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 inNeuroImage (Orlando, Fla.) Vol. 213; p. 116687
Main Authors Betzel, Richard F., Byrge, Lisa, Esfahlani, Farnaz Zamani, Kennedy, Daniel P.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.06.2020
Elsevier Limited
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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.
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
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  surname: Betzel
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  surname: Byrge
  fullname: Byrge, Lisa
  organization: Department of Psychological and Brain Sciences, USA
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  givenname: Farnaz Zamani
  surname: Esfahlani
  fullname: Esfahlani, Farnaz Zamani
  organization: Department of Psychological and Brain Sciences, USA
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  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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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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