Individual sympathetic postganglionic neurons coinnervate myenteric ganglia and smooth muscle layers in the gastrointestinal tract of the rat. Issue 13 (24th February 2016)

• Record Type: Journal Article
• Authors: Walter, Gary C.; Phillips, Robert J.; McAdams, Jennifer L.; Powley, Terry L.
• Is Part Of: Journal of comparative neurology. Volume 524:Issue 13(2016)
• Page Start: 2577
• Page End: 2603
• Publication Date: 2016-02-24
• Subjects: autonomic nervous system -- celiac ganglion -- enteric nervous system -- muscularis externa -- superior mesenteric ganglion -- RRID:RGD_61109 -- RRID:AB_2307337 -- RRID:AB_2336819 -- RRID:nig‐0000‐10294 -- RRID:rid_000081 -- RRID:AB_572268 -- RRID:AB_2313713 -- RRID:AB_2313574 -- RRID:AB10566286 -- RRID:AB_10562715; Comparative neurobiology -- Periodicals; Neurology -- Periodicals; 616
• DOI: 10.1002/cne.23978
• Languages: English
• ISSNs: 0021-9967

Abstract

Abstract : A full description of the terminal architecture of sympathetic axons innervating the gastrointestinal (GI) tract has not been available. To label sympathetic fibers projecting to the gut muscle wall, dextran biotin was injected into the celiac and superior mesenteric ganglia (CSMG) of rats. Nine days postinjection, animals were euthanized and stomachs and small intestines were processed as whole mounts (submucosa and mucosa removed) to examine CSMG efferent terminals. Myenteric neurons were counterstained with Cuprolinic Blue; catecholaminergic axons were stained immunohistochemically for tyrosine hydroxylase. Essentially all dextran‐labeled axons (135 of 136 sampled) were tyrosine hydroxylase‐positive. Complete postganglionic arbors ( n = 154) in the muscle wall were digitized and analyzed morphometrically. Individual sympathetic axons formed complex arbors of varicose neurites within myenteric ganglia/primary plexus and, concomitantly, long rectilinear arrays of neurites within circular muscle/secondary plexus or longitudinal muscle/tertiary plexus. Very few CSMG neurons projected exclusively (i.e., ∼100% of an arbor's varicose branches) to myenteric plexus (∼2%) or smooth muscle (∼14%). With less stringent inclusion criteria (i.e., ≥85% of an axon's varicose branches), larger minorities of neurons projected predominantly to either myenteric plexus (∼13%) or smooth muscle (∼27%). The majority (i.e., ∼60%) of all individual CSMG postganglionics formed mixed, heterotypic arbors that coinnervated extensively (>15% of their varicose branches per target) both myenteric ganglia and smooth muscle. The fact that ∼87% of all sympathetics projected either extensively or even predominantly to smooth muscle, while simultaneously contacting myenteric plexus, is consistent with the view that these neurons control GI muscle directly, if not exclusively. J. Comp. Neurol. 524:2577–2603, 2016. © 2016 Wiley Periodicals, Inc. Abstract : Individual sympathetic postganglionic neurons, labeled by injections of the anterograde tracer dextran, projected directly to both the gastrointestinal smooth muscle sheets and the local myenteric ganglia throughout the stomach and small intestine. This widespread co‐innervation pattern suggests that sympathetic fibers may directly influence smooth muscle while contributing to myenteric‐plexus‐muscle coordination.