Endothelial and smooth muscle cell conduction in arterioles controlling blood flow

We performed intracellular recording with Lucifer yellow dye microinjection to investigate the cellular pathway(s) by which constriction and dilation are conducted along the wall of arterioles (diameter 47 ± 1 μm, n = 63) supplying blood flow to the cheek pouch of anesthetized hamsters. At rest, membrane potential ( E m ) of endothelial (−36 ± 1 mV) and smooth muscle (−35 ± 1 mV) cells was not different. Micropipette delivery of norepinephrine (NE) or phenylephrine (PE) produced smooth muscle cell depolarization (5–41 mV) and vasoconstriction (7–49 μm) at the site of release and along the arteriole with no effect on E m of endothelial cells. KCl produced conduction of depolarization and vasoconstriction with similar electrical kinetics in endothelial and smooth muscle cells. Acetylcholine triggered conduction of vasodilation (2–25 μm) and hyperpolarization (3–33 mV) along both cell layers; in smooth muscle, this change in E m was prolonged and followed by a transient depolarization. These cell-specific electrophysiological recordings uniquely illustrate that depolarization and constriction are initiated and conducted along smooth muscle, independent of the endothelium. Furthermore, conduction of vasodilation is explained by the spread of hyperpolarization along homologously coupled endothelial and smooth muscle cells, with distinctive responses between cell layers. The discontinuity between endothelium and smooth muscle indicates that these respective pathways are not electrically coupled during blood flow control.