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 Breakspear
  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 Breakspear

    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.

Reviewing Editor

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

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).

Version 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.

Metrics

  • 710
    views
  • 117
    downloads
  • 2
    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. 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 Breakspear
  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

Share this article

https://doi.org/10.7554/eLife.84683

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.