Topographic inventories of vagal afferents in gastrointestinal muscle

Abstract

To inventory and characterize the two types of vagal afferents (both putative mechanoreceptors) in the muscle of the gastrointestinal tract, the authors injected wheat germ agglutinin-horseradish peroxidase into the nodose ganglia of rats that had received unilateral ventral rhizotomies to eliminate efferents. The gut, from the oral esophagus to the distal colon, was divided into wholemounts, processed with tetramethylbenzidine, and surveyed to establish normative topographic maps of afferents. Vagal intraganglionic laminar endings (IGLEs) were ubiquitous, with concentrations varying on a longitudinal gradient (higher rostrally). This overall gradient was punctuated by denser condensations of endings in the oral esophagus, gastric corpus, and distal ileum. In regional specializations, IGLEs were fused into conspicuous, dense networks in the laryngeal esophagus and the antrum. Intramuscular arrays (IMAs) had restricted distributions, including the walls of the stomach and the sphincters throughout the gut. In the forestomach, a singular concentration of orthogonally crossed IMAs was organized into a lattice or "fovea." IMAs displayed variations in morphology, with one specialization consisting of short, terminal processes associated with sphincters and a more widespread form consisting of long, rectilinear processes in the forestomach, along the greater curvature, and in limited intestinal regions. On the basis of their topographic patterns and structural specializations, the two putative mechanoreceptors may have different functions: IGLEs appear situated to integrate intramural tension, and perhaps myenteric neuronal activity, into rhythmical, propagated motor programs, such as swallowing, peristalsis, and emptying. IMAs are distributed strategically and appear to satisfy structural requirements for stretch receptors tuned to tonic or more aperiodic events that may affect central nervous system processing as well as local gastrointestinal coordination.