Sleep increases propagation speed of physiological brain pulsations

Abstract

During sleep, there is an increase in the brain cerebrospinal fluid (CSF) solute convection driven by physiological pulsations. Although the main drivers of CSF flow, namely cardiac, respiratory, and vasomotor pulsations, become more powerful during sleep, there is relatively little information regarding their effects on CSF flow velocity across human brain during sleep. Here, we used functional magnetic resonance encephalography (MREG) to measure non-invasively changes in brain water flow during to sleep by tracking the propagating ultrafast signal changes induced by physiological brain pulsations. We first undertook a phantom study confirming that dense optical flow analysis of MREG data accurately detects water flow velocity, and reflects the power of the physiological pulsations. We then applied the method to quantify CSF water flow velocity in brain of healthy volunteers during EEG-verified awake and sleep recordings of ultrafast MREG data. Sleep induced an increase in CSF flow speed, as demonstrated by elevated vasomotor and respiratory pulsation speeds, while the speed of cardiovascular impulse propagation remained unchanged. The speed increases match previous findings of respective pulsation power changes, and correlated with slow delta EEG power. The sleep-induced CSF flow speed increases occurred dynamically over both pulsation cycles, without the large effects on flow directions reported previously in several neurological conditions. In conclusion, sleep increases 3D water flow speed dynamically in human brain regions showing concomitant pulse power increases, supporting a porous media model of hydrodynamics in brain cortex.