Arterial segments (less than 250 micron o.d.) excised from canine ileum were mounted in a chamber that permitted arterial transmural pressure (TMP) to be altered and measured. Subsequently, the periarterial nerves were field stimulated with single pulses (0.1 msec, 70 V), and the resting membrane potential (Em) as well as the nerve-mediated alterations in smooth muscle Em were measured using intracellular microelectrodes at TMPs between 0 and 160 mm Hg. The resting Em was greatest at TMPs of 40 mm Hg (-54.7 +/- 2.6 mV) and depolarized as the TMP was increased, reaching a value of -44.8 +/- 3.1 mV at 160 mm Hg. At TMP greater than or equal to 60 mm Hg, a proportion of the preparations exhibited spontaneous electrical activity (SA) consisting of constant rhythmic oscillations in Em or action potentials (APs) or of trains of rhythmic APs that progressively decreased in amplitude, interrupted by periods of hyperpolarization. SA stopped when the TMP was lowered to 40 mm Hg and was reestablished when the TMP was reelevated to TMPs above 60 mm Hg. Nerve stimulation evoked excitatory junction potentials (ejps) or APs. At constant stimulus parameters, ejps of maximum amplitude having the greatest rate of potential rise and fall were produced at TMP of 100 mm Hg. At TMPs greater than 100 mm Hg or less than 100 mm Hg, the amplitude and the rate of rise and fall of the ejps decreased. Ejps formed in response to a constant single pulse stimulus (0.1 msec, 70 V) elicited APs only at TMPs greater than or equal to 60 mm Hg. Neither ejps nor APs were inhibited by alpha-receptor-blocking agents. These studies indicate that the TMP at which an artery is maintained plays an important role in determining the resting Em, the occurrence of spontaneous action potentials, and the alterations in Em associated with nerve stimulation.