Topographical arrangement of hypoglossal motoneurons: An HRP study in the cat

doi:10.1016/0304-3940(79)90024-7

Neuroscience Letters

Volume 13, Issue 2, July 1979, Pages 99-104

https://doi.org/10.1016/0304-3940(79)90024-7 Get rights and content

Abstract

Myotopical localization of hypoglossal motoneurons and representation of the main branches of the hypoglossal nerve within the hypoglossal nucleus were examined in the cat by the HRP method.

The hypoglossal nucleus is divided cytoarchitectonically into the ventromedial and dorsolateral divisions; the medial and lateral branches of the hypoglossal nerve are represented respectively in the ventromedial and dorsolateral divisions. The genioglossus motoneurons are located in the ventrolateral part of the ventromedial division, and the geniohyoid motoneurons are in the most ventral part of the ventromedial division. The hypoglossus and styloglossus motoneurons are located in the lateral and dorsolateral parts of the dorsolateral division.

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Cited by (78)

Activities of human genioglossus motor units
2011, Respiratory Physiology and Neurobiology
Upper airway muscles play an important role in regulating airway lumen and in increasing the ability of the pharynx to remain patent in the face of subatmospheric intraluminal pressures produced during inspiration. Due to the considerable technical challenges associated with recording from muscles of the upper airway, much of the experimental work conducted in human subjects has centered on recording respiratory-related activities of the extrinsic tongue protudor muscle, the genioglossus (GG). The GG is one of eight muscles that invest the human tongue (Abd-El-Malek, 1939). All eight muscles are innervated by the hypoglossal nerve (cranial nerve XII) the cell bodies of which are located in the hypoglossal motor nucleus (HMN) of the caudal medulla. Much of the earlier work on the respiratory-related activity of XII motoneurons was based on recordings obtained from single motor axons dissected from the whole XII nerve or from whole muscle GG EMG recordings. Detailed information regarding respiratory-related GG motor unit activities was lacking until as recently as 2006. This paper examines key findings that have emerged from the last decade of work conducted in human subjects. Wherever appropriate, these results are compared with results obtained from in vitro and in vivo studies conducted in non-human mammals. The review is written with the objective of facilitating some discussion and some new thoughts regarding future research directions. The material is framed around four topics: (a) motor unit type, (b) rate coding and recruitment, (c) motor unit activity patterns, and (d) a compartment based view of pharyngeal airway control.
Glutamatergic Kölliker-Fuse nucleus neurons innervate hypoglossal motoneurons whose axons form the medial (protruder) branch of the hypoglossal nerve in the rat
2011, Brain Research
Citation Excerpt :
However, little is known about the neuroanatomical substrates for network modulation of respiratory-related hypoglossal motor output. The extrinsic and intrinsic tongue muscles are innervated by motoneurons in the HGN, where motoneurons innervating the protruder and retractor tongue muscles have been revealed to exist in the ventral compartment and in the dorsal compartment of the nucleus, respectively by retrograde labeling studies (Krammer et al., 1979; O'Reilly and FitzGerald, 1990; Uemura et al., 1979). Efferent fibers from the HGN form the hypoglossal nerve (HGn), and those innervating the protruder (genioglossus and geniohyoid) and retractor (styloglossus and hyoglossus) tongue muscles form medial and lateral branches of the HGn, respectively (Krammer et al., 1979; Sawczuk and Mosier, 2001).
This study was performed to understand the anatomical substrates for Kölliker–Fuse nucleus (KFN) modulation of respiratory-related tongue movement. After application of cholera toxin B subunit (CTb) to the medial branch of the hypoglossal nerve (HGn) and injection of biotinylated dextran amine (BDA) into the KFN ipsilaterally, an overlapping distribution of BDA-labeled axon terminals and CTb-labeled neurons was found in the ventral compartment of the hypoglossal nucleus (HGN) ipsilateral to the application and injection sites. At the electron microscopic level, the BDA-labeled terminals made asymmetrical synaptic contacts predominantly with dendrites of the HGN neurons, some of which were labeled with CTb. Using retrograde tracing combined with in situ hybridization, we demonstrated that almost all the KFN neurons sending their axons to the HGN were positive for vesicular glutamate transporter (VGLUT) 2 mRNA but not glutamic acid decarboxylase 67 mRNA. Using a combination of anterograde and retrograde tracing techniques and immunohistochemistry for VGLUT2, we further demonstrated that the KFN axon terminals with VGLUT2 immunoreactivity established close contact with the HGN motoneurons whose axons constitute the medial branch of the HGn. The present results suggest that glutamatergic KFN fibers may exert excitatory influence upon the HGN motoneurons sending their axons to the medial branch of the HGn for the control of protruder tongue muscles contraction to maintain airway patency during respiration.
Retrograde labeling reveals extensive distribution of genioglossal motoneurons possessing 5-HT<inf>2A</inf> receptors throughout the hypoglossal nucleus of adult dogs
2007, Brain Research
Citation Excerpt :
Genioglossal motoneurons (GGMNs) comprise the largest subgroup of such inspiratory hypoglossal motoneurons (IHMNs) and their activity controls GG muscle tone that leads to protrusion of the tongue, which helps to maintain upper airway patency during inspiration. The location of GGMNs within the hypoglossal (XII) nucleus has been studied in the rat (Krammer et al., 1979; Uemura-Sumi et al., 1988; Altschuler et al., 1994; Aldes, 1995), cat (Uemura et al., 1979; Miyazaki et al., 1981), rabbit (Uemura-Sumi et al., 1988), frog (Matesz et al., 1999), monkey (Uemura-Sumi et al., 1981; Sokoloff and Deacon, 1992), and neonatal dog (Chibuzo and Cummings, 1982; Uemura-Sumi et al., 1988). However, the exact distribution and relative density of GGMNs within the XII nucleus of adult dogs has not been investigated but is of great interest to assess the findings from recent neurophysiological studies of IHMNs as in our decerebrate canine model (Tonkovic-Capin et al., 1998; Brandes et al., 2006).
Inspiratory hypoglossal motoneurons (IHMNs) innervate the muscles of the tongue and play an important role in maintaining upper airway patency. However, this may be reduced during sleep and by sedatives, potent analgesics, and volatile anesthetics. The genioglossal (GG) muscle is the main protruder and depressor muscle of the tongue and contributes to upper airway patency during inspiration. In vitro data suggest that serotonin (5-hydroxytryptamine, 5-HT), via the 5-HT_2A receptor (5-HT_2AR) subtype, plays a key role in controlling the excitability of IHMNs. The distribution of GG motoneurons (GGMNs) within the hypoglossal (XII) nucleus has not been studied in the adult dog. Further, it is uncertain whether the 5-HT_2AR is located on GGMNs in the adult dog. We therefore used the cholera toxin B (CTB) subunit as a retrograde tracer to map the location of GGMNs in combination with immunofluorescent labeling to determine the presence and colocalization of 5-HT_2AR within the XII nucleus in adult mongrel dogs. Injection of CTB into the GG muscle resulted in retrogradely labeled cells in a compact column throughout the XII nucleus, extending from 0.75 mm caudal to 3.45 mm rostral to the obex. Fluorescence immunohistochemistry revealed extensive 5-HT_2AR labeling on CTB-labeled GGMNs. Identification of the 5-HT_2AR on GGMNs in the XII nucleus of the adult dog supports in vitro data and suggests a physiological role for this receptor subtype in controlling the excitability of GGMNs, which contribute to the maintenance of upper airway patency.
Phenotype and contractile properties of mammalian tongue muscles innervated by the hypoglossal nerve
2005, Respiratory Physiology and Neurobiology
The XIIth cranial nerve plays a role in chewing, respiration, suckling, swallowing, and speech [Lowe, A.A., 1981. The neural regulation of tongue movements. Prog. Neurobiol. 15, 295–344.]. The muscles innervated by this nerve are functionally subdivided into three categories: those causing protrusion, retrusion, and changing the shape of the tongue. Myosin heavy chain (MHC) II isoform makes up the majority of the MHC phenotype with some variability among mammalian species and some evidence suggests between genders. In addition, there are regional differences in fiber type within some of these muscles that suggest functional compartmentalization. The transition from developmental MHC isoforms to their adult phenotype appears to vary not only from muscle to muscle but also from species to species. Motor units within this hypoglossal motor system can be categorized as predominantly fast fatigue resistant. Based on twitch contraction time and fatigue index, it appears that hypoglossal innervated muscles are more similar to fast-twitch muscles innervated by spinal nerves than, for example, extraocular muscles.
Genioglossal hypoglossal muscle motoneurons are contacted by nerve terminals containing delta opioid receptor but not mu opioid receptor-like immunoreactivity in the cat: A dual labeling electron microscopic study
2005, Brain Research
Citation Excerpt :
This is the second study to our knowledge that has provided ultrastructural proof of a neurotransmitter or a receptor [i.e., substance P (SP) and DOR] directly synapsing upon a hypoglossal motoneuron retrogradely labeled from the genioglossus muscle, the major protruder of the tongue. Previous light microscopic studies have investigated the distribution of hypoglossal motoneurons following injection of HRP into specific branches of the hypoglossal nerve [12] or into extrinsic tongue musculature [2,19–22]. These studies have found that there was a somatotopic organization to the nucleus.
This study has investigated (1) the distribution of delta opioid receptor (DOR) or mu opioid receptor (MOR) containing elements in the hypoglossal nucleus of the adult cat; and (2) the association of these processes with retrogradely labeled genioglossus muscle motoneurons. Cholera toxin B conjugated to horseradish peroxidase (CTB-HRP) was injected into the genioglossus muscle on the right side of four isoflurane-anesthetized cats. Forty-four to 52 h later, the animals were sacrificed. Motoneurons containing HRP were labeled with a histochemical reaction utilizing tetramethylbenzidine (TMB) as the chromogen. The tissues were then processed for immunocytochemistry, using an antiserum raised against DOR or MOR using diaminobenzidine (DAB) as the chromogen. At the light microscopic level, retrogradely labeled cells were observed primarily ipsilaterally in ventral and ventrolateral subdivisions of the hypoglossal nucleus. The majority of these labeled cells were observed immediately caudal to obex. DOR-like immunoreactive processes were apparent at the light microscopic level in the hypoglossal nucleus, but MOR-like immunoreactive processes were not. Both DOR and MOR-like immunoreactive processes were observed in other brainstem areas such as the spinal trigeminal nucleus. At the electron microscopic level, DOR-like immunoreactive nerve terminals formed synaptic contacts with retrogradely labeled genioglossus muscle motoneuronal dendrites and perikarya in the hypoglossal nucleus. Nineteen (19) percent of the DOR terminals contacted retrogradely labeled genioglossus muscle motoneurons. DOR-immunoreactive terminals also synapsed on unlabeled dendrites and somata. Few MOR-like immunoreactive terminals were found at the EM level in the hypoglossal nucleus, and none of these terminals contacted retrogradely labeled neuronal profiles from the GG muscle. These are the first ultrastructural studies demonstrating synaptic interactions between functionally identified hypoglossal motoneurons and DOR terminals, and that enkephalins most likely act presynaptically to modulate the release of other neurotransmitters that affect GG motoneuron activity. These studies demonstrate that hypoglossal motoneurons which innervate the major protruder muscle of the tongue, the genioglossus muscle, are modulated by terminals containing DOR, and that enkephalins acting on DOR but not MOR in the hypoglossal nucleus may play a role in the control of tongue protrusion.
Hypocretin (orexin) input to trigeminal and hypoglossal motoneurons in the cat: A double-labeling immunohistochemical study
2001, Brain Research
In trigeminal and hypoglossal motor nuclei of adult cats, hypocretin immunoreactive fiber varicosities were observed in apposition to retrogradely labeled motoneuron somata and dendrites. Among those lateral hypothalamus neurons that project to the hypoglossal nucleus some were determined to be hypocretin immunoreactive and were located amongst the single-labeled hypocretinergic neurons. These data suggest that hypocretin may play a role in the synaptic control of these motoneurons.

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Topographical arrangement of hypoglossal motoneurons: An HRP study in the cat

Abstract

Neurosci. Lett.

Sem. méd.

J. comp. Neurol.

The hypoglossal complex of vertebrates

J. comp. Neurol.

The Brain Stem of the Cat. A Cytoarchitectonic Atlas with Stereotaxic Coordinates

Quelques localisations dans le noyau de l'hypoglosse et du trijumeau chez l'homme

Folia Neuro-biol.

Beiträge zur mikroxkopischen Anatomie und zur lokalisationslehre einiger Gehirnnervenkerne (Nervus hypoglossus, vagus and facialis)

J. Psychol. Neurol.

Beiträge zur mikroxkopischen Anatomie und zur lokalisationslehre einiger Gehirnnervenkerne (Nervus hypoglossus, vagus and facialis)

J. Psychol. Neurol.

Beiträge zur mikroxkopischen Anatomie und zur lokalisationslehre einiger Gehirnnervenkerne (Nervus hypogloss, vagus and facialis)

J. Psychol. Neurol.

Experimentelle Untersuchungen über die Ursprünge des Nervus hypoglossus und seines absteigendes Astes

Jahrb. Psychiat. Neurol.

Topographical representation of peripheral branches of the facial nerve within the facial nucleus: a HRP study in the cat

Neurosci. Lett.