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Integration and segregation across large-scale intrinsic brain networks as a marker of sustained attention and task-unrelated thought
Journal article   Open access   Peer reviewed

Integration and segregation across large-scale intrinsic brain networks as a marker of sustained attention and task-unrelated thought

Agnieszka Zuberer, Aaron Kucyi, Ayumu Yamashita, Charley M. Wu, Martin Walter, Eve M. Valera and Michael Esterman
NeuroImage (Orlando, Fla.), v 229, 117610
01 Apr 2021
PMID: 33418073
url
https://doi.org/10.1016/j.neuroimage.2020.117610View
Published, Version of Record (VoR) Open

Abstract

fMRI Integration Segregation Spontaneous thought Sustained attention
•Most of our brain activity is unrelated to immediate external events.•We spend up to 50% of our time engaged in task-unrelated thought that contribute to attentional lapses.•We mapped intrinsic fluctuations of sustained attention and mind wandering.•Optimal sustained attention involves concurrent network segregation and integration.•Mind wandering disrupts specific neural subsystems of sustained attention.•Our findings provide a novel framework for global markers of sustained attention. Sustained attention is a fundamental cognitive process that can be decoupled from distinct external events, and instead emerges from ongoing intrinsic large-scale network interdependencies fluctuating over seconds to minutes. Lapses of sustained attention are commonly associated with the subjective experience of mind wandering and task-unrelated thoughts. Little is known about how fluctuations in information processing underpin sustained attention, nor how mind wandering undermines this information processing. To overcome this, we used fMRI to investigate brain activity during subjects’ performance (n=29) of a cognitive task that was optimized to detect and isolate continuous fluctuations in both sustained attention (via motor responses) and task-unrelated thought (via subjective reports). We then investigated sustained attention with respect to global attributes of communication throughout the functional architecture, i.e., by the segregation and integration of information processing across large scale-networks. Further, we determined how task-unrelated thoughts related to these global information processing markers of sustained attention. The results show that optimal states of sustained attention favor both enhanced segregation and reduced integration of information processing in several task-related large-scale cortical systems with concurrent reduced segregation and enhanced integration in the auditory and sensorimotor systems. Higher degree of mind wandering was associated with losses of the favored segregation and integration of specific subsystems in our sustained attention model. Taken together, we demonstrate that intrinsic ongoing neural fluctuations are characterized by two converging communication modes throughout the global functional architecture, which give rise to optimal and suboptimal attention states. We discuss how these results might potentially serve as neural markers for clinically abnormal attention. Most of our brain activity unfolds in an intrinsic manner, i.e., is unrelated to immediate external stimuli or tasks. Here we use a gradual continuous performance task to map this intrinsic brain activity to both fluctuations of sustained attention and mind wandering. We show that optimal sustained attention is associated with concurrent segregation and integration of information processing within many large-scale brain networks, while task-unrelated thought is related to sub-optimal information processing in specific subsystems of this sustained attention network model. These findings provide a novel information processing framework for investigating the neural basis of sustained attention, by mapping attentional fluctuations to genuinely global features of intra-brain communication.

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Collaboration types
Domestic collaboration
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Web of Science research areas
Neuroimaging
Neurosciences
Radiology, Nuclear Medicine & Medical Imaging
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