Sleep‐stage‐dependent alterations in cerebral oxygen metabolism quantified by magnetic resonance

Author:

Xu Jing1,Wiemken Andrew2,Langham Michael C.1,Rao Hengyi3,Nabbout Marianne1,Caporale Alessandra S.145ORCID,Schwab Richard J.2,Detre John A.3,Wehrli Felix W.1ORCID

Affiliation:

1. Laboratory for Structural, Physiological, and Functional Imaging, Department of Radiology, Perelman School of Medicine University of Pennsylvania Philadelphia Pennsylvania USA

2. Division of Sleep Medicine, Department of Medicine, Perelman School of Medicine University of Pennsylvania Philadelphia Pennsylvania USA

3. Department of Neurology, Perelman School of Medicine University of Pennsylvania Philadelphia Pennsylvania USA

4. Department of Neurosciences, Imaging and Clinical Sciences ‘G. d'Annunzio University’ of Chieti‐Pescara Chieti Italy

5. Institute for Advanced Biomedical Technologies (ITAB) ‘G. d'Annunzio University’ of Chieti‐Pescara Chieti Italy

Abstract

AbstractA key function of sleep is to provide a regular period of reduced brain metabolism, which is critical for maintenance of healthy brain function. The purpose of this work was to quantify the sleep‐stage‐dependent changes in brain energetics in terms of cerebral metabolic rate of oxygen (CMRO2) as a function of sleep stage using quantitative magnetic resonance imaging (MRI) with concurrent electroencephalography (EEG) during sleep in the scanner. Twenty‐two young and older subjects with regular sleep hygiene and Pittsburgh Sleep Quality Index (PSQI) in the normal range were recruited for the study. Cerebral blood flow (CBF) and venous oxygen saturation (SvO2) were obtained simultaneously at 3 Tesla field strength and 2.7‐s temporal resolution during an 80‐min time series using OxFlow, an in‐house developed imaging sequence. The method yields whole‐brain CMRO2 in absolute physiologic units via Fick's Principle. Nineteen subjects yielded evaluable data free of subject motion artifacts. Among these subjects, 10 achieved slow‐wave (N3) sleep, 16 achieved N2 sleep, and 19 achieved N1 sleep while undergoing the MRI protocol during scanning. Mean CMRO2 was 98 ± 7(μmol min−1)/100 g awake, declining progressively toward deepest sleep stage: 94 ± 10.8 (N1), 91 ± 11.4 (N2), and 76 ± 9.0 μmol min−1/100 g (N3), with each level differing significantly from the wake state. The technology described is able to quantify cerebral oxygen metabolism in absolute physiologic units along with non‐REM sleep stage, indicating brain oxygen consumption to be closely associated with depth of sleep, with deeper sleep stages exhibiting progressively lower CMRO2 levels.

Funder

National Institutes of Health

National Institute of Biomedical Imaging and Bioengineering

National Center for Advancing Translational Sciences

Publisher

Wiley

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