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Brain network dynamics are hierarchically organized in time

  1. Mark W. Woolricha,b
  1. aOxford Centre for Human Brain Activity (OHBA), Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford, Oxford OX3 7JX, United Kingdom;
  2. bOxford Centre for Functional MRI of the Brain (FMRIB), Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom
  1. Edited by Marcus E. Raichle, Washington University in St. Louis, St. Louis, MO, and approved September 28, 2017 (received for review April 3, 2017)

Significance

We address the important question of the temporal organization of large-scale brain networks, finding that the spontaneous transitions between networks of interacting brain areas are predictable. More specifically, the network activity is highly organized into a hierarchy of two distinct metastates, such that transitions are more probable within, than between, metastates. One of these metastates represents higher order cognition, and the other represents the sensorimotor systems. Furthermore, the time spent in each metastate is subject-specific, is heritable, and relates to behavior. Although evidence of non–random-state transitions has been found at the microscale, this finding at the whole-brain level, together with its relation to behavior, has wide implications regarding the cognitive role of large-scale resting-state networks.

Abstract

The brain recruits neuronal populations in a temporally coordinated manner in task and at rest. However, the extent to which large-scale networks exhibit their own organized temporal dynamics is unclear. We use an approach designed to find repeating network patterns in whole-brain resting fMRI data, where networks are defined as graphs of interacting brain areas. We find that the transitions between networks are nonrandom, with certain networks more likely to occur after others. Further, this nonrandom sequencing is itself hierarchically organized, revealing two distinct sets of networks, or metastates, that the brain has a tendency to cycle within. One metastate is associated with sensory and motor regions, and the other involves areas related to higher order cognition. Moreover, we find that the proportion of time that a subject spends in each brain network and metastate is a consistent subject-specific measure, is heritable, and shows a significant relationship with cognitive traits.

Footnotes

  • ?1To whom correspondence should be addressed. Email: diego.vidaurre{at}ohba.ox.ac.uk.
  • Author contributions: D.V. and M.W.W. designed research; D.V., S.M.S., and M.W.W. performed research; D.V. and S.M.S. contributed new reagents/analytic tools; D.V. analyzed data; and D.V. and M.W.W. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • See Commentary on page 12641.

  • This article contains supporting information online at www.danielhellerman.com/lookup/suppl/doi:10.1073/pnas.1705120114/-/DCSupplemental.

This is an open access article distributed under the PNAS license.

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