Sensory Vagal Nature and Anatomical Access Paths to Esophagus Laminar Nerve Endings in Myenteric Ganglia. Determination by Surgical Degeneration Methods

Rodrigo, José; Felipe, J. De; Robles-Chillida, E.M.; Antón, J.A. Pérez; Mayo, Isabel; Gomez, A Ferreira

doi:10.1159/000145496

Cited by 71 publications

(62 citation statements)

References 12 publications

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“…In addition to IMAs, IGLEs are mechanoreceptors associated with the myenteric ganglia of the cat esophagus (34). IGLEs are not physically associated with ICC (20,29), and, in W/W v mutant mice lacking ICC-IM, IGLEs were not affected (21).…”

Section: Discussionmentioning

confidence: 99%

“…It is likely that more than one structurally and functionally distinct type of mechanoreceptor exists within the esophagus (4,5,8). As early as 1929, intraganglionic laminar nerve endings (IGLE) were considered candidates for esophageal stretch receptors (34). In an elegant study by Berthoud and Powley (4), intramuscular vagal afferents were shown to be positioned and structured as likely candidates for the gastric stretch receptor.…”

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Survival dependency of intramuscular ICC on vagal afferent nerves in the cat esophagus

Huizinga¹,

Reed²,

Berezin³

et al. 2008

American Journal of Physiology-Regulatory, Integrative and Comp

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cells of Cajal (ICC) have been proposed as stretch receptors for vagal afferent nerves in the stomach based on immunohistochemical studies. The aim of the present study was to use electron microscopy and the anterograde degeneration technique to investigate ultrastructural features and survival dependency of ICC associated with vagal afferent innervation of the cat esophagus. This is the first report on the ultrastructural characteristics of ICC in the cat esophagus. Intramuscular ICC (ICC-IM) were identified throughout the musculature, whereas ICC in the myenteric plexus were rare. ICC-IM were particularly numerous in septa aligned with smooth muscle bundles. They were in synapse-like contact with nerve varicosities and in gap junction contact with smooth muscle cells. Smooth muscle cells also made contact with ICC through peg and socket junctions. Precision damage through small-volume injection of saline in the center of the nodose ganglion from the lateral side, known to selectively affect sensory nerves, was followed within 24 h by degeneration of a subset of nerve varicosities associated with ICC-IM, as well as degeneration of the associated ICC-IM. Smooth muscle cells were not affected. Nerves of Auerbachs plexus and associated ICC were not affected. In summary, ICC-IM aligning the esophageal muscle bundles form specialized synapse-like contacts with vagal afferent nerves as well as gap junction and peg-and-socket contacts with smooth muscle cells. This is consistent with a role of ICC-IM as stretch receptors associated with vagal afferent nerves; the ICC-vagal nerve interaction appears essential for the survival of the ICC. interstitial cells of Cajal; esophagus; stretch receptor; vagus; afferent innervation; intramuscular interstitial cells of Cajal FOR NORMAL ESOPHAGEAL function, the vagus nerves provide the major sensory and motor innervation to both striated and smooth muscle portions of the esophagus. Sensory pathways from the esophagus have been studied both electrophysiologically (40, 41) and by nerve tracing techniques (4,11,28). However, the precise location and structure of the sensory receptor(s) involved in control of esophageal motor function remain controversial. It is likely that more than one structurally and functionally distinct type of mechanoreceptor exists within the esophagus (4, 5, 8). As early as 1929, intraganglionic laminar nerve endings (IGLE) were considered candidates for esophageal stretch receptors (34). In an elegant study by Berthoud and Powley (4), intramuscular vagal afferents were shown to be positioned and structured as likely candidates for the gastric stretch receptor. Intramuscular arrays (IMA) enter circular or longitudinal muscle layers, run parallel to respective muscle fibers, and bifurcate to create an array of parallel terminal elements in stomach and sphincters (28). In the stomach, these terminal elements consist of interconnected parallel axonal telodendria that are arrayed in close proximity to one another and that form appositions with interstitial cells ...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Survival dependency of intramuscular ICC on vagal afferent nerves in the cat esophagus

Huizinga¹,

Reed²,

Berezin³

et al. 2008

American Journal of Physiology-Regulatory, Integrative and Comp

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“…They present as profuse leafy structures covering myenteric ganglia from the esophagus to the colon. Neurectomy experiments (Rodrigo et al 1982) and anterograde wheat germ agglutinin-horseradish peroxidase (WGA-HRP) tracing from the nodose ganglion (Neuhuber 1987) have identified their vagal afferent nature. Morphological findings of an intimate relationship of IGLEs to connective tissue layers enveloping myenteric ganglia in the rat esophagus (Neuhuber 1987;Neuhuber and Clerc 1990) and electrophysiological studies in the guinea pig indicated that IGLEs function as mechanotransduction sites of vagal tension receptors both in the esophagus (Zagorodnyuk and Brookes 2000;Zagorodnyuk et al 2003) and stomach (Zagorodnyuk et al 2001).…”

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confidence: 99%

Number and Distribution of Intraganglionic Laminar Endings in the Mouse Esophagus as Demonstrated with Two Different Immunohistochemical Markers

Raab

Neuhuber

2005

J Histochem Cytochem.

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S U M M A R YIntraganglionic laminar endings (IGLEs) represent the only vagal mechanosensory terminals in the tunica muscularis of the esophagus. Two specific markers for IGLEs were recently described in mouse: the purinergic P2 ϫ 2 receptor and the vesicular glutamate transporter 2 (VGLUT2). This study aimed at comparing both markers with respect to their suitability for quantitative analysis. We counted IGLEs immunostained for VGLUT2 and P2 ϫ 2 , respectively, and mapped their distribution in esophageal wholemounts of C57Bl/6 mice. Numbers and distribution of IGLEs were compared with those of myenteric ganglia as demonstrated by cuprolinic blue histochemistry. Whereas the distribution of VGLUT2-immunopositive IGLEs closely matched that of myenteric ganglia, P2 ϫ 2 -immunopositive IGLEs were rarely found in upper and middle esophagus but increasingly in its lower parts. P2 ϫ 2 stained only half the number of IGLEs found with VGLUT2 immunostaining. We also investigated the correlation between anterograde tracing and immunohistochemistry for identifying IGLEs. Confocal microscopy revealed colocalization of all three markers in ‫ف‬ 50% of IGLEs. The remaining IGLEs showed only tracer and VGLUT2 labeling but no P2 ϫ 2 immunoreactivity. Thus, VGLUT2 and P2 ϫ 2 represent two specific markers for qualitative demonstration of esophageal IGLEs. However, VGLUT2 may be superior to P2 ϫ 2 as a quantitative marker for IGLEs in the esophagus of C57Bl/6 mice.

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“…Quantification of IGLEs. Criteria for IGLE identification were as determined previously: an IGLE must consist of (1) a laminar aggregate of (2) fine terminal puncta (3) within the neuropil of a myenteric ganglion, and (4) must cover all or part of the myenteric ganglion (Rodrigo et al, 1975(Rodrigo et al, , 1982Neuhuber, 1987;. Counting of IGLEs was conducted at 100ϫ magnification and verified at 200ϫ when necessary.…”

Section: Anterograde Labeling Of Vagal Gi Afferentsmentioning

confidence: 99%

“…Among vagal GI afferents, intraganglionic laminar endings (IGLEs) are the predominant vagal mechanoreceptor innervating GI smooth muscle (SM) and are concentrated in the region of the upper GI tract in which most food collects during consumption of a meal Wang and Powley, 2000). They consist of plates of densely packed terminal puncta that innervate myenteric ganglia and are activated by muscle wall tension or stretch and possibly by satiation hormones, such as CCK (Rodrigo et al, 1982;Schwartz and Moran, 1994;Zagorodnyuk et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

Reduced Intestinal Brain-Derived Neurotrophic Factor Increases Vagal Sensory Innervation of the Intestine and Enhances Satiation

Biddinger

Fox

2014

Journal of Neuroscience

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Sensory Vagal Nature and Anatomical Access Paths to Esophagus Laminar Nerve Endings in Myenteric Ganglia. Determination by Surgical Degeneration Methods

Cited by 71 publications

References 12 publications

Survival dependency of intramuscular ICC on vagal afferent nerves in the cat esophagus

Survival dependency of intramuscular ICC on vagal afferent nerves in the cat esophagus

Number and Distribution of Intraganglionic Laminar Endings in the Mouse Esophagus as Demonstrated with Two Different Immunohistochemical Markers

Reduced Intestinal Brain-Derived Neurotrophic Factor Increases Vagal Sensory Innervation of the Intestine and Enhances Satiation

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