Characterization of mechanosensitive pelvic nerve afferent fibers innervating the colon of the rat

Abstract

1. Single-unit activity was recorded from S1 sacral dorsal root afferent fibers in the anesthetized rat. A total of 364 afferent fibers were identified by electrical stimulation of the pelvic nerve and subsequently tested for response to colorectal distension (CRD) and urinary bladder distension (UBD). Sixty-seven percent (n = 244) of the fibers were unmyelinated C-fibers and 33% (n = 120) were thinly myelinated A delta-fibers. 2. In three initial experiments, 35 fibers were identified by pelvic nerve stimulation and tested for response only to CRD; none of these fibers responded to CRD. In 20 subsequent experiments, 329 pelvic nerve afferent fibers were tested for response to CRD and UBD. Thirty-four percent (n = 112) of the 329 fibers were unresponsive to noxious CRD (80 mmHg) or to UBD (slow filling< or = 100 mmHg), 44% (n = 146) responded to UBD, 16% (n = 53) responded to CRD, and 6% (n = 18) responded to mechanical stimulation of the anal mucosa. 3. Of the total of 53 pelvic nerve afferent fibers that responded to CRD, 43 (81%) were C-fibers (mean: 1.5 m/s) and 10 (19%) were A delta-fibers (mean: 4.7 m/s). Fifteen of the CRD-sensitive fibers had no resting activity, whereas 38 fibers exhibited some resting activity (mean: 2.6 imp/s). 4. Reproducibility of responses to repeated CRD (80 mmHg, 30s, 10 trials at 4-min intervals) was tested in 17 fibers. In 16, responses to repeated distension were reproducible without evidence of facilitation or inhibition of subsequent responses. One fiber gave greater responses during the 9th and 10th trials. 5. Responses to graded CRD were studied in 44 fibers. All fibers exhibited monotonic, increasing stimulus-response functions < or = 80 mmHg of distension. Thresholds for response of the 44 fibers were determined after extrapolation of the least-squares linear-regression line to the ordinate and varied between 0 and 40 mmHg. Two populations of pelvic nerve afferent fibers in the colon were apparent: low threshold (LT) afferent fibers had a mean threshold of 2.9 mmHg (range: 0-10 mmHg; n = 34) and high threshold (HT) afferent fibers had a mean threshold of 32.6 mmHg (range: 28.0-40.0 mmHg; n = 10). 6. Chemosensitivity to bradykinin (BK) was tested in nine LT fibers. Seven fibers responded to BK (0.1 to 100 micrograms/kg ia) and two fibers did not respond up to 100 micrograms/kg of BK. Responses to BK tested in three fibers were dose dependent.(ABSTRACT TRUNCATED AT 400 WORDS)

Extrinsic primary afferent signalling in the gut

“…43 Like their vagal counterparts, these endings are rarely responsive to capsaicin, the activator of TrpV1 channels (transient receptor potential cation channel subfamily V member 1). Similar low-threshold mechanoreceptors have been recorded previously in pelvic pathways in the cat, 44 rat 45 and mouse, 46 where they were referred to as 'muscular' receptors.…”

In vitro recordings of afferent fibres with receptive fields in the serosa, muscle and mucosa of rat colon

“…Certainly, our data would indicate a nonnociceptive role for mucosal afferents due to their responsiveness to non-noxious stimuli, but we would challenge the use of the term 'mechanically insensitive' because mucosal stroking is a hitherto untested yet adequate mechanical stimulus and should therefore be included in future visceral afferent classifications. Mucosal afferents from the colon have not been reported previously, although those further down the gut in the rectal and anal canal have been demonstrated where somatic and visceral domains meet (Clifton et al 1976;Koley et al 1984;J anig & Koltzenburg, 1991;Sengupta & Gebhart, 1994). Colonic mucosal afferents have probably been encountered before, but their adequate stimulus not found.…”

Distinct subclassification of DRG neurons innervating the distal colon and glans penis/distal urethra based on the electrophysiological current signature

“…There are, of course, notable differences between our in vitro study and the aforementioned in vivo studies that focused on somatic (skin, muscle, joint) sensory cells, which prevent conclusions as to whether the function of our visceral and mucocutaneous cell types are restricted to nociception. Furthermore, given that in vitro and in vivo studies indicate that many colonic sensory afferents respond to low-threshold mechanical stimuli but are polymodal and therefore may respond to algogenic substances (e.g., Lynn and Blackshaw 1999, Raybould et al 1999, Sengupta and Gebhart 1994, and Su and Gebhart 1998, these cell types may not necessarily be classified as strictly "nociceptors" per se. Nonetheless, all of the cells recorded in this study do fit within the in vivo classification scheme of nociceptive-type cells, based on AP and AHP duration criteria.…”