In the porcine coronary artery, endothelium-derived hyperpolarizing factor (EDHF) is responsible for 70% of the endothelium-dependent vasodilatation caused by bradykinin. This relaxation is associated with the simultaneous hyperpolarization of endothelial and smooth muscle cells. The synchronism of these two hyperpolarizations suggests that an electrical communication between the endothelial and smooth muscle cells may underly endothelium dependent hyperpolarizations of vascular smooth muscle, a phenomenon that has been attributed to EDHF. By contrast, in the porcine ciliary artery, EDHF is not implicated in the bradykinin-evoked endothelium-dependent relaxations. Experiments were designed to compare the behavior of arteries with and without EDHF-mediated responses. In a strip of ciliary artery incubated in vitro, dye coupling experiments demonstrated heterocellular coupling between the endothelial and smooth muscle cells. In addition, a 12 mV transient bradykinin-induced hyperpolarization was measured using microelectrodes in endothelial cells. Nevertheless, bradykinin evoked no hyperpolarization of smooth muscle cells in this artery, although a 4 mV hyperpolarization could be recorded in a few smooth muscle cells next to the endothelium. These observations are compatible with the concept that in arteries where the EDHF-component is absent, the current which causes the hyperpolarization of the endothelial cell is not strong enough to passively change the membrane potential of the coupled multiple layers of smooth muscle cells. As a corollary, a phenomenon other than passive electrical coupling alone must be responsible for the transmission of the hyperpolarization of the endothelial cells to the smooth muscle cells in aneries where endothelium-dependent hyperpolarizations occur.