Multilayer network switching rate predicts brain performance

Proc Natl Acad Sci U S A. 2018 Dec 26;115(52):13376-13381. doi: 10.1073/pnas.1814785115. Epub 2018 Dec 13.

Abstract

Large-scale brain dynamics are characterized by repeating spatiotemporal connectivity patterns that reflect a range of putative different brain states that underlie the dynamic repertoire of brain functions. The role of transition between brain networks is poorly understood, and whether switching between these states is important for behavior has been little studied. Our aim was to model switching between functional brain networks using multilayer network methods and test for associations between model parameters and behavioral measures. We calculated time-resolved fMRI connectivity in 1,003 healthy human adults from the Human Connectome Project. The time-resolved fMRI connectivity data were used to generate a spatiotemporal multilayer modularity model enabling us to quantify network switching, which we define as the rate at which each brain region transits between different networks. We found (i) an inverse relationship between network switching and connectivity dynamics, where the latter was defined in terms of time-resolved fMRI connections with variance in time that significantly exceeded phase-randomized surrogate data; (ii) brain connectivity was lower during intervals of network switching; (iii) brain areas with frequent network switching had greater temporal complexity; (iv) brain areas with high network switching were located in association cortices; and (v) using cross-validated elastic net regression, network switching predicted intersubject variation in working memory performance, planning/reasoning, and amount of sleep. Our findings shed light on the importance of brain dynamics predicting task performance and amount of sleep. The ability to switch between network configurations thus appears to be a fundamental feature of optimal brain function.

Keywords: brain performance; dynamic functional connectivity; fMRI; multilayer networks; switching.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Brain / physiology
  • Brain Mapping / methods
  • Cerebral Cortex / metabolism
  • Cerebral Cortex / physiology
  • Connectome / methods
  • Female
  • Healthy Volunteers
  • Humans
  • Magnetic Resonance Imaging / methods
  • Male
  • Memory, Short-Term
  • Nerve Net / metabolism*
  • Nerve Net / physiology*
  • Neural Networks, Computer
  • Psychomotor Performance
  • Task Performance and Analysis