The rectum receives specialized extrinsic afferent innervation by stretch-sensitive, low threshold, slowly adapting mechanoreceptors, with transduction sites shown to correspond to rectal intraganglionic laminar endings (IGLEs). Rectal IGLEs are located in myenteric ganglia, surrounded by the longitudinal and circular smooth muscle layers; in this study we investigated the mechanical stimuli to which they respond. Mechanoreceptors had graded responses to highly focal transmural compression with von Frey hairs. They were activated when stretched circumferentially by imposed increases of both length and load. Under both conditions, firing typically occurred in bursts associated with phasic muscle contractions. However, many contractions did not evoke firing. Longitudinal stretch also evoked firing, again associated with contractile activity. Thus, mechanoreceptors did not show directional sensitivity. Two agonists that excited smooth muscle directly (0.1 microm [beta-Ala(8)]-neurokinin A (4-10) and 1 microm carbachol) activated rectal mechanoreceptors, but not in the presence of Ca(2)(+)-free solution or when preparations were kept entirely slack. We measured the dimensions, in both longitudinal and circumferential axes, of receptive fields during smooth muscle contractile activity, using video micrography. Contractile activity within the receptive field often differed significantly from the behaviour of the preparation as a whole, providing an explanation for many of the discrepancies between gross contractility and firing. Simultaneous contraction of both muscle layers within the receptive field was the strongest predictor of mechanoreceptor activation. Our results suggest that rectal mechanoreceptors do not act simply as tension receptors: rather they appear to detect mechanical deformation of myenteric ganglia - especially flattening - associated with stretch of the receptive field, or contractions of smooth muscle within the receptive field.