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

Abstract

The fundamental roles that the stomach plays in ingestion and digestion notwithstanding, little morphological information is available on vagal intramuscular arrays (IMAs), the afferents that innervate gastric smooth muscle. To characterize IMAs better, rats were given injections of dextran biotin in the nodose ganglia, and, after tracer transport, stomach whole mounts were collected. Specimens were processed for avidin–biotin permanent labeling, and subsets of the whole mounts were immunohistochemically processed for c-Kit or stained with cuprolinic blue. IMAs (n = 184) were digitized for morphometry and mapping. Throughout the gastric muscle wall, IMAs possessed common phenotypic features. Each IMA was generated by a parent neurite arborizing extensively, forming an array of multiple (mean = 212) branches averaging 193 μm in length. These branches paralleled, and coursed in apposition with, bundles of muscle fibers and interstitial cells of Cajal. Individual arrays averaged 4.3 mm in length and innervated volumes of muscle sheet, presumptive receptive fields, averaging 0.1 mm3. Evaluated by region and by muscle sheet, IMAs displayed architectural adaptations to the different loci. A subset (32%) of circular muscle IMAs issued specialized polymorphic collaterals to myenteric ganglia, and a subset (41%) of antral longitudinal muscle IMAs formed specialized net endings associated with the serosal boundary. IMAs were concentrated in regional patterns that correlated with the unique biomechanical adaptations of the stomach, specifically proximal stomach reservoir functions and antral emptying operations. Overall, the structural adaptations and distributions of the IMAs were consonant with the hypothesized stretch receptor roles of the afferents.

Identifying unique subtypes of spinal afferent nerve endings within the urinary bladder of mice

“…These were characterized previously in the circular muscle of the colon (see Figure in Kyloh & Spencer, ). They are somewhat analogous in structure to the vagal intramuscular arrays identified in the stomach (Powley, Hudson, McAdams, Baronowsky, & Phillips, ). “Complex type” endings were identified by their single parent axon that was found to bifurcate numerous times close to its ending with other short axon terminals, but their key signifying feature was that each axon arbor lacked any preferential directionality with respect to neighboring axon terminals (an example is shown in Figure e in Spencer et al, ).…”

On the nature of high-amplitude propagating pressure waves in the human colon

“…Rectal bisacodyl evoked HAPWs that started in the proximal colon after~10 min. Hence, bisacodyl will activate extrinsic sensory nerves that communicate with the spinal cord neurons, which ultimately evoke vagal responses to initiate proximal HAPWs (39,54). A positive response to rectal bisacodyl confirms intactness of critical neural reflexes.…”

“…Rectal stimulation will become more important in the future since solidstate catheters and fiber-optic catheters do not have the ability to deliver a stimulus to the proximal colon, a stimulus that was routinely given using water-perfused catheters. Although both proximal and rectal bisacodyl can induce HAPWs that start in the proximal colon, a different mechanism of action may underlie it, as the proximal and distal colon is predominantly innervated by the vagus and sacral nerves, respectively (21) (13,39,54). Although proximal bisacodyl can evoke HAPWs, rectal bisacodyl may be more relevant for the testing of the rectal reflex to initiate HAPWs.…”

Differential Effects of Afferent and Efferent Vagus Nerve Stimulation on Gastric Motility Assessed with Magnetic Resonance Imaging

“…Here, we performed afferent VNS at the cervical level to mimic the vagovagal reflex occurring in the physiological state. The vagal afferents carry signals from stretch receptors 39,40 and chemoreceptors 41 to dorsal vagal complex in the brainstem, resulting in downstream, coordinated signals to different segments of the GI tract 2,42 . It has been widely demonstrated that fundic distention could induce reflex excitation on antral motility 12,14 and Lu 21 pyloric relaxation 43 .…”