Active Dilation of Penetrating Arterioles Restores Red Blood Cell Flux to Penumbral Neocortex after Focal Stroke

Abstract

Pial arterioles actively change diameter to regulate blood flow to the cortex. However, it is unclear whether arteriole reactivity and its homeostatic role of conserving red blood cell (RBC) flux remains intact after a transient period of ischemia. To examine this issue, we measured vasodynamics in pial arteriole networks that overlie the stroke penumbra during transient middle cerebral artery occlusion in rat. In vivo two-photon laser-scanning microscopy was used to obtain direct and repeated measurements of RBC velocity and lumen diameter of individual arterioles, from which the flux of RBCs was calculated. We observed that occlusion altered surface arteriole flow patterns in a manner that ensured undisrupted flow to penetrating arterioles throughout the imaging field. Small-diameter arterioles (< 23 µm), which included 88% of all penetrating arterioles, exhibited robust vasodilation over a 90-min occlusion period. Critically, persistent vasodilation compensated for an incomplete recovery of RBC velocity during reperfusion to enable a complete restoration of postischemic RBC flux. Further, histologic examination of tissue hypoxia suggested re-oxygenation through all cortical layers of the penumbra. These findings indicate that selective reactivity of small pial arterioles is preserved in the stroke penumbra and acts to conserve RBC flux during reperfusion.