Format

Send to

Choose Destination
J Neurosci. 2017 Jan 11;37(2):281-290. doi: 10.1523/JNEUROSCI.1759-16.2016.

Dynamic Shifts in Large-Scale Brain Network Balance As a Function of Arousal.

Author information

1
Department of Psychology, Northwestern University, Evanston, Illinois 60208, c.young@donders.ru.nl.
2
Donders Institute for Brain, Cognition and Behaviour.
3
Department of Psychiatry, and.
4
Department of Cognitive Neuroscience, Maastricht University, 6200 MD Maastricht, The Netherlands.
5
The Steve Tisch School of Film and Television.
6
Functional Brain Center, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel Aviv 6423906, Israel, and.
7
Department of Cognitive Neuroscience, Radboud University Medical Center, 6525 HP Nijmegen, The Netherlands.
8
Department of Psychiatry and Psychotherapy, University Hospital Essen, 45147 Essen, Germany.
9
Sackler Faculty of Medicine, and.
10
School of Psychological Sciences, Tel Aviv University, Tel Aviv 69978, Israel.

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 neurophysiological 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.

SIGNIFICANCE STATEMENT:

How does brain functioning change in arousing or stressful situations? Extant literature suggests that through global projections, arousal-related neuromodulatory changes can rapidly alter coordination of neural activity across brain-wide neural systems or large-scale networks. Since it is unknown how such processes unfold, we developed a method to dynamically track levels of within-network and between-network interaction. We applied this technique to human neuroimaging data acquired while participants watched realistic and emotionally arousing cinematographic material. Results demonstrate that cohesion within the salience network monotonically increases with arousal, while cohesion of this network with the executive control network peaks at moderate arousal. Our findings explain how cognitive performance shifts as a function of arousal, and provide new insights into vulnerability for stress-related psychopathology.

KEYWORDS:

arousal; functional MRI; functional connectivity; large-scale networks; stress

PMID:
28077708
DOI:
10.1523/JNEUROSCI.1759-16.2016
[Indexed for MEDLINE]
Free full text

Supplemental Content

Full text links

Icon for HighWire
Loading ...
Support Center