Pressure Pulsatility Links Cardio-Respiratory and Brain Rhythmicity.

brain neurons electrical rhythmicity electroencephalogram (EEG) heartbeat- and breathing-induced intracranial pressure pulsatility millinewton pulsatile forces neural network entrainment pressure-activated Piezo channels proprioceptors touch receptors

Journal

Journal of integrative neuroscience
ISSN: 0219-6352
Titre abrégé: J Integr Neurosci
Pays: Singapore
ID NLM: 101156357

Informations de publication

Date de publication:
23 Oct 2023
Historique:
received: 06 04 2023
revised: 29 06 2023
accepted: 21 07 2023
medline: 5 1 2024
pubmed: 5 1 2024
entrez: 4 1 2024
Statut: ppublish

Résumé

This article presents evidence indicating that intracranial pressure (ICP) pulsatility, associated with the heartbeat and breathing, is not just a source of mechanical artefact in electrical recordings, but is "sensed" and plays a role in the brain's information processing. Patch-clamp recording of pressure-activated channels, and detection of Piezo2-protein channel expression in brain neurons, suggest that these channels provide neurons with an intrinsic resonance to ICP pulsatility, which acts to synchronize remote neural networks. Direct measurements in human patients indicate that heartbeat and breathing rhythms generate intracranial forces of tens of millinewtons, exceeding by orders of magnitude the localized forces shown by atomic force microscopy and optical tweezers to activate Piezo channels in isolated neocortical and hippocampal neurons. Additionally, many human touch and proprioceptors, which are also transduced by Piezo channels, show spiking that is phase-locked to heartbeat- and breathing-induced extracranial pressure pulsations. Finally, based on the observation that low-frequency oscillations modulate the phase and amplitude of high-frequency oscillations, body and brain oscillations are proposed to form a single hierarchical system in which the heartbeat is the basic frequency and scaling factor for all other oscillations. Together, these results support the idea that ICP pulsatility may be elemental in modulating the brain's electrical rhythmicity.

Identifiants

pubmed: 38176935
pii: S0219-6352(23)00605-8
doi: 10.31083/j.jin2206143
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

143

Informations de copyright

© 2023 The Author(s). Published by IMR Press.

Déclaration de conflit d'intérêts

The author declares no conflict of interest. Owen P. Hamill is serving as one of the Editorial Board members and Guest editor of this journal. We declare that Owen P. Hamill had no involvement in the peer review of this article and has no access to information regarding its peer review. Full responsibility for the editorial process for this article was delegated to Gernot Riedel.

Auteurs

Owen P Hamill (OP)

Department of Neurobiology, University of Texas Medical Branch, Galveston, TX 77555, USA.

Classifications MeSH