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Temporal Dynamics and Developmental Maturation of Salience, Default and Central-Executive Network Interactions Revealed by Variational Bayes Hidden Markov Modeling

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  • Srikanth Ryali
  • Kaustubh Supekar
  • Tianwen Chen
  • John Kochalka
  • Weidong Cai
  • Jonathan Nicholas
  • Aarthi Padmanabhan
  • Vinod Menon

Abstract

Little is currently known about dynamic brain networks involved in high-level cognition and their ontological basis. Here we develop a novel Variational Bayesian Hidden Markov Model (VB-HMM) to investigate dynamic temporal properties of interactions between salience (SN), default mode (DMN), and central executive (CEN) networks—three brain systems that play a critical role in human cognition. In contrast to conventional models, VB-HMM revealed multiple short-lived states characterized by rapid switching and transient connectivity between SN, CEN, and DMN. Furthermore, the three “static” networks occurred in a segregated state only intermittently. Findings were replicated in two adult cohorts from the Human Connectome Project. VB-HMM further revealed immature dynamic interactions between SN, CEN, and DMN in children, characterized by higher mean lifetimes in individual states, reduced switching probability between states and less differentiated connectivity across states. Our computational techniques provide new insights into human brain network dynamics and its maturation with development.Author Summary: Characterizing the temporal dynamics of functional interactions between distributed brain regions is of fundamental importance for understanding human brain organization and its development. Progress in the field has been hampered both by a lack of strong computational techniques to investigate brain dynamics and an inadequate focus on core brain systems involved in higher-order cognition. Here we address these gaps by developing a novel variational Bayesian Hidden Markov Model (VB-HMM) that uncovers non-stationary dynamical functional networks in human fMRI data. In two cohorts of adults, VB-HMM revealed multiple short-lived states characterized by rapid switching and transient connectivity between the salience (SN), default mode (DMN), and central executive (CEN) networks—three brain systems critical for higher-order cognition. In children, relative to adults, VB-HMM revealed immature dynamic interactions between SN, CEN, and DMN, characterized by higher mean lifetimes in individual states, reduced switching probability between states and less differentiated connectivity across states. Our findings suggest that the flexibility of switching between distinct brain states is weaker in childhood, and they provide a novel framework for modeling immature brain network organization in children. More generally, the approach used here may prove useful to the investigation of dynamic brain organization in neurodevelopmental and psychiatric disorders.

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  • Srikanth Ryali & Kaustubh Supekar & Tianwen Chen & John Kochalka & Weidong Cai & Jonathan Nicholas & Aarthi Padmanabhan & Vinod Menon, 2016. "Temporal Dynamics and Developmental Maturation of Salience, Default and Central-Executive Network Interactions Revealed by Variational Bayes Hidden Markov Modeling," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-29, December.
  • Handle: RePEc:plo:pcbi00:1005138
    DOI: 10.1371/journal.pcbi.1005138
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    Cited by:

    1. William Hedley Thompson & Craig Geoffrey Richter & Pontus Plavén-Sigray & Peter Fransson, 2018. "Simulations to benchmark time-varying connectivity methods for fMRI," PLOS Computational Biology, Public Library of Science, vol. 14(5), pages 1-23, May.

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