Cardiovascular and vasomotor pulsations in the brain and periphery during awake and NREM sleep in a multimodal fMRI study

Front Neurosci. 2024 Oct 8:18:1457732. doi: 10.3389/fnins.2024.1457732. eCollection 2024.

Abstract

Introduction: The cerebrospinal fluid dynamics in the human brain are driven by physiological pulsations, including cardiovascular pulses and very low-frequency (< 0.1 Hz) vasomotor waves. Ultrafast functional magnetic resonance imaging (fMRI) facilitates the simultaneous measurement of these signals from venous and arterial compartments independently with both classical venous blood oxygenation level dependent (BOLD) and faster arterial spin-phase contrast.

Methods: In this study, we compared the interaction of these two pulsations in awake and sleep using fMRI and peripheral fingertip photoplethysmography in both arterial and venous signals in 10 healthy subjects (5 female).

Results: Sleep increased the power of brain cardiovascular pulsations, decreased peripheral pulsation, and desynchronized them. However, vasomotor waves increase power and synchronicity in both brain and peripheral signals during sleep. Peculiarly, lag between brain and peripheral vasomotor signals reversed in sleep within the default mode network. Finally, sleep synchronized cerebral arterial vasomotor waves with venous BOLD waves within distinct parasagittal brain tissue.

Discussion: These changes in power and pulsation synchrony may reflect systemic sleep-related changes in vascular control between the periphery and brain vasculature, while the increased synchrony of arterial and venous compartments may reflect increased convection of regional neurofluids in parasagittal areas in sleep.

Keywords: cardiovascular pulsations; heart rate variability; multimodal imaging; sleep; ultrafast fMRI; vasomotor pulsations.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by Academy of Finland and Aivosäätiö TERVA grants 314497, 335720 (VKi), Academy of Finland Grant 275342, 338599 (VKi), JPND, Jane & Aatos Erkko Foundation grants 1 & 210043 (VKi), Uniogs/MRC Oulu doctoral program -grant (HH, JK), Pohjois-Suomen Terveydenhuollon tukisäätiö (HH, VKo), The Finnish Medical Foundation (MJ, VKi, JK), Finnish Neurological Foundation (VKi), KEVO grants from Oulu University hospital (VKi), Orion Research Foundation sr (MJ, JK), Medical Research Center (MRC)—Oulu (JK), Maire Taponen Foundation (JK), Finnish Brain Foundation sr (JK, VKi), Instrumentarium Science Foundation sr (MJ, JK), The University of Oulu Scholarship Foundation (JK), Emil Aaltonen foundation (HH, MJ), and The EU Joint Programme Neurodegenerative Disease Research 2022-120 (VKi).