Dendritic architecture of nucleus ambiguus motoneurons projecting to the upper alimentary tract in the rat

Abstract

The motor innervation for palatal, pharyngeal, laryngeal, and esophageal muscles originates within the nucleus ambiguus. Although the viscerotopic organization of the upper alimentary tract in the nucleus ambiguus has been extensively studied, little information concerning the dendritic arborization of nucleus ambiguus motoneurons is available. The neural tracer cholera toxin-horseradish peroxidase, which is particularly effective at revealing dendrites of retrogradely labeled neurons, was used to determine the dendritic architecture and organization of nucleus ambiguus motoneurons. In 72 rats, cholera toxin-horseradish peroxidase in volumes of 1.0-18 microliters was directly applied under pressure to the musculature of various sites along the upper alimentary tract. Motoneurons innervating the soft palate, pharynx, cricothyroid muscle, and cervical esophagus were all found to have extensive dendrites that extended into the adjacent reticular formation with a distinct pattern for each muscle group. In contrast, the dendrites of motoneurons innervating the thoracic and subdiaphragmatic esophagus were confined to the compact formation of the nucleus ambiguus. Dendritic bundling within the confines of the nucleus ambiguus was prominent following injection of tracer into the soft palate, pharynx, and esophagus. The bundles were primarily oriented in a rostrocaudal direction. These data suggest that the extensive extranuclear dendritic arborization of motoneurons innervating the soft palate, pharynx, larynx, and cervical esophagus provide a wide ranging target for multiple central afferents that may be involved in the differential control of muscles that participate in multiple complex motor functions. The lack of extensive extranuclear dendrites of motoneurons innervating the distal esophagus suggest that they receive focused central afferents. The prominent bundling of dendrites within the nucleus ambiguus may provide for synchronization of motoneurons innervating a specific muscle and perhaps for synchronization of motoneurons innervating different muscles acting in sequence.

Ultrastructure and synaptology of the nucleus ambiguus in the rat: The semicompact and loose formations

“…The nucleus ambiguus comprises four major subdivisions that can be differentiated on the basis of their cytoarchitecture and efferent connections (Molhant, 1912;Lawn, 1966;Bieger and Hopkins, 1987;Hopkins, 1987;Altschuler et al, 1991;Kitamura et al, 1993). The subdivisions of the nucleus ambiguus, namely, a rostra1 esophagomotor compact formation, an intermediate pharyngomotor semicompact formation, a caudal laryngomotor loose formation, and a general visceromotor external formation (Bieger and Hopkins, 1987), have different roles in swallowing, respiration, vocalization, and autonomic function.…”

“…In comparison to esophagomotor neurons of the compact formation, the somata of motoneurons of the rat semicompact and loose formations are more diffusely distributed, spanning up to 2.5 mm in the ventrolateral medulla. In addition, the dendritic arbors of these cells extend beyond the borders of the nucleus, unlike those of the compact formation, indicating the possibility for the convergence of a wider range of inputs with a varied complement of synapses capable of a more finely modulated control (Altschuler et al, 1991). Here we describe the morphology and structural relationships of neurons situated within the rat semicompact and loose formations of the nucleus ambiguus that project to the pharynx and larynx, respectively.…”

Direct synaptic projections to esophageal motoneurons in the nucleus ambiguus from the nucleus of the solitary tract of the rat

“…The AmC is a well defined cell column situated in the rostral half of the nucleus ambiguus, and composed of mainly medium-sized neurons containing well-developed cell organelles, longitudinally orientated dendritic bundles, axon terminals, and small neurons having a small rim of cytoplasm (Bieger and Hopkins, 1987;Hopkins, 1995;Hayakawa et al, 1996). Ultrastructural retrograde tracing studies have also shown that there are four kinds of neurons in the AmC, that is, cervical esophageal motoneurons, subdiaphragmatic esophageal motoneurons, small neurons which are not projecting to the alimentary canal, and a few pharyngeal motoneurons in the rostral part of the AmC (Bieger and Hopkins, 1987;Altschuler et al, 1991;Hopkins, 1995;Hayakawa et al, 1996). The esophageal motoneurons are characterized by somato-somatic, somato-dendritic, or dendro-dendritic apposition by adherent junctions (Hopkins, 1995;Hayakawa et al, 1996).…”

“…Based on cytoarchitecture and innervation of target organs as revealed by retrograde tracing studies, it has been shown that the nucleus ambiguus is composed of compact, semicompact, loose, and external formations (Bieger and Hopkins, 1987;Altschuler et al, 1991). The esophageal motoneurons are located in the compact formation of the nucleus ambiguus (AmC; Lawn, 1966;Yoshida et al, 1981;Holstege et al, 1983;Fryscak et al, 1984;Bieger and Hopkins, 1987;Kitamura et al, 1993).…”

“…Using anterograde tracing with wheat germ agglutinin conjugated horseradish peroxidase (WGA-HRP), we attempted to clarify what kind of axon terminals the NTS neurons have within the AmC, and where these terminals contact different portions of the dendrite by means of electron microscopy. Also, in order to prove direct projections of the NTS to the esophageal motoneurons, the esophageal motoneurons were labeled retrogradely by cholera toxin subunit B conjugated horseradish peroxidase (CT-HRP), which is particularly effective for revealing retrogradely labeled neurons and dendrites (Wan et al, 1982;Shapiro and Miselis, 1985;Altschuler et al, 1991). We then labeled the NTS terminals anterogradely by WGA-HRP, and examined the ultrastructure of the labeled NTS terminals contacting the retrogradely labeled neurons in the AmC.…”