Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice

Background & Aims: Mechanosensory information from the colon is conducted via lumbar splanchnic nerves (LSN) and sacral pelvic nerves (PN) to the spinal cord. The precise nature of mechanosensory information encoded by each pathway has remained elusive. Here, we characterize and directly compare the properties of mechanosensitive primary afferents from these 2 pathways. Methods: Using a novel in vitro mouse colon preparation, mechanosensitive primary afferents were recorded from the LSN and PN and distinguished based on their response to receptive field stimulation with 3 distinct mechanical stimuli: probing (70 mg-4 g), circular stretch (1-5 g), and mucosal stroking (10-1000 mg). Results: Five different classes of afferent were recorded from the LSN and PN. Three of these classes of afferent (serosal, muscular, and mucosal) were conserved between both pathways; however, their respective proportions, receptive field distributions, and response properties differed greatly. In general, these 3 classes of afferent recorded from the PN responded to lower stimulation intensities, displayed greater response magnitudes, and adapted less completely to mechanical stimulation compared with their LSN counterparts. In addition, the LSN and PN each contain a specialized class of afferent (mesenteric and muscular/mucosal), which is unique to their respective pathway. Conclusions: The splanchnic and pelvic pathways contain distinct populations of mechanosensitive afferents. These afferents are capable of detecting an array of mechanical stimuli and are individually tuned to detect the type, magnitude, and duration of the stimulus. This knowledge contributes to our understanding of the role that these 2 pathways play in conveying mechanical information from the colon.