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Neurotransmitters And Neuromodulators Involved In Laryngeal Innervation
Y. Hisa, Hitoshi Bamba, S. Koike, K. Shogaki, Nobuhisa Tadaki, T. Uno
Published 1999 · Medicine, Biology
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The distribution and role of neurotransmitters and neuromodulators in laryngeal innervation are reviewed, and our recent findings regarding the nitrergic innervation of the larynx are demonstrated for the better understanding of the complexity of the laryngeal innervation system. Noradrenergic innervation of the larynx was studied with fluorescence histochemistry and electron microscopy after application of 5-hydroxydopamine. These studies confirmed the existence of noradrenergic innervation for the submucosal glands and blood vessels, and the origin and course of noradrenergic nerve fibers contained in the laryngeal nerves and their destinations in the larynx. Cholinergic innervation of the larynx has not been clarified in detail. Many kinds of neuropeptides have been demonstrated to be involved in laryngeal innervation. Vasoactive intestinal polypeptide originating from intralaryngeal ganglionic neurons participates in laryngeal vasodilation and reduction of laryngeal seromucous secretion. Neuropeptide Y nerve fibers are few in the larynx, and most originate from the superior cervical ganglion. They are distributed around the large or medium-sized blood vessels, especially arteries. They are also associated with excretory structures. Substance P was the first neuropeptide found to be a sensory neurotransmitter in the laryngeal afferent system. It is also involved in regulation of laryngeal blood flow and secretion. Calcitonin gene—related peptide is associated with the sensory, autonomic, and motor innervation of the larynx. The majority of enkephalin nerve fibers are located close to excretory structures, although no information on the physiological significance of enkephalin is available. In addition to the above neuropeptides, the peptides histidine isoleucine, histidine methionine, and helospectin have been shown to exist in the larynx. The nitrergic innervation of the larynx has been recently studied with NADPH-diaphorase histochemistry and immunohistochemistry using antiserum against nitric oxide synthase. Nitric oxide originates from the neurons in the intralaryngeal ganglia and is believed to modulate blood flow and secretion of the larynx. It controls the laryngeal exocrine secretion in cooperation with intrinsic vasoactive intestinal polypeptide and/or extrinsic calcitonin gene—related peptide. Nitric oxide from the nodose ganglion may modulate nociception of the larynx. The existence of nitrergic neurons located in the intrinsic laryngeal muscles has been demonstrated. Many of them are bipolar or pseudounipolar, so they might be sensory in nature. The effect of injury of the recurrent laryngeal nerve on the induction of nitric oxide synthase in the laryngeal motoneurons is also discussed.
This paper references
Inhibition of nitric oxide synthase reduces motoneuron death due to spinal root avulsion
W. Wu (1993)
Regulatory peptides in the human larynx and recurrent nerves.
C. Hauser-Kronberger (1993)
Multiple co-existence of peptides and classical transmitters in peripheral autonomic and sensory neurons--functional and pharmacological implications.
J. M. Lundberg (1986)
NADPH-diaphorase and VIP are co-localized in neurons of gallbladder ganglia.
E. K. Talmage (1993)
NADPH-diaphorase staining in autonomic and somatic cranial ganglia of the rat.
R. Morris (1993)
Occurrence, distribution and ontogeny of CGRP immunoreactivity in the rat lower respiratory tract: Effect of capsaicin treatment and surgical denervations
A. Cadieux (1986)
Axotomy increases NADPH-diaphorase staining in rat vagal motor neurons
M. Gonzalez (1987)
Immunoreactive helospectin: Distribution and co-localization with VIP/PHM in the human nasal mucosa, soft palate, and larynx
C. Hauser-Kronberger (1992)
Expression of Nitric-Oxide Synthase (NOS) in Injured CNS Neurons as Shown by NADPH Diaphorase Histochemistry
W. Wu (1993)
Distribution of Met-enkephalyl-Arg-Gly-Leu in rat larynx: Partial coexistence with vasoactive intestinal polypeptide, peptide histidine isoleucine and neuropeptide Y
J. Krekel (1990)
The intramscular ganglia of the cat's tongue.
M. Fitzgerald (1969)
Effect of calcitonin gene-related peptide on contraction of striated muscle in the mouse
K. Takami (1985)
Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry
U. Scherer-Singler (1983)
Sensory Nerve Endings in the Mucosa of the Epiglottis—Morphologic Investigations with Silver Impregnation, Immunohistochemistry, and Electron Microscopy
T. Shin (1987)
Effect of calcitonin gene-related peptide on the cyclic AMP level of isolated mouse diaphragm.
K. Takami (1986)
Vascular effects of helodermin, helospectin I and helospectin II: a comparison with vasoactive intestinal peptide (VIP)
L. Grundemar (1990)
Immunohistochemical Study of Intralaryngeal Ganglia in the Cat
K. Tsuda (1992)
Distribution of Neuropeptide-Like Immunoreactive Nerve Fibers in the Canine Larynx
M. Kawasoe (1990)
Peptide-containing nerve fibers in human airways: distribution and coexistence pattern.
A. Luts (1993)
Ultrastructural and histochemical study of the neuromuscular junctions in the denervated intrinsic laryngeal muscle of the cat.
T. Yoshihara (1991)
Synapse formation by autonomic nerves in the previously denervated neuromuscular junctions of the feline intrinsic laryngeal muscles
M. Nomoto (1991)
NO news is good news.
E. Culotta (1992)
Nitrergic neurons in the canine intrinsic laryngeal muscle
Y. Hisa (1996)
Potent stimulation of glycoprotein secretion in canine trachea by substance P.
S. Coles (1984)
Neuronal NADPH diaphorase is a nitric oxide synthase.
B. Hope (1991)
Enkephalin-like immunoreactivity in ganglionic cells in the larynx and superior cervical ganglion of the rat
S. Domeij (1991)
Target-specific projections of intrinsic ganglionic neurons with different chemical codes in the canine larynx
S. Masuko (1991)
Precise Localization of VIP-, NPY-, and TH-immunoreactivities of cat laryngeal glands
Yasumasa Tanaka (1995)
Nitric oxide synthase immunoreactivity in the human ileocecal region
M. S. Faussone-Pellegrini (1994)
Distribution of SP- and CGRP-immunoreactivity in the cat's larynx.
Y. Tanaka (1993)
Neuropeptide Participation in Canine Laryngeal Sensory Innervation
Y. Hisa (1994)
The distribution and origin of axon terminals with NADPH diaphorase activity in the nucleus of the solitary tract of the rat
Y. Lü (1994)
Calcitonin gene‐related peptide in nucleus ambiguus motoneurons in rat: Viscerotopic organization
Bong Hee Lee (1992)
Nitric oxide synthase in VIP-containing vasodilator nerve fibres in the guinea-pig.
W. Kummer (1992)
NADPH-diaphorase activity as a marker for nitric oxide synthase in neurons of the guinea pig respiratory tract.
T. Shimosegawa (1994)
Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradrenergic neurons and effects of NPY on sympathetic function.
J. M. Lundberg (1982)
Neuromuscular junctions of the posterior cricoarytenoid muscle in the human adult, human fetus and cat. Histochemical and electron microscopic study.
T. Yoshihara (1984)
Ganglionic neurons in vagal and laryngeal nerves projecting to larynx, and their peptidergic features in the cat.
Y. Tanaka (1993)
Nitric oxide: first in a new class of neurotransmitter? Science 1992;257:494-6
SH Snyder (1992)
Peptide-containing neurons projecting to the vocal cords of the rat: retrograde tracing and immunocytochemistry.
A. Luts (1990)
Regulatory peptides and general neuroendocrine markers in human nasal mucosa, soft palate and larynx.
K. Albegger (1991)
CGRP-immunoreactive cells supplying laryngeal sensory nerve fibres in the cat's nodose ganglion.
Y. Tanaka (1993)
Nitric oxide synthase in motor neurons after axotomy.
W. Yu (1994)
Ultrastructural and fluorescence histochemical studies on the sympathetic innervation of the canine laryngeal glands.
Y. Hisa (1982)
Nitric oxide: first in a new class of neurotransmitters.
S. Snyder (1992)
Ganglion cells in the mammalian tongue.
F. W. Gairns (1952)
Histochemical localization of nitric oxide synthase in rat enteric nervous system
Y. Aimi (1993)
Nitric oxide as an endogenous modulator of cholinergic neurotransmission in guinea-pig airways.
M. Belvisi (1991)
Fluorescence histochemical studies on the noradrenergic innervation of the canine larynx.
Y. Hisa (1982)
Calcitonin gene-related peptide prevents disuse-induced sprouting of rat motor nerve terminals
T. Tsujimoto (1988)
Nitric oxide producing neurons in the monkey and human digestive system
R. De Giorgio (1994)
Calcitonin gene-related peptide-immunoreactive nerves in the tongue, epiglottis and pharynx of the rat: Occurrence, distribution and origin
G. Terenghi (1986)
Tyrosine hydroxylase-immunoreactive cells in the nodose ganglion for the canine larynx.
T. Uno (1996)
Nitrergic Innervation of the Rat Larynx Measured by Nitric Oxide Synthase Immunohistochemistry and Nadph-Diaphorase Histochemistry
Nobuhisa Tadaki (1996)
Nitric oxide synthase in guinea pig lower airway innervation
A. Fischer (1993)
Substance P nerve fibres in the canine larynx by PAP immunohistochemistry.
Y. Hisa (1985)
Ganglions and ganglionic neurons in the cat's larynx.
Y. Yoshida (1993)
Substance P Immunoreactive Nerve Fibers of the Canine Laryngeal Mucosa
T. Shin (1987)
Nitric oxide may act as a messenger between dorsal root ganglion neurones and their satellite cells
R. Morris (1992)
Implantation of PNS Graft Inhibits the Induction of Neuronal Nitric Oxide Synthase and Enhances the Survival of Spinal Motoneurons Following Root Avulsion
W. Wu (1994)
Parasympathetic postganglionic cells in the glossopharyngeal nerve trunk and their relationship to unmyelinated nerve fibers in the fungiform papillae of the frog
K. Inoue (1991)
Effects of neuropeptides and capsaicin on the canine tracheal vasculature in vivo
R. Salonen (1988)
Peripheral analgesia and activation of the nitric oxide-cyclic GMP pathway.
I. D. Durate (1990)
The autonomic innervation of the human vocal cord: Neuropeptides
J. Basterra (1989)
Innervation of the larynx. II. Ramus anastomoticus and ganglion cells of the superior laryngeal nerve
F. Lemere (1932)
Nitric oxide synthase in rat nasal mucosa; immunohistochemical and histochemical localization.
S. Lee (1995)
Occurrence and distribution of VIP nerves in the nasal mucosa and tracheobronchial wall.
R. Uddman (1978)
Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues.
T. Dawson (1991)
Nitrergic innervation of the rat esophagus: focus on motor endplates.
J. Woerl (1994)
Sensory neuropeptides and airway function.
J. Solway (1991)
Neuromuscular junctions of the posterior cricoarytenoid muscle in the cat.
T. Kanda (1983)
Is there a role for an endothelium-derived relaxing factor in nociception?
S. T. Meller (1990)
THE UNLABELED ANTIBODY ENZYME METHOD OF IMMUNOHISTOCHEMISTRY PREPARATION AND PROPERTIES OF SOLUBLE ANTIGEN-ANTIBODY COMPLEX (HORSERADISH PEROXIDASE-ANTIHORSERADISH PEROXIDASE) AND ITS USE IN IDENTIFICATION OF SPIROCHETES
L. Sternberger (1970)
Relationship of neuropeptides to nitrergic innervation of the canine laryngeal glands
Y. Hisa (1996)
Some anatomical and neurohistochemical observations on the chick tongue.
Bhargava Kn (1974)
Calcitonin gene-related peptide-like immunoreactive motoneurons innervating the canine inferior pharyngeal constrictor muscle.
Y. Hisa (1994)
Distributions of the calcitonin gene-related peptide and substance P in the monkey larynx.
K. Murano (1993)
Nitric oxide synthase in VIP-containing vasodilator nerve fibers in the guineapig
W Kummer (1992)
NADPHdiaphorase-positive nerve fibers associated with motor endplates in the rat esophagus: new evidence for co-innervation of striated muscle by enteric
WL Neuhuber (1994)
Calcitonin gene-related peptide regulates muscle acetylcholine receptor synthesis
H. New (1986)
On sensory innervation of larynx in dog.
H. Koizumi (1953)
This paper is referenced by
Laryngeal anatomy and physiology update
R. J. Andrews (1999)
Exploring the Relation between Glottal Closure and Plasma Substance P: A Study Protocol.
K. Tsunoda (2019)
Airway response of healthy individuals to affective picture series.
T. Ritz (2002)
Serotonin and substance P: Synergy or competition in the control of breathing
M. Szereda-Przestaszewska (2020)
The effects of vagal stimulation on laryngeal vascular resistance and intraluminal pressure in the dog.
N. Yelmen (2004)
Nonadrenergic innervation of the rat laryngeal vasculature
M. Lyon (2000)
Associations Between Autonomic Nervous System Function, Voice, and Dysphonia: A Systematic Review.
R. Cardoso (2019)
The effects of stress reactivity on extralaryngeal muscle tension in vocally normal participants as a function of personality
Maria Dietrich (2009)
Intrinsic Laryngeal Muscle Response to a Public Speech Preparation Stressor: Personality and Autonomic Predictors.
L. Helou (2020)
Induction of Nitric Oxide Synthase Activity in Nucleus Ambiguus Motoneurons after Injury to the Rat Recurrent Laryngeal Nerve
Hitoshi Bamba, Toshiyuki Uno, Shinobu Koike, Kazuh (2000)
Associations Between Teachers' Autonomic Dysfunction and Voice Complaints.
R. Cardoso (2020)
Airway Gland Structure and Function.
J. Widdicombe (2015)
Superior Laryngeal Nerve
T. Uno (2016)
Intrinsic laryngeal muscle activity in response to autonomic nervous system activation
L. Helou (2013)
Expression of nNOS in the human larynx
M. Șelaru (2015)
Medullary mediation of the laryngeal adductor reflex: A possible role in sudden infant death syndrome
X. Wang (2016)
Taste buds and nerve fibers in the rat larynx: an ultrastructural and immunohistochemical study.
K. Nishijima (2004)
Basic Knowledge of Vocal Fold Paralysis
E. Yumoto (2015)