downregulation of the two signals is mediated by decreased glutamate signaling, while divergence may be subject to active GABAergic inhibition. The results demonstrate that the DMN relates to cognitive processing in a flexible manner and does not always act as a cohesive task-negative network in isolation.

Data availability

Raw data will not be publicly available due to reasons of data protection. Sharing of raw data requires a data sharing agreement, approved by the departments of legal affairs and data clearing of the Medical University of Vienna. Details about this process can be obtained from the corresponding author. Processed data are available at Dryad https://doi.org/10.5061/dryad.5qfttdzbd. Custom code is available at GitHub https://github.com/NeuroimagingLabsMUV/Godbersen2023_eLife.

The following data sets were generated

Article and author information

Author details

  1. Godber M Godbersen

    Department of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  2. Sebastian Klug

    Department of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  3. Wolfgang Wadsak

    Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Vienna, Austria
    Competing interests
    Wolfgang Wadsak, 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)..
  4. Verena Pichler

    Department of Pharmaceutical Sciences, University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  5. Julia Raitanen

    Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  6. Anna Rieckmann

    Umeå Center for Functional Brain Imaging, Umeå University, Umea, Sweden
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5389-1578
  7. Lars Stiernman

    Department of Integrative Medical Biology, Umeå University, Umea, Sweden
    Competing interests
    No competing interests declared.
  8. Luca Cocchi

    Clinical Brain Networks 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:" 0000-0003-3651-2676
  9. Mike Breakspears

    School of Medicine and Public Health, University of Newcastle Australia, Brisbane, Australia
    Competing interests
    No competing interests declared.
  10. Marcus Hacker

    Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Vienna, Austria
    Competing interests
    Marcus Hacker, received consulting fees and/or honoraria from Bayer Healthcare BMS, Eli Lilly, EZAG, GE Healthcare, Ipsen, ITM, Janssen, Roche, and Siemens Healthineers..
  11. Rupert Lanzenberger

    Department of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria
    Competing interests
    Rupert Lanzenberger, received investigator-initiated research funding from Siemens Healthcare regarding clinical research using PET/MRI. He is a shareholder of the start-up company BM Health GmbH since 2019..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4641-9539
  12. Andreas Hahn

    Department of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria
    For correspondence
    andreas.hahn@meduniwien.ac.at
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9727-7580

Funding

Austrian Science Fund (KLI610)

  • Andreas Hahn

Medical University of Vienna (MDPhD Excellence Programm)

  • Sebastian Klug

European Research Council (ERC-STG-716065)

  • Anna Rieckmann
  • Lars Stiernman

National Health and Medical Research Council (GN2001283)

  • 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: All participants provided written informed consent after a detailed explanation of the study protocol, they were insured and reimbursed for participation. The study was approved by the Ethics Committee of the Medical University of Vienna (ethics number 1479/2015) and procedures were carried out according to the Declaration of Helsinki. The study was pre-registered at ClinicalTrials.gov (NCT03485066).

Reviewing Editor

  1. Shella Keilholz, Emory University and Georgia Institute of Technology, United States

Publication history

  1. Preprint posted: August 12, 2022 (view preprint)
  2. Received: November 3, 2022
  3. Accepted: May 3, 2023
  4. Accepted Manuscript published: May 25, 2023 (version 1)
  5. Accepted Manuscript updated: May 26, 2023 (version 2)
  6. Version of Record published: May 30, 2023 (version 3)

Copyright

© 2023, Godbersen 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. Godber M Godbersen
  2. Sebastian Klug
  3. Wolfgang Wadsak
  4. Verena Pichler
  5. Julia Raitanen
  6. Anna Rieckmann
  7. Lars Stiernman
  8. Luca Cocchi
  9. Mike Breakspears
  10. Marcus Hacker
  11. Rupert Lanzenberger
  12. Andreas Hahn
(2023)
Task-evoked metabolic demands of the posteromedial default mode network are shaped by dorsal attention and frontoparietal control networks
eLife 12:e84683.
https://doi.org/10.7554/eLife.84683

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