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

Abstract

Abstract The glymphatic brain clearance mechanism convects brain cerebrospinal fluid driven by physiological pulsations such as cardiovascular and very low-frequency (VLF < 0.1 Hz) vasomotor waves. Presently, ultrafast functional magnetic resonance imaging (fMRI) facilitates the measurement of these signals from both venous and arterial compartments. 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 ten subjects (5 female). Sleep increased the power of brain cardiovascular pulsations, decreased peripheral pulsation and desynchronized them. Vasomotor waves, however, increase in both power and synchronicity in brain and peripheral signals during sleep. Peculiarly, vasomotor lag reversed in sleep within the default mode network vs. peripheral signal. Finally, sleep synchronized cerebral arterial vasomotion measured with cardiovascular hemodynamic envelope (CHe) vs. venous blood oxygenation level dependent (BOLD) signals in parasagittal brain tissue. These changes in power and pulsation synchrony may reflect differential changes in vascular control between the periphery and brain vasculature, while the increased synchrony of arterial and venous compartments may reflect increased convection of neurofluids in parasagittal areas in sleep. Statement of Significance This study shows that while sleep attenuated the cardiovascular synchrony and powers of pulsatility between the periphery and brain, it also increased brain tissue synchrony of venous and arterial vasomotor waves, specifically in the parasagittal regions. The study also shows that vasomotor waves increased in the human brain and the periphery during NREM sleep. Thus, sleep induces a whole-body vasomotor synchronization where the initiation of peripheral vasomotor waves is preceded within the default mode network area. Based on these results, we suggest that the synchronization of vasomotor waves may be a significant contributor to the enhancement of glymphatic fluid exchange in the human brain during sleep.