Neurofluid coupling during sleep and wake states.

Cerebral hemodynamics Cerebrospinal fluid NREM sleep Neural activity Systemic physiology

Journal

Sleep medicine
ISSN: 1878-5506
Titre abrégé: Sleep Med
Pays: Netherlands
ID NLM: 100898759

Informations de publication

Date de publication:
10 2023
Historique:
received: 06 02 2023
revised: 17 07 2023
accepted: 22 07 2023
medline: 25 9 2023
pubmed: 4 8 2023
entrez: 3 8 2023
Statut: ppublish

Résumé

In clinical populations, the movement of cerebrospinal fluid (CSF) during sleep is a growing area of research with potential mechanistic connections in both neurodegenerative (e.g., Alzheimer's Disease) and neurodevelopmental disorders. However, we know relatively little about the processes that influence CSF movement. To inform clinical intervention targets this study assesses the coupling between (a) real-time CSF movement, (b) neuronal-driven movement, and (c) non-neuronal systemic physiology driven movement. This study included eight young, healthy volunteers, with concurrently acquired neurofluid dynamics using functional Magnetic Resonance Imaging (MRI), neural activity using Electroencephalography (EEG), and non-neuronal systemic physiology with peripheral functional Near-Infrared Spectroscopy (fNIRS). Neuronal and non-neuronal drivers were assessed temporally; wherein, EEG measured slow wave activity that preceded CSF movement was considered neuronally driven. Similarly, slow wave oscillations (assessed via fNIRS) that coupled with CSF movement were considered non-neuronal systemic physiology driven. Our results document neural contributions to CSF movement were only present during light NREM sleep but low-frequency non-neuronal oscillations were strongly coupled with CSF movement in all assessed states - awake, NREM-1, NREM-2. The clinical/research implications of these findings are two-fold. First, neuronal-driven oscillations contribute to CSF movement outside of deep sleep (NREM-3); therefore, interventions aimed at increasing CSF movement may yield meaningful increases with the promotion of NREM sleep more generally - a focus on NREM S3 may not be needed. Second, non-neuronal systemic oscillations contribute across wake and sleep stages; therefore, interventions may increase CSF movement by manipulating systemic physiology.

Sections du résumé

BACKGROUND
In clinical populations, the movement of cerebrospinal fluid (CSF) during sleep is a growing area of research with potential mechanistic connections in both neurodegenerative (e.g., Alzheimer's Disease) and neurodevelopmental disorders. However, we know relatively little about the processes that influence CSF movement. To inform clinical intervention targets this study assesses the coupling between (a) real-time CSF movement, (b) neuronal-driven movement, and (c) non-neuronal systemic physiology driven movement.
METHODS
This study included eight young, healthy volunteers, with concurrently acquired neurofluid dynamics using functional Magnetic Resonance Imaging (MRI), neural activity using Electroencephalography (EEG), and non-neuronal systemic physiology with peripheral functional Near-Infrared Spectroscopy (fNIRS). Neuronal and non-neuronal drivers were assessed temporally; wherein, EEG measured slow wave activity that preceded CSF movement was considered neuronally driven. Similarly, slow wave oscillations (assessed via fNIRS) that coupled with CSF movement were considered non-neuronal systemic physiology driven.
RESULTS AND CONCLUSIONS
Our results document neural contributions to CSF movement were only present during light NREM sleep but low-frequency non-neuronal oscillations were strongly coupled with CSF movement in all assessed states - awake, NREM-1, NREM-2. The clinical/research implications of these findings are two-fold. First, neuronal-driven oscillations contribute to CSF movement outside of deep sleep (NREM-3); therefore, interventions aimed at increasing CSF movement may yield meaningful increases with the promotion of NREM sleep more generally - a focus on NREM S3 may not be needed. Second, non-neuronal systemic oscillations contribute across wake and sleep stages; therefore, interventions may increase CSF movement by manipulating systemic physiology.

Identifiants

pubmed: 37536211
pii: S1389-9457(23)00264-2
doi: 10.1016/j.sleep.2023.07.021
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

44-53

Subventions

Organisme : NIA NIH HHS
ID : R21 AG068962
Pays : United States
Organisme : NIH HHS
ID : S10 OD012336
Pays : United States

Informations de copyright

Copyright © 2023 Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Auteurs

Vidhya Vijayakrishnan Nair (V)

Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, 47907, USA.

Brianna R Kish (BR)

Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, 47907, USA.

Pearlynne Lh Chong (PL)

Department of Human Development and Family Science, College of Health and Human Sciences, Purdue University, West Lafayette, IN, 47907, USA.

Ho-Ching Shawn Yang (HS)

Department of Radiology and Imaging Sciences, Indiana University School of Medicine, Indianapolis, IN, 46202, USA.

Yu-Chien Wu (YC)

Department of Radiology and Imaging Sciences, Indiana University School of Medicine, Indianapolis, IN, 46202, USA; Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, 46202, USA.

Yunjie Tong (Y)

Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, 47907, USA. Electronic address: tong61@purdue.edu.

A J Schwichtenberg (AJ)

Department of Human Development and Family Science, College of Health and Human Sciences, Purdue University, West Lafayette, IN, 47907, USA. Electronic address: ajschwichtenberg@purdue.edu.

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Classifications MeSH