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Sensory Regulation Of Swallowing And Airway Protection: A Role For The Internal Superior Laryngeal Nerve In Humans

S. Jafari, R. Prince, Daniel Y. Kim, D. Paydarfar
Published 2003 · Medicine

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During swallowing, the airway is protected from aspiration of ingested material by brief closure of the larynx and cessation of breathing. Mechanoreceptors innervated by the internal branch of the superior laryngeal nerve (ISLN) are activated by swallowing, and connect to central neurones that generate swallowing, laryngeal closure and respiratory rhythm. This study was designed to evaluate the hypothesis that the ISLN afferent signal is necessary for normal deglutition and airway protection in humans. In 21 healthy adults, we recorded submental electromyograms, videofluoroscopic images of the upper airway, oronasal airflow and respiratory inductance plethysmography. In six subjects we also recorded pressures in the hypopharynx and upper oesophagus. We analysed swallows that followed a brief infusion (4–5 ml) of liquid barium onto the tongue, or a sip (1–18 ml) from a cup. In 16 subjects, the ISLN was anaesthetised by transcutaneous injection of bupivacaine into the paraglottic compartment. Saline injections using the identical procedure were performed in six subjects. Endoscopy was used to evaluate upper airway anatomy, to confirm ISLN anaesthesia, and to visualise vocal cord movement and laryngeal closure. Comparisons of swallowing and breathing were made within subjects (anaesthetic or saline injection vs. control, i.e. no injection) and between subjects (anaesthetic injection vs. saline injection). In the non‐anaesthetised condition (saline injection, 174 swallows in six subjects; no injection, 522 swallows in 20 subjects), laryngeal penetration during swallowing was rare (1.4 %) and tracheal aspiration was never observed. During ISLN anaesthesia (16 subjects, 396 swallows), all subjects experienced effortful swallowing and an illusory globus sensation in the throat, and 15 subjects exhibited penetration of fluid into the larynx during swallowing. The incidence of laryngeal penetration in the anaesthetised condition was 43 % (P < 0.01, compared with either saline or no injection) and of these penetrations, 56 % led to tracheal aspiration (without adverse effects). We further analysed the swallow cycle to evaluate the mechanism(s) by which fluid entered the larynx. Laryngeal penetration was not caused by premature spillage of oral fluid into the hypopharynx, delayed clearance of fluid from the hypopharynx, or excessive hypopharyngeal pressure generated by swallowing. Furthermore, there was no impairment in the ability of swallowing to halt respiratory airflow during the period of pharyngeal bolus flow. Rather, our observations suggest that loss of airway protection was due to incomplete closure of the larynx during the pharyngeal phase of swallowing. In contrast to the insufficient closure during swallowing, laryngeal closure was robust during voluntary challenges with the Valsalva, Müller and cough manoeuvres under ISLN anaesthesia. We suggest that an afferent signal arising from the ISLN receptor field is necessary for normal deglutition, especially for providing feedback to central neural circuits that facilitate laryngeal closure during swallowing. The ISLN afferent signal is not essential for initiating and sequencing the swallow cycle, for co‐ordinating swallowing with breathing, or for closing the larynx during voluntary manoeuvres.
This paper references
10.1080/00031305.1991.10475767
A Unified Approach to Mixed Linear Models
R. Mclean (1991)
Laryngeal afferent control of swallowing: anaesthesia of the internal superior laryngeal nerve causes glottic dysfunction and aspiration in humans
S. Jafari (2001)
10.1093/BRAIN/81.3.364
CORTICOBULBAR CONNEXIONS TO THE PONS AND LOWER BRAIN-STEM IN MAN
H. G. Kuypers (1958)
Role of sensation in swallowing
RW Bastian (1999)
10.1016/0034-5687(85)90016-7
Laryngeal cold receptors.
G. Sant'ambrogio (1985)
10.3109/08990229109144748
Immediate expansion of receptive fields of neurons in area 3b of macaque monkeys after digit denervation.
M. Calford (1991)
10.3109/00016487409126336
Folding mechanism of the human larynx.
B. R. Fink (1974)
10.1016/0006-8993(79)90715-7
Inputs to the swallowing medullary neurons from the peripheral afferent fibers and the swallowing cortical area
A. Jean (1979)
10.1007/BF00234137
Mechanisms underlying recovery of eye-head coordination following bilateral labyrinthectomy in monkeys
J. Dichgans (2004)
10.1161/01.STR.30.4.744
Swallowing function after stroke: prognosis and prognostic factors at 6 months.
G. Mann (1999)
10.1097/00000542-195205000-00015
The Comparative Anatomy and Physiology of the Larynx
Robert Brazy (1952)
10.1016/S0006-8993(99)01151-8
Effects of functional disruption of lateral pericentral cerebral cortex on primate swallowing
N. Narita (1999)
10.1152/PHYSREV.2001.81.2.929
Brain stem control of swallowing: neuronal network and cellular mechanisms.
A. Jean (2001)
10.1152/AJPGI.1994.267.4.G644
Influence of mucosal receptors on deglutitive regulation of pharyngeal and upper esophageal sphincter function.
G. N. Ali (1994)
10.1111/j.1469-7793.1999.609ae.x
Perceptual distortions of the human body image produced by local anaesthesia, pain and cutaneous stimulation
S. Gandevia (1999)
10.1016/0034-5687(79)90047-1
Properties of inspiratory termination by superior laryngeal and vagal stimulation.
S. Iscoe (1979)
10.1152/AJPREGU.1986.250.4.R721
Resetting of mammalian respiratory rhythm: existence of a phase singularity.
D. Paydarfar (1986)
10.1016/0034-5687(83)90075-0
Laryngeal receptors responding to transmural pressure, airflow and local muscle activity.
G. Sant'ambrogio (1983)
10.1001/ARCHOTOL.1941.00660030355002
SPHINCTER ACTION OF THE LARYNX
J. Pressman (1941)
10.1152/AJPLEGACY.1928.84.1.36
A STUDY OF THE SENSORY AREAS ELICITING THE SWALLOWING REFLEX
W. T. Pommerenke (1928)
10.1016/0022-3999(94)00104-D
Globus pharyngis: development of a symptom assessment scale.
I. Deary (1995)
10.1097/00005537-199910000-00017
Recovery of Laryngeal Sensation After Superior Laryngeal Nerve Anastomosis
J. Blumin (1999)
10.1113/jphysiol.1991.sp018537
Afferent pathway(s) for pharyngeal dilator reflex to negative pressure in man: a study using upper airway anaesthesia.
R. Horner (1991)
10.1002/AJA.1000510206
Innervation of the larynx. I. Innervation of laryngeal muscles
F. Lemere (1932)
10.1098/rspl.1891.0043
II. On the mechanism of the closure of the larynx. A preliminary communication
T. Stuart (1892)
The respiratory function of the larynx: some observations on laryngeal innervation, preliminary report
JA Murtagh (1945)
Laryngeal phonatory
M Tanabe (1975)
10.1007/BF02233643
Studies on the normal deglutition complex
G. Vantrappen (2005)
10.1044/JSHR.3803.556
Effects of a sour bolus on oropharyngeal swallowing measures in patients with neurogenic dysphagia.
J. Logemann (1995)
Closure mechanisms of the laryngeal vestibule during swallowing
JA Logemann (1992)
10.1288/00005537-195310000-00003
Anatomical and physiological correlations on stimulating the human superior laryngeal nerve
J. Ogura (1953)
10.1002/(SICI)1097-0185(199812)252:4<646::AID-AR15>3.0.CO;2-E
Anatomy of the human internal superior laryngeal nerve
Ira Sanders (1998)
10.1016/0006-8993(72)90004-2
Reticular ascending activation of frontal cortical neurons in rabbits, with special reference to the regulation of deglutition.
T. Sumi (1972)
Deglutition
AJ Miller (1982)
10.1053/GAST.1997.V113.PM9352847
Impaired deglutitive airway protection: a videofluoroscopic analysis of severity and mechanism.
P. Kahrilas (1997)
10.1177/000348947708600603
New Insights into the Causes of Postoperative Aspiration following Conservation Surgery of the Larynx
P. Ward (1977)
Innervation of the larynx: III
F Lemere (1933)
10.1152/JAPPL.1995.79.5.1567
Superior laryngeal nerve blockade and inspiratory resistive load detection in normal subjects.
M. Fitzpatrick (1995)
10.1016/S0361-9230(99)00067-2
Effect of superior laryngeal nerve transection on pharyngeal muscle contraction timing and sequence of activity during eating and stimulation of the nucleus solitarius in dogs
A. V. Haagen (1999)
10.1097/00132586-196802000-00008
Local anesthesia for peroral endoscopy. Using superior laryngeal nerve block with topical application.
J. Gaskill (1966)
10.1152/JN.1956.19.1.44
An electromyographic analysis of reflex deglutition.
R. Doty (1956)
10.1152/JN.1964.27.3.464
SOME FUNCTIONAL CHARACTERISTICS OF MECHANORECEPTORS IN THE LARYNX OF THE CAT.
S. Sampson (1964)
10.1113/jphysiol.1992.sp019372
Responses of laryngeal receptors to intralaryngeal CO2 in the cat.
D. Bartlett (1992)
Localisation et activité des neurones deglutiteurs bulbairs
A Jean (1972)
10.1001/ARCHOTOL.1933.03580060445001
INNERVATION OF THE LARYNX: III. EXPERIMENTAL PARALYSIS OF THE LARYNGEAL NERVE
F. Lemere (1933)
10.1152/AJPGI.1992.262.2.G338
Closure mechanisms of laryngeal vestibule during swallow.
J. Logemann (1992)
10.1177/000348949210100204
Characteristics of Late Responses to Superior Laryngeal Nerve Stimulation in Humans
C. Ludlow (1992)
10.1016/0006-8993(69)90313-8
Some properties of cortically-evoked swallowing and chewing in rabbits.
T. Sumi (1969)
10.1136/jnnp.23.1.10
EFFECTS OF POSTERIOR ROOT SECTION ON THE ACTIVITY OF SOME MUSCLES IN MAN
P. Nathan (1960)
10.1177/000348940211100402
Swallowing and Sensation: Evaluation of Deglutition in the Anesthetized Larynx
L. Sulica (2002)
Corticobular connexions to the pons and lower brain-stem in man: an anatomical study.
H. Kuypers (1958)
[Localization and activity of medullary swallowing neurones].
A. Jean (1972)
10.1152/JAPPL.1995.79.6.2169
A simple and reliable method to calibrate respiratory magnetometers and Respitrace.
R. Banzett (1995)
10.1002/CA.980080202
Superior laryngeal nerve block: An anatomical study
M. Stockwell (1995)
10.1111/J.1748-1716.1963.TB02590.X
Reflex Responses and Recurrent Discharges Evoked by Stimulation of Laryngeal Nerves
A. Maåtensson (1963)
10.1177/000348947208100106
Mechanical and Physiological Properties of Reflex Laryngeal Closure
Y. Murakami (1972)
10.1016/0014-4886(74)90033-8
Anatomical and functional differentiation of superior laryngeal nerve fibers affecting swallowing and respiration.
A. Miller (1974)
10.1016/0034-5687(95)00050-X
Stimulus-response characteristics of CO2-induced air hunger in normal subjects.
R. Banzett (1996)
10.1097/00005537-199912000-00014
Role of Sensation in Swallowing Function
R. Bastian (1999)
10.1007/BF00363579
Neuronal mechanisms in swallowing
T. Sumi (2004)
10.1288/00005537-197403000-00006
Effects of surface anesthesia on deglutition in man
Ingemar MÅrnsson (1974)
An Experimental Investigation into the Functions of the Eighth Pair of Nerves, or the Glosso-Pharyngeal, Pneumogastric, and Spinal Accessory
J. Reid (1839)
[The innervation of the larynx].
A. Réthi (1962)
10.1001/ARCHOTOL.1976.00780120048004
Laryngeal reflexes in cat, dog, and man.
C. Sasaki (1976)
10.1016/0016-5085(90)91078-K
Coordination of deglutitive glottic closure with oropharyngeal swallowing.
R. Shaker (1990)
10.1016/0016-5085(95)90393-3
Dynamic magnetic resonance imaging of vocal cord closure during deglutition.
R. F. Flaherty (1995)
10.1113/jphysiol.1977.sp012065
Effects of related sensory inputs on motor performances in man studied through changes in perceived heaviness
S. Gandevia (1977)
Swallowing disorders in persons with cerebrovascular accident.
S. L. Veis (1985)
10.1097/00005537-199709000-00018
Laryngopharyngeal Sensory Testing With Modified Barium Swallow As Predictors of Aspiration Pneumonia After Stroke
J. Aviv (1997)
10.1259/0007-1285-25-296-406
The protection of the laryngeal airway during swallowing.
G. Ardran (1952)
10.1113/jphysiol.1995.sp020584
Respiratory phase resetting and airflow changes induced by swallowing in humans.
D. Paydarfar (1995)



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10.1007/s00455-020-10226-8
Correction to: Abnormalities of Aspiration and Swallowing Function in Survivors of Acute Respiratory Failure
S. Langmore (2021)
10.5535/arm.20171
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Ga Yang Shim (2021)
10.1101/2021.05.04.442535
Modelling of synaptic interactions between two brainstem half-centre oscillators that coordinate breathing and swallowing
P. Tolmachev (2021)
10.1007/s00455-020-10199-8
Abnormalities of Aspiration and Swallowing Function in Survivors of Acute Respiratory Failure
S. Langmore (2020)
10.2334/josnusd.19-0408
Evaluation of the association between orofacial pain and dysphagia.
T. Tsujimura (2020)
10.1007/978-1-0716-0655-1_9
Peripheral Nerve Regeneration in a Novel Rat Model of Dysphagia.
K. Sakai (2020)
10.1177/0003489419901145
Inter- and Intra-Rater Reliability of Laryngeal Sensation Testing with the Touch Method During Flexible Endoscopic Evaluations of Swallowing
James C Borders (2020)
10.1044/2019_AJSLP-19-00095
Oral and Oropharyngeal Sensory Function in Adults With Chronic Obstructive Pulmonary Disease.
Fernanda Borowsky da Rosa (2020)
10.1007/s00455-019-10087-w
Adaptations to Oral and Pharyngeal Swallowing Function Induced by Injury to the Mylohyoid Muscle
S. N. King (2020)
10.1038/s41598-020-71713-4
Machine learning analysis to automatically measure response time of pharyngeal swallowing reflex in videofluoroscopic swallowing study
J. M. Lee (2020)
10.1007/s00405-020-06507-5
European white paper: oropharyngeal dysphagia in head and neck cancer
L. Baijens (2020)
10.1002/lary.28642
The Internal Superior Laryngeal Nerve in Humans: Evidence for Pure Sensory Function
Laura F Santoso (2020)
10.1016/j.ijporl.2020.110518
Pathophysiology of aspiration in a unilateral SLN lesion model using quantitative analysis of VFSS.
Maya Stevens (2020)
10.1016/j.amjoto.2020.102712
Comparison of the efficacy of two different local anesthetics in inferior turbinate reduction.
Ozan Erol (2020)
10.3390/ijms21176214
Targeting Chemosensory Ion Channels in Peripheral Swallowing-Related Regions for the Management of Oropharyngeal Dysphagia
M. Z. Hossain (2020)
10.1007/s00455-020-10126-x
The Effect of Cranial Nerve Stimulation on Swallowing: A Systematic Review
M. Florie (2020)
10.1002/cre2.274
The pilot study examining the effects of swallowing position on lung volume fraction and the coordination between respiration and non‐nutritive swallowing reflex
Yamaguchi-Komeyama (2020)
10.1007/s00455-020-10100-7
Effects of Superior Laryngeal Nerve Lesion on Kinematics of Swallowing and Airway Protection in an Infant Pig Model
A. R. Lammers (2020)
10.3389/fnhum.2020.00112
Swallow Motor Pattern Is Modulated by Fixed or Stochastic Alterations in Afferent Feedback
S. N. King (2020)
10.1016/j.cell.2020.03.004
An Airway Protection Program Revealed by Sweeping Genetic Control of Vagal Afferents
S. Prescott (2020)
10.1007/978-1-0716-0655-1
Stem Cells and Tissue Repair: Methods and Protocols
Chrissa Kioussi (2020)
10.18297/etd/3342
Coordination of airway protective behaviors and swallow: effects of afferent feedback and sex.
Alyssa Huff (2019)
10.1016/J.TIFS.2019.02.045
A review of the approaches to predict the ease of swallowing and post-swallow residues
M. Marconati (2019)
10.1113/JP277895
Involvement of the epithelial sodium channel in initiation of mechanically evoked swallows in anaesthetized rats
T. Tsujimura (2019)
Dysphagia in solid malignancies outside the head, neck and upper gastrointestinal tract
Ciarán Kenny (2019)
10.3389/fneur.2019.01301
Specific Vagus Nerve Lesion Have Distinctive Physiologic Mechanisms of Dysphagia
F. Gould (2019)
10.15126/THESIS.00851680
In vitro models for the formulation of easy-to-swallow products.
M. Marconati (2019)
10.1007/s00455-019-09980-1
Relationship Between Laryngeal Sensation, Length of Intubation, and Aspiration in Patients with Acute Respiratory Failure
James C. Borders (2019)
10.1101/832147
Adaptations to Oral and Pharyngeal Swallowing Function Induced by Injury to the Mylohyoid Muscle
S. N. King (2019)
10.1002/hed.25588
Sensory dysphagia: A case series and proposed classification of an under recognized swallowing disorder
Laura F Santoso (2019)
10.1016/J.AFORL.2018.08.001
Les pharyngotomies latérales
O. Laccourreye (2019)
10.1159/000487037
Introducing a Virtual Lesion Model of Dysphagia Resulting from Pharyngeal Sensory Impairment
P. Muhle (2018)
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