This report describes the chemical and thermal sensitivity of mechanosensitive pelvic nerve afferent fibers innervating the colon of the rat. A total of 51 fibers in the S1 dorsal root, identified by electrical stimulation of the pelvic nerve, were studied. An approximately 7 cm length of descending colon was isolated in situ to permit intracolonic perfusion and distension with Krebs solution. Reproducibility of responses to repetitive colorectal distension (CRD, 40 mmHg, 30 s, every 4 min) was documented. All fibers gave monotonic, incrementing responses to graded CRD (5 to 60 mmHg). Increases (n = 6) or decreases (n = 6) in pH of the perfusate failed to produce any change in resting activity or responses to CRD. Infusion of bile salts increased the resting activity of 6/6 fibers in a concentration-dependent manner, but did not affect the magnitude of responses to CRD. After intracolonic instillation of an inflammatory soup (bradykinin 10(-5) M, PGE2 10(-5) M, serotonin 10(-5) M, histamine 10(-5) M and KCl 10(-3) M), 13/22 fibers exhibited sensitization of responses to CRD. Seventy-three percent of 45 fibers tested responded to intracolonic perfusion of heated Krebs solution. The estimated threshold for response was 45 degreesC and response magnitude increased with the temperature. A smaller proportion (30%) of 37 fibers tested responded to intracolonic perfusion of cold Krebs solution. The estimated threshold for response was 28 degreesC. Of 36 fibers tested, 8 were activated by both heat and cold; typically, fibers activated by heat did not respond to cold. In a sample of 26 fibers tested for response to all three modalities of stimulation, 11 responded to mechanical, chemical and thermal stimuli; the remaining 15 responded to mechanical and either chemical or thermal stimulation. Changes in intracolonic pressure in response to chemical and thermal stimuli were also evaluated. Inflammatory soup and bile salts did not change intracolonic pressure; heat and cold produced a modest decrease and increase in muscle tension, respectively. These results document that mechanosensitive pelvic nerve afferent fibers are also chemosensitive and/or thermosensitive, supporting the notion that visceral mechanoreceptors in general are likely polymodal in character.