Perturbation of intraparenchymal arterioles during K+-induced cortical spreading depression in cats

Abstract

During K+-induced cortical spreading depression (CSD) in the rat cerebral cortex, we previously observed repetitive wave-ring spread of oligemia/hypoperfusion followed by hyperemia/hyperperfusion. The oligemia/hypoperfusion occurred before upstream feeding arteriolar changes, suggesting that the capillary changes of the oligemia/hypoperfusion was of neuronal origin (Tomita M et al (2005) J CBF & M, in press). In this communication, we examined intraparenchymal arteriolar changes in the early phase of tissue oligemia. Six cats were used. Under -chloralose-urethan anesthesia, a skull window was opened in the parieto-temporal region. The dura was removed and the cerebral cortex was exposed. An optical fiber of 150 m in diameter was inserted into the brain tissue obliquely from 3 mm behind the skull window, so that the light source was positioned at the center of the ROI 1 mm below the pia. Intraparenchymal 20–40 m arterioles were both trans-illuminated in silhouette from below and epi-illuminated from above. They were monitored with a Canon video camera, and images were taken into a computer through a Scion frame grabber card (LG-3). When K+ was microinjected into the cortex at a site near the ROI, oligemic wave-ring spread was reproduced as reported previously (Tomita Y et al (2002) Neurosci Lett:322,157). We found that capillary flow in the oligemic area became very slow, with clustered RBCs passing through small vessels like ants marching. During oligemia/hypoperfusion, we noticed in all cases segmental constriction/dilatation of arteriole(s), forming a sausage-string shape (Fig. 1 and Fig. 2a) which had never been seen in other series of experiments. Chronological changes of arteriolar diameter were seen; for example, in 2 cases, a part of the arteriole suddenly contracted by 50% for about 1 to 1.5 sec and then dilated to 250% at 10 sec and remained dilated for more than 1 min (Fig. 2b). In the remaining cases, the time courses of constriction/dilatation of arteriole(s) were rather slow. In one case, the vascular dilatation occurred at a branching site and moved peripherally along the arteriole, like the movement of an egg swallowed by a snake. Despite these events, subtraction pictures revealed that the majority of the epi-cortical pial arteries did not change their diameter in this early phase. Based on these observations, we speculate that arterioles were perturbed by discrepant controls of high K+ concentration in the extracellular fluid, unknown feedback signals from oligemic tissue, and autonomic ganglionic regulation.