Endothelium and smooth muscle pathways for conduction along resistance microvessels

Blood flow control involves the interplay of signaling between endothelial cells and smooth muscle cells in vascular resistance networks. The conduction of electrical signals along the blood vessel wall through gap junctions is highly effective at coordinating vasodilatation (through hyperpolarization) and vasoconstriction (through depolarization) via electromechanical coupling in smooth muscle. In the hamster cheek pouch, the signals for vasodilatation and vasoconstriction conduct along arterioles. In the cheek pouch retractor muscle, the signal for vasodilatation conducts along arterioles and feed arteries, while constriction spreads via perivascular sympathetic nerves. To define the roles of endothelium and smooth muscle as conduction pathways in resistance micro-vessels of these tissues, intracellular recording and selective light-dye damage to endothelial cells or to smooth muscle cells were performed. In cheek pouch arterioles, homologous coupling within endothelium and within smooth muscle provides parallel pathways for electrical signaling, with the specificity of the stimulus determining which cell layer is effective. Thus, depolarization (e.g., to phenylephrine) is conducted along the smooth muscle layer, independently of the endothelium. In turn, hyperpolarization (e.g., to acetylcholine) conducts along the endothelium (releasing EDHF) and also along the smooth muscle. For feed arteries of the retractor muscle, endothelial cells conduct hyperpolarization; although the smooth muscle cells are ineffective as a conduction pathway, they are electrically coupled to endothelial cells. Such differences in the nature of cell-to-cell coupling between vascular beds may reflect corresponding variations in the functional expression of gap junctions. Nevertheless, across tissues, conduction along the endothelium coordinates relaxation of smooth muscle within and among resistance microvessels, whether through EDHF release or through direct electrical coupling.