Organization of vagal afferents in pylorus: Mechanoreceptors arrayed for high sensitivity and fine spatial resolution?

Abstract

The pylorus is innervated by vagal mechanoreceptors that project to gastrointestinal smooth muscle, but the distributions and specializations of vagal endings in the sphincter have not been fully characterized. To evaluate their organization, the neural tracer dextran biotin was injected into the nodose ganglia of rats. Following tracer transport, animals were perfused, and their pylori and antra were prepared as whole mounts. Specimens were processed to permanently label the tracer, and subsets were counterstained with Cuprolinic blue or immunostained for c-Kit. Intramuscular arrays (IMAs) in the circular muscle comprised the principal vagal afferent innervation of the sphincter. These pyloric ring IMAs were densely distributed and evidenced a variety of structural specializations. Morphometric comparisons between the arbors innervating the pylorus and a corresponding sample of IMAs in the adjacent antral circular muscle highlighted that sphincter IMAs branched profusely, forming more than twice as many branches as did antral IMAs (means of 405 vs. 165, respectively), and condensed their numerous neurites into compact receptive fields (~48% of the area of antral IMAs) deep in the circular muscle (~6 μm above the submucosa). Separate arbors of IMAs in the sphincter interdigitated and overlapped to form a 360° band of mechanoreceptors encircling the pyloric canal. The annulus of vagal IMA arbors, putative stretch receptors tightly intercalated in the sphincter ring and situated near the lumen of the pyloric canal, creates an architecture with the potential to generate gut reflexes on the basis of pyloric sensory maps of high sensitivity and fine spatial resolution.

Vagal Intramuscular Arrays: The Specialized Mechanoreceptor Arbors That Innervate the Smooth Muscle Layers of the Stomach Examined in the Rat

“…Because gastric contents vary in consistency, they can vary in the resistance or tension that they generate, while the circumference of the antral lumen (i.e., stretch or length of the muscle sheets) does not necessarily covary. As discussed elsewhere (Powley et al, ), the same dissociation of the different forces can also occur in the stomach sphincter orifices as well.…”

“…As illustrated in Figure , gastric IMAs were concentrated in two functionally specialized areas; the arbors were massed in the proximal stomach, the compartment consisting of the forestomach and proximal corpus adjacent to the forestomach, and in the distal antrum. Although they are not the subject of the present experiment, IMAs are also densely distributed in the smooth muscle of the lower esophageal sphincter (Powley et al, ) and in the pylorus (Powley et al, ) as well. Thus, those gastric sites (i.e., the lower esophageal sphincter, proximal stomach, antrum, and pylorus) in which mechanical forces associated with ingestion and digestion regularly dissociate are the sites heavily innervated by IMAs (as well as IGLEs).…”

Individual sympathetic postganglionic neurons coinnervate myenteric ganglia and smooth muscle layers in the gastrointestinal tract of the rat

“…For each of the digitized sympathetic arbors, the following standardized morphometric measures captured with the Neurolucida software were analyzed for all neurites: total arbor length, parent axon length (using the Strahler Analysis algorithm), varicose neurite length, total number of terminal branches, highest branch order, and 2D terminal field size (using the Convex Hull algorithm [cf. Powley et al, , , ]).…”

Vagal Intramuscular Arrays: The Specialized Mechanoreceptor Arbors That Innervate the Smooth Muscle Layers of the Stomach Examined in the Rat

“…As illustrated in Figure 3, gastric IMAs were concentrated in two functionally specialized areas; the arbors were massed in the proximal stomach, the compartment consisting of the forestomach and proximal corpus adjacent to the forestomach, and in the distal antrum. Although they are not the subject of the present experiment, IMAs are also densely distributed in the smooth muscle of the lower esophageal sphincter and in the pylorus (Powley et al, 2014) as well. Thus, those gastric sites (i.e., the lower esophageal sphincter, proximal stomach, antrum, and pylorus) in which mechanical forces associated with ingestion and digestion regularly dissociate are the sites heavily innervated by IMAs (as well as IGLEs).…”

“…Because gastric contents vary in consistency, they can vary in the resistance or tension that they generate, while the circumference of the antral lumen (i.e., stretch or length of the muscle sheets) does not necessarily covary. As discussed elsewhere (Powley et al, 2014), the same dissociation of the different forces can also occur in the stomach sphincter orifices as well.Those regions of the stomach in which tension and stretch are frequently and conspicuously uncorrelated are the same regions in which vagal IMAs are densely distributed. As illustrated in Figure 3, gastric IMAs were concentrated in two functionally specialized areas; the arbors were massed in the proximal stomach, the compartment consisting of the forestomach and proximal corpus adjacent to the forestomach, and in the distal antrum.…”