The ebb and flow of attention: Between-subject variation in intrinsic connectivity and cognition associated with the dynamics of ongoing experience
Cognition is dynamic, allowing us the flexibility to shift focus from different aspects of the environment, or between internally- and externally-oriented trains of thought. Although we understand how individuals switch attention across different tasks, the neurocognitive processes that underpin the...
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Published in | NeuroImage (Orlando, Fla.) Vol. 185; no. 1; pp. 286 - 299 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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United States
Elsevier Inc
15.01.2019
Elsevier Limited Elsevier |
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Abstract | Cognition is dynamic, allowing us the flexibility to shift focus from different aspects of the environment, or between internally- and externally-oriented trains of thought. Although we understand how individuals switch attention across different tasks, the neurocognitive processes that underpin the dynamics of less constrained elements of cognition are less well understood. To explore this issue, we developed a paradigm in which participants intermittently responded to external events across two conditions that systematically vary in their need for updating working memory based on information in the external environment. This paradigm distinguishes the influences on cognition that emerge because of demands placed by the task (sustained) from changes that result from the time elapsed since the last task response (transient). We used experience sampling to identify dynamic changes in ongoing cognition in this paradigm, and related between subject variation in these measures to variations in the intrinsic organisation of large-scale brain networks. We found systems important for attention were involved in the regulation of off-task thought. Coupling between the ventral attention network and regions of primary motor cortex was stronger for individuals who were able to regulate off-task thought in line with the demands of the task. This pattern of coupling was linked to greater task-related thought when environmental demands were high and elevated off-task thought when demands were low. In contrast, the coupling of the dorsal attention network with a region of lateral visual cortex was stronger for individuals for whom off-task thoughts transiently increased with the time since responding to the external world . This pattern is consistent with a role for this system in the time-limited top-down biasing of visual processing to increase behavioural efficiency. Unlike the attention networks, coupling between regions of the default mode network and dorsal occipital cortex was weaker for individuals for whom the level of detail decreased with the passage of time when the external task did not require continuous monitoring of external information. These data provide novel evidence for how neural systems vary across subjects and may underpin individual variation in the dynamics of thought, linking attention systems to the maintenance of task-relevant information, and the default mode network to supporting experiences with vivid detail.
•We explored between-subject variation in the neural correlates of ongoing thought.•The connectivity of attention networks was linked to the dynamics of off-task thought.•The ventral attention network was linked to sustained changes in off-task thought.•The dorsal attention network was linked to transient changes in off-task thought.•Default mode network connectivity was linked to levels of detail in ongoing thought. |
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AbstractList | Cognition is dynamic, allowing us the flexibility to shift focus from different aspects of the environment, or between internally- and externally-oriented trains of thought. Although we understand how individuals switch attention across different tasks, the neurocognitive processes that underpin the dynamics of less constrained elements of cognition are less well understood. To explore this issue, we developed a paradigm in which participants intermittently responded to external events across two conditions that systematically vary in their need for updating working memory based on information in the external environment. This paradigm distinguishes the influences on cognition that emerge because of demands placed by the task (sustained) from changes that result from the time elapsed since the last task response (transient). We used experience sampling to identify dynamic changes in ongoing cognition in this paradigm, and related between subject variation in these measures to variations in the intrinsic organisation of large-scale brain networks. We found systems important for attention were involved in the regulation of off-task thought. Coupling between the ventral attention network and regions of primary motor cortex was stronger for individuals who were able to regulate off-task thought in line with the demands of the task. This pattern of coupling was linked to greater task-related thought when environmental demands were high and elevated off-task thought when demands were low. In contrast, the coupling of the dorsal attention network with a region of lateral visual cortex was stronger for individuals for whom off-task thoughts transiently increased with the time since responding to the external world . This pattern is consistent with a role for this system in the time-limited top-down biasing of visual processing to increase behavioural efficiency. Unlike the attention networks, coupling between regions of the default mode network and dorsal occipital cortex was weaker for individuals for whom the level of detail decreased with the passage of time when the external task did not require continuous monitoring of external information. These data provide novel evidence for how neural systems vary across subjects and may underpin individual variation in the dynamics of thought, linking attention systems to the maintenance of task-relevant information, and the default mode network to supporting experiences with vivid detail. Cognition is dynamic, allowing us the flexibility to shift focus from different aspects of the environment, or between internally- and externally-oriented trains of thought. Although we understand how individuals switch attention across different tasks, the neurocognitive processes that underpin the dynamics of less constrained elements of cognition are less well understood. To explore this issue, we developed a paradigm in which participants intermittently responded to external events across two conditions that systematically vary in their need for updating working memory based on information in the external environment. This paradigm distinguishes the influences on cognition that emerge because of demands placed by the task (sustained) from changes that result from the time elapsed since the last task response (transient). We used experience sampling to identify dynamic changes in ongoing cognition in this paradigm, and related between subject variation in these measures to variations in the intrinsic organisation of large-scale brain networks. We found systems important for attention were involved in the regulation of off-task thought. Coupling between the ventral attention network and regions of primary motor cortex was stronger for individuals who were able to regulate off-task thought in line with the demands of the task. This pattern of coupling was linked to greater task-related thought when environmental demands were high and elevated off-task thought when demands were low. In contrast, the coupling of the dorsal attention network with a region of lateral visual cortex was stronger for individuals for whom off-task thoughts transiently increased with the time since responding to the external world increased. This pattern is consistent with a role for this system in the time-limited top-down biasing of visual processing to increase behavioural efficiency. Unlike the attention networks, coupling between regions of the default mode network and dorsal occipital cortex was weaker for individuals for whom the level of detail decreased with the passage of time when the external task did not require continuous monitoring of external information. These data provide novel evidence for how neural systems vary across subjects and may be underpin individual variation in the dynamics of thought, linking attention systems to the maintenance of task-relevant information, and the default mode network to supporting experiences with vivid detail. Cognition is dynamic, allowing us the flexibility to shift focus from different aspects of the environment, or between internally- and externally-oriented trains of thought. Although we understand how individuals switch attention across different tasks, the neurocognitive processes that underpin the dynamics of less constrained elements of cognition are less well understood. To explore this issue, we developed a paradigm in which participants intermittently responded to external events across two conditions that systematically vary in their need for updating working memory based on information in the external environment. This paradigm distinguishes the influences on cognition that emerge because of demands placed by the task (sustained) from changes that result from the time elapsed since the last task response (transient). We used experience sampling to identify dynamic changes in ongoing cognition in this paradigm, and related between subject variation in these measures to variations in the intrinsic organisation of large-scale brain networks. We found systems important for attention were involved in the regulation of off-task thought. Coupling between the ventral attention network and regions of primary motor cortex was stronger for individuals who were able to regulate off-task thought in line with the demands of the task. This pattern of coupling was linked to greater task-related thought when environmental demands were high and elevated off-task thought when demands were low. In contrast, the coupling of the dorsal attention network with a region of lateral visual cortex was stronger for individuals for whom off-task thoughts transiently increased with the time since responding to the external world . This pattern is consistent with a role for this system in the time-limited top-down biasing of visual processing to increase behavioural efficiency. Unlike the attention networks, coupling between regions of the default mode network and dorsal occipital cortex was weaker for individuals for whom the level of detail decreased with the passage of time when the external task did not require continuous monitoring of external information. These data provide novel evidence for how neural systems vary across subjects and may underpin individual variation in the dynamics of thought, linking attention systems to the maintenance of task-relevant information, and the default mode network to supporting experiences with vivid detail. •We explored between-subject variation in the neural correlates of ongoing thought.•The connectivity of attention networks was linked to the dynamics of off-task thought.•The ventral attention network was linked to sustained changes in off-task thought.•The dorsal attention network was linked to transient changes in off-task thought.•Default mode network connectivity was linked to levels of detail in ongoing thought. Cognition is dynamic, allowing us the flexibility to shift focus from different aspects of the environment, or between internally- and externally-oriented trains of thought. Although we understand how individuals switch attention across different tasks, the neurocognitive processes that underpin the dynamics of less constrained elements of cognition are less well understood. To explore this issue, we developed a paradigm in which participants intermittently responded to external events across two conditions that systematically vary in their need for updating working memory based on information in the external environment. This paradigm distinguishes the influences on cognition that emerge because of demands placed by the task (sustained) from changes that result from the time elapsed since the last task response (transient). We used experience sampling to identify dynamic changes in ongoing cognition in this paradigm, and related between subject variation in these measures to variations in the intrinsic organisation of large-scale brain networks. We found systems important for attention were involved in the regulation of off-task thought. Coupling between the ventral attention network and regions of primary motor cortex was stronger for individuals who were able to regulate off-task thought in line with the demands of the task. This pattern of coupling was linked to greater task-related thought when environmental demands were high and elevated off-task thought when demands were low. In contrast, the coupling of the dorsal attention network with a region of lateral visual cortex was stronger for individuals for whom off-task thoughts transiently increased with the time since responding to the external world . This pattern is consistent with a role for this system in the time-limited top-down biasing of visual processing to increase behavioural efficiency. Unlike the attention networks, coupling between regions of the default mode network and dorsal occipital cortex was weaker for individuals for whom the level of detail decreased with the passage of time when the external task did not require continuous monitoring of external information. These data provide novel evidence for how neural systems vary across subjects and may underpin individual variation in the dynamics of thought, linking attention systems to the maintenance of task-relevant information, and the default mode network to supporting experiences with vivid detail.Cognition is dynamic, allowing us the flexibility to shift focus from different aspects of the environment, or between internally- and externally-oriented trains of thought. Although we understand how individuals switch attention across different tasks, the neurocognitive processes that underpin the dynamics of less constrained elements of cognition are less well understood. To explore this issue, we developed a paradigm in which participants intermittently responded to external events across two conditions that systematically vary in their need for updating working memory based on information in the external environment. This paradigm distinguishes the influences on cognition that emerge because of demands placed by the task (sustained) from changes that result from the time elapsed since the last task response (transient). We used experience sampling to identify dynamic changes in ongoing cognition in this paradigm, and related between subject variation in these measures to variations in the intrinsic organisation of large-scale brain networks. We found systems important for attention were involved in the regulation of off-task thought. Coupling between the ventral attention network and regions of primary motor cortex was stronger for individuals who were able to regulate off-task thought in line with the demands of the task. This pattern of coupling was linked to greater task-related thought when environmental demands were high and elevated off-task thought when demands were low. In contrast, the coupling of the dorsal attention network with a region of lateral visual cortex was stronger for individuals for whom off-task thoughts transiently increased with the time since responding to the external world . This pattern is consistent with a role for this system in the time-limited top-down biasing of visual processing to increase behavioural efficiency. Unlike the attention networks, coupling between regions of the default mode network and dorsal occipital cortex was weaker for individuals for whom the level of detail decreased with the passage of time when the external task did not require continuous monitoring of external information. These data provide novel evidence for how neural systems vary across subjects and may underpin individual variation in the dynamics of thought, linking attention systems to the maintenance of task-relevant information, and the default mode network to supporting experiences with vivid detail. |
Author | Turnbull, Adam Smallwood, Jonathan Jefferies, Elizabeth Wang, Hao-Ting Margulies, Daniel S. Schooler, Jonathan W. |
Author_xml | – sequence: 1 givenname: Adam surname: Turnbull fullname: Turnbull, Adam email: agt520@york.ac.uk organization: Department of Psychology, University of York, UK – sequence: 2 givenname: Hao-Ting surname: Wang fullname: Wang, Hao-Ting organization: Department of Psychology, University of York, UK – sequence: 3 givenname: Jonathan W. surname: Schooler fullname: Schooler, Jonathan W. organization: Psychological and Brain Sciences, University of California, Santa Barbara, USA – sequence: 4 givenname: Elizabeth surname: Jefferies fullname: Jefferies, Elizabeth organization: Department of Psychology, University of York, UK – sequence: 5 givenname: Daniel S. surname: Margulies fullname: Margulies, Daniel S. organization: CNRS, Paris, France – sequence: 6 givenname: Jonathan surname: Smallwood fullname: Smallwood, Jonathan organization: Department of Psychology, University of York, UK |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30266263$$D View this record in MEDLINE/PubMed https://hal.science/hal-02383732$$DView record in HAL |
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ContentType | Journal Article |
Copyright | 2018 Elsevier Inc. Copyright © 2018 Elsevier Inc. All rights reserved. Copyright Elsevier Limited Jan 15, 2019 Distributed under a Creative Commons Attribution 4.0 International License |
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SubjectTerms | Attention Attention - physiology Brain - physiology Brain Mapping - methods Cognition Cognition & reasoning Cognition - physiology Cognitive science Cortex (motor) Creativity Female Humans Information processing Laboratories Magnetic Resonance Imaging Male Memory, Short-Term - physiology Nerve Net - physiology Neural networks Neuroscience Neurosciences Occipital lobe Short term memory Studies Variation Visual cortex Young Adult |
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Title | The ebb and flow of attention: Between-subject variation in intrinsic connectivity and cognition associated with the dynamics of ongoing experience |
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