Task-evoked metabolic demands of the posteromedial default mode network are shaped by dorsal attention and frontoparietal control networks
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.
-
Data from: Task-evoked metabolic demands of the posteromedial default mode network are shaped by dorsal attention and frontoparietal control networksDryad Digital Repository, doi:10.5061/dryad.5qfttdzbd.
Article and author information
Author details
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).
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
-
- 939
- views
-
- 141
- downloads
-
- 16
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Neuroscience
In albino mice and EphB1 knockout mice, mistargeted retinal ganglion cell axons form dense islands of axon terminals in the dorsal lateral geniculate nuclei (dLGN). The formation of these islands of retinal input depends on developmental patterns of spontaneous retinal activity. We reconstructed the microcircuitry of the activity-dependent islands and found that the boundaries of the island represent a remarkably strong segregation within retinogeniculate connectivity. We conclude that when sets of retinal input are established in the wrong part of the dLGN, the developing circuitry responds by forming a synaptically isolated subcircuit within the otherwise fully connected network. The fact that there is a developmental starting condition that can induce a synaptically segregated microcircuit has important implications for our understanding of the organization of visual circuits and our understanding of the implementation of activity-dependent development.
-
- Neuroscience
Neural activity in auditory cortex tracks the amplitude-onset envelope of continuous speech, but recent work counterintuitively suggests that neural tracking increases when speech is masked by background noise, despite reduced speech intelligibility. Noise-related amplification could indicate that stochastic resonance – the response facilitation through noise – supports neural speech tracking, but a comprehensive account is lacking. In five human electroencephalography experiments, the current study demonstrates a generalized enhancement of neural speech tracking due to minimal background noise. Results show that (1) neural speech tracking is enhanced for speech masked by background noise at very high signal-to-noise ratios (~30 dB SNR) where speech is highly intelligible; (2) this enhancement is independent of attention; (3) it generalizes across different stationary background maskers, but is strongest for 12-talker babble; and (4) it is present for headphone and free-field listening, suggesting that the neural-tracking enhancement generalizes to real-life listening. The work paints a clear picture that minimal background noise enhances the neural representation of the speech onset-envelope, suggesting that stochastic resonance contributes to neural speech tracking. The work further highlights non-linearities of neural tracking induced by background noise that make its use as a biological marker for speech processing challenging.