The relationship between changes in intracolonic volume related to propulsive contractions and synaptic potentials recorded intracellularly in neurons in the inferior mesenteric ganglion (IMG) was investigated in vitro. Distension of the colon induced propulsive contractions (frequency, 2-5/min), which reduced intracolonic volume by 88%. Each propulsive contraction was sustained for 10-12 s, after which time the colon refilled. The sustained propulsive contractions were associated with a decrease in the amplitude and frequency of fast cholinergic excitatory postsynaptic potentials (EPSPs) and partial repolarization of the slow EPSP. The pressure-volume relationships of the colonic segments had two limbs: at distension pressures less than 15 cmH2O ("volume limb") the intracolonic volume was proportional to the distension pressure; greater than 15 cmH2O ("pressure limb") the intracolonic volume did not increase further. The changes in synaptic input were related to these pressure-volume relationships. In the volume limb, the frequency and amplitude of fast EPSPs were proportional to intracolonic volume and maximized with volume. In the pressure limb, there was a slow depolarization of the membrane that increased with greater distension pressures. Under isovolumic conditions, the changes in intraluminal pressure associated with colonic contractions were not associated with changes in excitatory synaptic input to IMG neurons. These experiments demonstrate that colonic mechanoreceptors to IMG neurons are sensitive to both intracolonic volume and pressure.