Hierarchical dynamics as a macroscopic organizing principle of the human brain

Proc Natl Acad Sci U S A. 2020 Aug 25;117(34):20890-20897. doi: 10.1073/pnas.2003383117. Epub 2020 Aug 12.

Abstract

Multimodal evidence suggests that brain regions accumulate information over timescales that vary according to anatomical hierarchy. Thus, these experimentally defined "temporal receptive windows" are longest in cortical regions that are distant from sensory input. Interestingly, spontaneous activity in these regions also plays out over relatively slow timescales (i.e., exhibits slower temporal autocorrelation decay). These findings raise the possibility that hierarchical timescales represent an intrinsic organizing principle of brain function. Here, using resting-state functional MRI, we show that the timescale of ongoing dynamics follows hierarchical spatial gradients throughout human cerebral cortex. These intrinsic timescale gradients give rise to systematic frequency differences among large-scale cortical networks and predict individual-specific features of functional connectivity. Whole-brain coverage permitted us to further investigate the large-scale organization of subcortical dynamics. We show that cortical timescale gradients are topographically mirrored in striatum, thalamus, and cerebellum. Finally, timescales in the hippocampus followed a posterior-to-anterior gradient, corresponding to the longitudinal axis of increasing representational scale. Thus, hierarchical dynamics emerge as a global organizing principle of mammalian brains.

Keywords: fMRI; frequency; functional connectivity; intrinsic; subcortex.

Publication types

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

MeSH terms

  • Adult
  • Brain / physiology*
  • Brain Mapping / methods*
  • Cerebral Cortex / physiology
  • Corpus Striatum / physiology
  • Databases, Factual
  • Female
  • Gray Matter / physiology
  • Hippocampus / physiology
  • Humans
  • Magnetic Resonance Imaging / methods
  • Male
  • Neural Pathways / physiology*
  • Rest / physiology
  • Time Factors