Temporal fluctuations in the brain’s modular architecture during movie-watching
Brain networks are flexible and reconfigure over time to support ongoing cognitive processes. However, tracking statistically meaningful reconfigurations across time has proven difficult. This has to do largely with issues related to sampling variability, making instantaneous estimation of network o...
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Published in | NeuroImage (Orlando, Fla.) Vol. 213; p. 116687 |
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Language | English |
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01.06.2020
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Abstract | Brain networks are flexible and reconfigure over time to support ongoing cognitive processes. However, tracking statistically meaningful reconfigurations across time has proven difficult. This has to do largely with issues related to sampling variability, making instantaneous estimation of network organization difficult, along with increased reliance on task-free (cognitively unconstrained) experimental paradigms, limiting the ability to interpret the origin of changes in network structure over time. Here, we address these challenges using time-varying network analysis in conjunction with a naturalistic viewing paradigm. Specifically, we developed a measure of inter-subject network similarity and used this measure as a coincidence filter to identify synchronous fluctuations in network organization across individuals. Applied to movie-watching data, we found that periods of high inter-subject similarity coincided with reductions in network modularity and increased connectivity between cognitive systems. In contrast, low inter-subject similarity was associated with increased system segregation and more rest-like architectures. We then used a data-driven approach to uncover clusters of functional connections that follow similar trajectories over time and are more strongly correlated during movie-watching than at rest. Finally, we show that synchronous fluctuations in network architecture over time can be linked to a subset of features in the movie. Our findings link dynamic fluctuations in network integration and segregation to patterns of inter-subject similarity, and suggest that moment-to-moment fluctuations in functional connectivity reflect shared cognitive processing across individuals. |
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AbstractList | Brain networks are flexible and reconfigure over time to support ongoing cognitive processes. However, tracking statistically meaningful reconfigurations across time has proven difficult. This has to do largely with issues related to sampling variability, making instantaneous estimation of network organization difficult, along with increased reliance on task-free (cognitively unconstrained) experimental paradigms, limiting the ability to interpret the origin of changes in network structure over time. Here, we address these challenges using time-varying network analysis in conjunction with a naturalistic viewing paradigm. Specifically, we developed a measure of inter-subject network similarity and used this measure as a coincidence filter to identify synchronous fluctuations in network organization across individuals. Applied to movie-watching data, we found that periods of high inter-subject similarity coincided with reductions in network modularity and increased connectivity between cognitive systems. In contrast, low inter-subject similarity was associated with increased system segregation and more rest-like architectures. We then used a data-driven approach to uncover clusters of functional connections that follow similar trajectories over time and are more strongly correlated during movie-watching than at rest. Finally, we show that synchronous fluctuations in network architecture over time can be linked to a subset of features in the movie. Our findings link dynamic fluctuations in network integration and segregation to patterns of inter-subject similarity, and suggest that moment-to-moment fluctuations in functional connectivity reflect shared cognitive processing across individuals. Brain networks are flexible and reconfigure over time to support ongoing cognitive processes. However, tracking statistically meaningful reconfigurations across time has proven difficult. This has to do largely with issues related to sampling variability, making instantaneous estimation of network organization difficult, along with increased reliance on task-free (cognitively unconstrained) experimental paradigms, limiting the ability to interpret the origin of changes in network structure over time. Here, we address these challenges using time-varying network analysis in conjunction with a naturalistic viewing paradigm. Specifically, we developed a measure of inter-subject network similarity and used this measure as a coincidence filter to identify synchronous fluctuations in network organization across individuals. Applied to movie-watching data, we found that periods of high inter-subject similarity coincided with reductions in network modularity and increased connectivity between cognitive systems. In contrast, low inter-subject similarity was associated with increased system segregation and more rest-like architectures. We then used a data-driven approach to uncover clusters of functional connections that follow similar trajectories over time and are more strongly correlated during movie-watching than at rest. Finally, we show that synchronous fluctuations in network architecture over time can be linked to a subset of features in the movie. Our findings link dynamic fluctuations in network integration and segregation to patterns of inter-subject similarity, and suggest that moment-to-moment fluctuations in functional connectivity reflect shared cognitive processing across individuals.Brain networks are flexible and reconfigure over time to support ongoing cognitive processes. However, tracking statistically meaningful reconfigurations across time has proven difficult. This has to do largely with issues related to sampling variability, making instantaneous estimation of network organization difficult, along with increased reliance on task-free (cognitively unconstrained) experimental paradigms, limiting the ability to interpret the origin of changes in network structure over time. Here, we address these challenges using time-varying network analysis in conjunction with a naturalistic viewing paradigm. Specifically, we developed a measure of inter-subject network similarity and used this measure as a coincidence filter to identify synchronous fluctuations in network organization across individuals. Applied to movie-watching data, we found that periods of high inter-subject similarity coincided with reductions in network modularity and increased connectivity between cognitive systems. In contrast, low inter-subject similarity was associated with increased system segregation and more rest-like architectures. We then used a data-driven approach to uncover clusters of functional connections that follow similar trajectories over time and are more strongly correlated during movie-watching than at rest. Finally, we show that synchronous fluctuations in network architecture over time can be linked to a subset of features in the movie. Our findings link dynamic fluctuations in network integration and segregation to patterns of inter-subject similarity, and suggest that moment-to-moment fluctuations in functional connectivity reflect shared cognitive processing across individuals. |
ArticleNumber | 116687 |
Author | Byrge, Lisa Betzel, Richard F. Esfahlani, Farnaz Zamani Kennedy, Daniel P. |
AuthorAffiliation | 2 Cognitive Science Program, Indiana University, Bloomington, IN 47405 3 Program in Neuroscience, Indiana University, Bloomington, IN 47405 1 Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN 47405 4 Network Science Institute, Indiana University, Bloomington, IN 47405 |
AuthorAffiliation_xml | – name: 1 Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN 47405 – name: 2 Cognitive Science Program, Indiana University, Bloomington, IN 47405 – name: 4 Network Science Institute, Indiana University, Bloomington, IN 47405 – name: 3 Program in Neuroscience, Indiana University, Bloomington, IN 47405 |
Author_xml | – sequence: 1 givenname: Richard F. surname: Betzel fullname: Betzel, Richard F. email: rbetzel@indiana.edu organization: Department of Psychological and Brain Sciences, USA – sequence: 2 givenname: Lisa surname: Byrge fullname: Byrge, Lisa organization: Department of Psychological and Brain Sciences, USA – sequence: 3 givenname: Farnaz Zamani surname: Esfahlani fullname: Esfahlani, Farnaz Zamani organization: Department of Psychological and Brain Sciences, USA – sequence: 4 givenname: Daniel P. surname: Kennedy fullname: Kennedy, Daniel P. organization: Department of Psychological and Brain Sciences, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32126299$$D View this record in MEDLINE/PubMed |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 RFB and DPK conceptualized the project. LB and DPK collected data. RFB and DPK wrote the original draft. All authors helped with data analysis. All authors helped review and edit the manuscript. AUTHOR CONTRIBUTIONS All authors conceived of the study. LB and DPK designed experimental protocols, collected, and preprocessed all fMRI data. RFB and FZE performed all analyses. All authors wrote and approved of the manuscript. |
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SubjectTerms | Adult Brain Brain - physiology Brain architecture Brain Mapping Cognition & reasoning Cognitive ability Female Humans Information processing Magnetic Resonance Imaging Male Mental Processes - physiology Motion Pictures Nerve Net - physiology Neural networks |
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Title | Temporal fluctuations in the brain’s modular architecture during movie-watching |
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