Altered functional connectivity and regional brain activity in a triple-network model in minimally conscious state and vegetative-state/unresponsive wakefulness syndrome patients: A resting-state functional magnetic resonance imaging study

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Abstract

The purpose of this study was to investigate changes in functional connectivity and regional brain activity between and within the default mode network (DMN), salience network (SN), and executive control network (ECN) among individuals with disorders of consciousness (DOC) in the conditions of minimally conscious state (MCS) and vegetative-state/unresponsive wakefulness syndrome (VS/UWS). Twenty-five VS/UWS patients, 14 MCS patients, and 30 healthy individuals as normal control, completed resting-state fMRI scans. ROI-wise functional connectivity and fractional amplitude of low-frequency fluctuation (fALFF) were implemented to examine group differences. All ROI-wise and fALFF analyses masks were identified from the triple-network model. ROI-wise analyses indicated significantly decreased functional connectivity between posterior cingulate cortex (DMN)-left anterior insula (SN), right anterior insula (SN)-left dorsolateral prefrontal cortex (ECN), and right anterior insula (SN)-right amygdala (SN) in VS/UWS patients compared to MCS patients. Moreover, fALFF were observed reduced in the triple-network across all DOC patients, and as the clinical manifestations of DOC deteriorated from MCS to VS/UWS, fALFF in dorsal DMN, anterior/posterior SN, and left ECN became significantly reduced. Moreover, a positive correlation between fALFF of the left ECN and Coma Recovery Scale-Revised (CRS-R) total scores was found across all DOC patients. These findings contribute to a better understanding of the underlying neural mechanism of functional connectivity and regional brain activity in DOC patients, and this triple-network model provides new connectivity pattern changes that may be integrated in future diagnostic tools based on the neural signatures of conscious states.

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Most cited references 32

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Control of goal-directed and stimulus-driven attention in the brain.

Maurizio Corbetta, Gordon L Shulman (2002)

We review evidence for partially segregated networks of brain areas that carry out different attentional functions. One system, which includes parts of the intraparietal cortex and superior frontal cortex, is involved in preparing and applying goal-directed (top-down) selection for stimuli and responses. This system is also modulated by the detection of stimuli. The other system, which includes the temporoparietal cortex and inferior frontal cortex, and is largely lateralized to the right hemisphere, is not involved in top-down selection. Instead, this system is specialized for the detection of behaviourally relevant stimuli, particularly when they are salient or unexpected. This ventral frontoparietal network works as a 'circuit breaker' for the dorsal system, directing attention to salient events. Both attentional systems interact during normal vision, and both are disrupted in unilateral spatial neglect.

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Saliency, switching, attention and control: a network model of insula function.

Vinod Menon, Lucina Q. Uddin (2011)

The insula is a brain structure implicated in disparate cognitive, affective, and regulatory functions, including interoceptive awareness, emotional responses, and empathic processes. While classically considered a limbic region, recent evidence from network analysis suggests a critical role for the insula, particularly the anterior division, in high-level cognitive control and attentional processes. The crucial insight and view we present here is of the anterior insula as an integral hub in mediating dynamic interactions between other large-scale brain networks involved in externally oriented attention and internally oriented or self-related cognition. The model we present postulates that the insula is sensitive to salient events, and that its core function is to mark such events for additional processing and initiate appropriate control signals. The anterior insula and the anterior cingulate cortex form a "salience network" that functions to segregate the most relevant among internal and extrapersonal stimuli in order to guide behavior. Within the framework of our network model, the disparate functions ascribed to the insula can be conceptualized by a few basic mechanisms: (1) bottom-up detection of salient events, (2) switching between other large-scale networks to facilitate access to attention and working memory resources when a salient event is detected, (3) interaction of the anterior and posterior insula to modulate autonomic reactivity to salient stimuli, and (4) strong functional coupling with the anterior cingulate cortex that facilitates rapid access to the motor system. In this manner, with the insula as its integral hub, the salience network assists target brain regions in the generation of appropriate behavioral responses to salient stimuli. We suggest that this framework provides a parsimonious account of insula function in neurotypical adults, and may provide novel insights into the neural basis of disorders of affective and social cognition.

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A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks.

Devarajan Sridharan, Daniel Levitin, Vinod Menon (2008)

Cognitively demanding tasks that evoke activation in the brain's central-executive network (CEN) have been consistently shown to evoke decreased activation (deactivation) in the default-mode network (DMN). The neural mechanisms underlying this switch between activation and deactivation of large-scale brain networks remain completely unknown. Here, we use functional magnetic resonance imaging (fMRI) to investigate the mechanisms underlying switching of brain networks in three different experiments. We first examined this switching process in an auditory event segmentation task. We observed significant activation of the CEN and deactivation of the DMN, along with activation of a third network comprising the right fronto-insular cortex (rFIC) and anterior cingulate cortex (ACC), when participants perceived salient auditory event boundaries. Using chronometric techniques and Granger causality analysis, we show that the rFIC-ACC network, and the rFIC, in particular, plays a critical and causal role in switching between the CEN and the DMN. We replicated this causal connectivity pattern in two additional experiments: (i) a visual attention "oddball" task and (ii) a task-free resting state. These results indicate that the rFIC is likely to play a major role in switching between distinct brain networks across task paradigms and stimulus modalities. Our findings have important implications for a unified view of network mechanisms underlying both exogenous and endogenous cognitive control.

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Author and article information

Contributors

Yituo Wang: URI : http://loop.frontiersin.org/people/1538378/overview

Xiaoyu Xia: URI : http://loop.frontiersin.org/people/354928/overview

Ying Peng: URI : http://loop.frontiersin.org/people/1739313/overview

Bing Wu: URI : http://loop.frontiersin.org/people/493902/overview

Journal

Journal ID (nlm-ta): Front Behav Neurosci

Journal ID (iso-abbrev): Front Behav Neurosci

Journal ID (publisher-id): Front. Behav. Neurosci.

Title: Frontiers in Behavioral Neuroscience

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1662-5153

Publication date (Electronic): 10 October 2022

Publication date Collection: 2022

Volume: 16

Electronic Location Identifier: 1001519

Affiliations

[1] ¹Department of Radiology, Seventh Medical Center of Chinese PLA General Hospital , Beijing, China

[2] ²Beijing Engineering Research Center of Mixed Reality and Advanced Display, School of Optics and Photonics, Beijing Institute of Technology , Beijing, China

[3] ³Senior Department of Neurosurgery, First Medical Center of Chinese PLA General Hospital , Beijing, China

[4] ⁴Department of Neurosurgery, Hainan Hospital of Chinese PLA General Hospital , Sanya, China

[5] ⁵The Second School of Clinical Medicine, Southern Medical University , Guangzhou, China

Author notes

Edited by: Hao Shu, Southeast University, China

Reviewed by: Leon James, Bupa Cromwell Hospital, United Kingdom; Stephen Karl Larroque, University of Liège, Belgium; Zhen Zhou, University of Pennsylvania, United States

*Correspondence: Bing Wu, 13910720619@ 123456163.com

This article was submitted to Pathological Conditions, a section of the journal Frontiers in Behavioral Neuroscience

Article

DOI: 10.3389/fnbeh.2022.1001519

PMC ID: 9588962

PubMed ID: 36299294

SO-VID: 4ef29ad3-52d6-458d-a6e3-1fcdb2675218

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 23 July 2022

Date accepted : 26 September 2022

Page count

Figures: 2, Tables: 1, Equations: 0, References: 32, Pages: 9, Words: 5769

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Altered functional connectivity and regional brain activity in a triple-network model in minimally conscious state and vegetative-state/unresponsive wakefulness syndrome patients: A resting-state functional magnetic resonance imaging study

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Most cited references 32

Control of goal-directed and stimulus-driven attention in the brain.

Saliency, switching, attention and control: a network model of insula function.

A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks.

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