Dynamic shifts in large-scale brain network balance as a function of arousal

Christina B. Young*, Gal Raz, Daphne Everaerd, Christian F. Beckmann, Indira Tendolkar, Talma Hendler, Guillén Fernández, Erno J. Hermans

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

91 Scopus citations

Abstract

The ability to temporarily prioritize rapid and vigilant reactions over slower higher-order cognitive functions is essential for adaptive responding to threat. This reprioritization is believed to reflect shifts in resource allocation between large-scale brain networks that support these cognitive functions, including the salience and executive control networks. However, how changes in communication within and between such networks dynamically unfold as a function of threat-related arousal remains unknown. To address this issue, we collected functional MRI data and continuously assessed the heart rate from 120 healthy human adults as they viewed emotionally arousing and ecologically valid cinematographic material. We then developed an analysis method that tracks dynamic changes in large-scale network cohesion by quantifying the level of within-network and between-network interaction. We found a monotonically increasing relationship between heart rate, a physiological index of arousal, and within-network cohesion in the salience network, indicating that coordination of activity within the salience network dynamically tracks arousal. Strikingly, salience-executive control between-network cohesion peaked at moderate arousal. These findings indicate that at moderate arousal, which has been associated with optimal noradrenergic signaling, the salience network is optimally able to engage the executive control network to coordinate cognitive activity, but is unable to do so at tonically elevated noradrenergic levels associated with acute stress. Our findings extend neurophysio-logical models of the effects of stress-related neuromodulatory signaling at the cellular level to large-scale neural systems, and thereby explain shifts in cognitive functioning during acute stress, which may play an important role in the development and maintenance of stress-related mental disorders.

Original languageEnglish
Pages (from-to)281-290
Number of pages10
JournalJournal of Neuroscience
Volume37
Issue number2
DOIs
StatePublished - 11 Jan 2017

Funding

FundersFunder number
National Science FoundationDGE0824162
European Research CouncilERC-2015CoG 682591, 602186
Ministry of Science, Technology and Space
Nederlandse Organisatie voor Wetenschappelijk Onderzoek918.66.613, 451.07.019

    Keywords

    • Arousal
    • Functional MRI
    • Functional connectivity
    • Large-scale networks
    • Stress

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