Spatial and Temporal Heterogeneities of Capillary Hemodynamics and Its Functional Coupling During Neural Activation

Abstract

The cerebral vascular system provides a means to meet the constant metabolic needs of neuronal activities in the brain. Within the cerebral capillary bed, the interactions of spatial and temporal hemodynamics play a deterministic role in oxygen diffusion, however, the progression of which remains unclear. Taking the advantages of high-spatiotemporal resolution of optical coherence tomography capillary velocimetry designed with the eigen-decomposition statistical analysis, we investigated intrinsic red blood cell (RBC) velocities and their spatiotemporal adjustment within the capillaries permeating mouse cerebral cortex during electrical stimulation of contralateral hind paw. We found that the mean capillary transit velocity (mCTV) is increased and its temporal fluctuation bandwidth (TFB) is broadened within hind-paw somatosensory cortex. In addition, the degree to which the mCTV is increased negatively correlates with resting state mCTV, and the degree to which the TFB is increased negatively correlates with both the resting state mCTV and the TFB. In order to confirm the changes are due to hemodynamic regulation, we performed angiographic analyses and found that the vessel density remains almost constant, suggesting the observed functional activation does not involve recruitment of reserved capillaries. To further differentiate the contributions of the mCTV and the TFB to the spatiotemporally coupled hemodynamics, changes in the mCTV and TBF of the capillary flow were modeled and investigated through a Monte Carlo simulation. The results suggest that neural activation evokes the spatial transit time homogenization within the capillary bed, which is regulated via both the heterogeneous acceleration of RBC flow and the heterogeneous increase of temporal RBC fluctuation, ensuring sufficient oxygenation during functional hyperemia.