An autonomic mode of brain activity

Prog Neurobiol. 2023 Oct:229:102510. doi: 10.1016/j.pneurobio.2023.102510. Epub 2023 Jul 27.

Abstract

The relevance of interactions between autonomic and central nervous systems remains unclear for human brain function and health, particularly when both systems are challenged under sleep deprivation (SD). We measured brain activity (with fMRI), pulse and respiratory signals, and baseline brain amyloid beta burden (with PET) in healthy participants. We found that SD relative to rested wakefulness (RW) resulted in a significant increase in synchronized low frequency (LF, < 0.1 Hz) activity in an autonomically-related network (AN), including dorsal attention, visual, and sensorimotor regions, which we previously found to have consistent temporal coupling with LF pulse signal changes (regulated by sympathetic tone). SD resulted in a significant phase coherence between the LF component of the pulse signal and a medial network with peak effects in the midbrain reticular formation, and between LF component of the respiratory variations (regulated by respiratory motor output) and a cerebellar network. The LF power of AN during SD was significantly and independently correlated with pulse-medial network and respiratory-cerebellar network phase coherences (total adjusted R2 = 0.78). Higher LF power of AN during SD (but not RW) was associated with lower amyloid beta burden (Cohen's d = 0.8). In sum, SD triggered an autonomic mode of synchronized brain activity that was associated with distinct autonomic-central interactions. Findings highlight the direct relevance of global cortical synchronization to brain clearance mechanisms.

Keywords: Amyloid beta burden; Cortical synchronization; FMRI; Midbrain reticular formation; Sleep deprivation; Sympathetic nervous system.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Amyloid beta-Peptides*
  • Autonomic Nervous System / physiology
  • Brain / physiology
  • Heart Rate / physiology
  • Humans
  • Nervous System Physiological Phenomena*

Substances

  • Amyloid beta-Peptides