Electrical activation of endothelium evokes vasodilation and hyperpolarization along hamster feed arteries.

Endothelial cells are considered electrically unexcitable. However, endothelium-dependent vasodilators (e.g., acetylcholine) often evoke hyperpolarization. We hypothesized that electrical stimulation of endothelial cells could evoke hyperpolarization and vasodilation. Feed artery segments (resting diameter: 63 +/- 1 microm; length 3-4 mm) of the hamster retractor muscle were isolated and pressurized to 75 mmHg, and focal stimulation was performed via microelectrodes positioned across one end of the vessel. Stimulation at 16 Hz (30-50 V, 1-ms pulses, 5 s) evoked constriction (-20 +/- 2 microm) that spread along the entire vessel via perivascular sympathetic nerves, as shown by inhibition with tetrodotoxin, omega-conotoxin, or phentolamine. In contrast, stimulation with direct current (30 V, 5 s) evoked vasodilation (16 +/- 2 microm) and hyperpolarization (11 +/- 1 mV) of endothelial and smooth muscle cells that conducted along the entire vessel. Conducted responses were insensitive to preceding treatments, atropine, or N(omega)-nitro-L-arginine, yet were abolished by endothelial cell damage (with air). Injection of negative current (</=1.6 nA) into a single endothelial cell reproduced vasodilator responses along the entire vessel. We conclude that, independent of ligand-receptor interactions, endothelial cell hyperpolarization evokes vasodilation that is readily conducted along the vessel wall. Moreover, electrical events originating within a single endothelial cell can drive the relaxation of smooth muscle cells throughout the entire vessel.