Entrainment of Arteriole Vasomotor Fluctuations by Neural Activity Is a Basis of Blood-Oxygenation-Level-Dependent "Resting-State" Connectivity

Neuron. 2017 Nov 15;96(4):936-948.e3. doi: 10.1016/j.neuron.2017.10.012. Epub 2017 Oct 26.

Abstract

Resting-state signals in blood-oxygenation-level-dependent (BOLD) imaging are used to parcellate brain regions and define "functional connections" between regions. Yet a physiological link between fluctuations in blood oxygenation with those in neuronal signaling pathways is missing. We present evidence from studies on mouse cortex that modulation of vasomotion, i.e., intrinsic ultra-slow (0.1 Hz) fluctuations in arteriole diameter, provides this link. First, ultra-slow fluctuations in neuronal signaling, which occur as an envelope over γ-band activity, entrains vasomotion. Second, optogenetic manipulations confirm that entrainment is unidirectional. Third, co-fluctuations in the diameter of pairs of arterioles within the same hemisphere diminish to chance for separations >1.4 mm. Yet the diameters of arterioles in distant (>5 mm), mirrored transhemispheric sites strongly co-fluctuate; these correlations are diminished in acallosal mice. Fourth, fluctuations in arteriole diameter coherently drive fluctuations in blood oxygenation. Thus, entrainment of vasomotion links neuronal pathways to functional connections.

Keywords: Coupled oscillators; Functional magnetic resonant imaging; Hemodynamics; Intrinsic optical imaging; Optogenetics; Two-photon imaging.

MeSH terms

  • Animals
  • Arterioles / physiology*
  • Cerebral Cortex / blood supply
  • Cerebral Cortex / physiology
  • Corpus Callosum / physiology*
  • Gamma Rhythm / physiology*
  • Magnetic Resonance Imaging
  • Male
  • Mice
  • Mice, Transgenic
  • Neural Pathways / physiology
  • Neuroimaging
  • Oxygen / blood*
  • Rest / physiology
  • Vasodilation / physiology*

Substances

  • Oxygen