Intracellular recordings were made from inferior mesenteric artery and vein and their primary and secondary branches. The major nerve trunks associated with the inferior mesenteric ganglion were stimulated with single shocks and repetitively. Excitatory junction potentials (EJPs) were recorded in arterial cells but not in veins. Stimulation of the postganglionic lumbar colonic nerves elicited the largest EJPs; stimulation of preganglionic lumbar splanchnic nerves or the interganglionic intermesenteric nerves elicited EJPs that were 40 and 44%, respectively, of the amplitude of the EJPs elicited with lumbar colonic nerve stimulation. In response to repetitive stimulation, the membranes of both artery and vein cells depolarized by an amount dependent on the frequency and duration of stimulation. At a given frequency of stimulation, the vein cells depolarized more rapidly and constricted sooner than the arterial cells. The depolarizations and the associated constrictions were attenuated by phentolamine (10(-6) M) or prazosin (10(-6) M). In 70% of arterial cells tested, repetitive nerve stimulation at 1-5 Hz resulted in a long-lasting hyperpolarization. At 2 Hz the hyperpolarizations averaged 2.0 +/- 0.4 mV. These hyperpolarizations were not blocked by either alpha- or beta-adrenergic antagonists. These studies demonstrate that the innervation of mesenteric arteries and veins can be activated by stimulating preganglionic, interganglionic, and postganglionic nerves and that there are fundamental differences between the electrical responses of adjacent arteries and veins to nerve stimulation.