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Movement Of The Tongue During Normal Breathing In Awake Healthy Humans

S. Cheng, J. Butler, S. Gandevia, L. Bilston
Published 2008 · Biology, Medicine

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Electromyographic (EMG) activity of the airway muscles suggest that genioglossus is the primary upper airway dilator muscle. However, EMG data do not necessarily translate into tissue motion and most imaging modalities are limited to assessment of the surfaces of the upper airway. In this study, we hypothesized that genioglossus moves rhythmically during the respiratory cycle and that the motion within is inhomogeneous. A ‘tagged’ magnetic resonance imaging technique was used to characterize respiratory‐related tissue motions around the human upper airway in quiet breathing. Motion of airway tissues at different segments of the eupnoeic respiratory cycle was imaged in six adult subjects by triggering the scanner at the end of inspiration. Displacements of the ‘tags’ were analysed using the harmonic phase method (HARP). Respiratory timing was monitored by a band around the upper abdomen. The genioglossus moved during the respiratory cycle. During expiration, the genioglossus moved posteriorly and during inspiration, it moved anteriorly. The degree of motion varied between subjects. The maximal anteroposterior movement of a point tracked on the genioglossus was 1.02 ± 0.54 mm (mean ±s.d.). The genioglossus moved over the geniohyoid muscle, with minimal movement in other muscles surrounding the airway at the level of the soft palate. Local deformation of the tongue was analysed using two‐dimensional strain maps. Across the respiratory cycle, positive strains within genioglossus reached peaks of 17.5 ± 9.3% and negative strains reached peaks of −16.3 ± 9.3% relative to end inspiration. The patterns of strains were consistent with elongation and compression within a constant volume structure. Hence, these data suggest that even during respiration, the tongue behaves as a muscular hydrostat.
This paper references
10.1164/RCCM.200411-1550OC
PO2-dependent changes in intrinsic and extrinsic tongue muscle activities in the rat.
E. F. Bailey (2005)
10.1159/000144377
Review of the evolution and phylogeny of the mammalian tongue.
G. Doran (1975)
10.1164/AJRCCM.160.1.9806054
Collapsibility of passive pharynx in patients with acromegaly.
S. Isono (1999)
Fluoroscopic MR of the pharynx in patients with obstructive sleep apnea.
L. Jäger (1998)
10.1016/j.jneumeth.2007.01.006
New display of the timing and firing frequency of single motor units
J. P. Saboisky (2007)
10.1121/1.2363926
Measuring tongue motion from tagged cine-MRI using harmonic phase (HARP) processing.
V. Parthasarathy (2007)
10.1378/CHEST.84.3.286
Breathing patterns. 2. Diseased subjects.
M. Tobin (1983)
10.1152/JAPPL.1995.78.2.680
Respiratory-related control of palatoglossus and levator palatini muscle activity.
D. J. Tangel (1995)
10.1113/JPHYSIOL.2003.038810
Within-breath control of genioglossal muscle activation in humans: effect of sleep-wake state.
R. Fogel (2003)
10.1152/JAPPLPHYSIOL.00203.2003
Upper airway response to electrical stimulation of the genioglossus in obstructive sleep apnea.
A. Oliven (2003)
10.1164/RCCM.200507-1148OC
Quantitative upper airway imaging with anatomic optical coherence tomography.
J. Armstrong (2006)
10.1164/AJRCCM.165.1.2011065
Pharyngeal pressure and flow effects on genioglossus activation in normal subjects.
A. Malhotra (2002)
10.1152/JAPPLPHYSIOL.01043.2007
Influence of tongue muscle contraction and dynamic airway pressure on velopharyngeal volume in the rat.
R. Fregosi (2008)
10.1016/j.resp.2006.08.010
Mechanical effects of genioglossus muscle stimulation on the pharyngeal airway by MRI in cats
M. Brennick (2007)
10.1152/JAPPL.2001.90.4.1373
MRI study of pharyngeal airway changes during stimulation of the hypoglossal nerve branches in rats.
M. Brennick (2001)
10.1002/(SICI)1522-2594(199912)42:6<1048::AID-MRM9>3.0.CO;2-M
Cardiac motion tracking using CINE harmonic phase (HARP) magnetic resonance imaging
N. Osman (1999)
10.1152/JAPPLPHYSIOL.01017.2002
Heterogeneous activity of the human genioglossus muscle assessed by multiple bipolar fine-wire electrodes.
P. Eastwood (2003)
10.1164/AJRCCM.164.11.2110043A
Wagging the tongue and guarding the airway. Reflex control of the genioglossus.
J. Remmers (2001)
10.1164/AJRCCM.151.2.7842206
Hypoglossal nerve stimulation affects the pressure-volume behavior of the upper airway.
W. Hida (1995)
10.1164/AJRCCM/147.5.1144
Effect of electrical stimulation of the hypoglossal nerve on airflow mechanics in the isolated upper airway.
A. R. Schwartz (1993)
10.1001/ARCHOTOL.127.10.1216
Therapeutic electrical stimulation of the hypoglossal nerve in obstructive sleep apnea.
A. R. Schwartz (2001)
10.1183/09031936.00131106
Effect of genioglossus contraction on pharyngeal lumen and airflow in sleep apnoea patients
A. Oliven (2007)
10.1001/ARCHOTOL.1997.01900010067009
Direct hypoglossal nerve stimulation in obstructive sleep apnea.
D. Eisele (1997)
10.1164/AJRCCM.158.4.9712063
State-related changes in upper airway caliber and surrounding soft-tissue structures in normal subjects.
F. J. Trudo (1998)
10.1152/JAPPLPHYSIOL.00332.2002
Geniohyoid muscle function in awake canines.
M. Yokoba (2003)
10.1152/JAPPL.1993.74.4.1504
Dynamic imaging of the upper airway during respiration in normal subjects.
R. Schwab (1993)
10.1016/S0021-9290(98)00109-2
Intramural mechanics of the human tongue in association with physiological deformations.
V. Napadow (1999)
10.1242/jeb.007096
Anatomical basis of lingual hydrostatic deformation
R. Gilbert (2007)
10.1002/NBM.1129
Regional velopharyngeal compliance in the rat: influence of tongue muscle contraction
Cornelius Van Zutphen (2007)
10.1016/S0034-5687(97)00095-9
Respiratory-related control of extrinsic tongue muscle activity.
R. Fregosi (1997)
10.1152/JAPPL.1988.64.2.535
Induction of upper airway occlusion in sleeping individuals with subatmospheric nasal pressure.
A. R. Schwartz (1988)
10.1111/J.1748-1716.1981.TB06757.X
Contraction times of the cat's tongue muscles measured by light reflection. Innervation of individual tongue muscles.
E. Hellstrand (1981)
10.1016/S0034-5687(01)00230-4
Genioglossal inspiratory activation: central respiratory vs mechanoreceptive influences.
G. Pillar (2001)
10.1152/JAPPLPHYSIOL.00324.2002
Awake negative pressure reflex response of the genioglossus in OSA patients and normal subjects.
R. Berry (2003)
10.1164/RCCM.200309-1283OC
Regional effects of selective pharyngeal muscle activation on airway shape.
S. Kuna (2004)
10.1016/0301-0082(80)90008-8
The neural regulation of tongue movements
A. Lowe (1980)
10.1152/JAPPL.1998.84.1.190
Effects of NREM sleep on dynamic within-breath changes in upper airway patency in humans.
M. Morrell (1998)
10.1152/JAPPL.1993.75.3.1053
Functional electrical stimulation and respiration during sleep.
M. Decker (1993)
10.1152/JAPPL.1986.61.3.890
Pharyngeal cross-sectional area in normal men and women.
I. G. Brown (1986)
10.1164/AJRCCM.156.2.9607115
Neuromuscular activity and upper airway collapsibility. Mechanisms of action in the decerebrate cat.
J. Rowley (1997)
10.1016/S0034-5687(01)00254-7
Sublingual electrical stimulation of the tongue during wakefulness and sleep.
A. Oliven (2001)
10.1172/JCI115751
Waking genioglossal electromyogram in sleep apnea patients versus normal controls (a neuromuscular compensatory mechanism).
W. Mezzanotte (1992)
10.1109/42.141648
Motion estimation from tagged MR image sequences
J. Prince (1992)
10.1093/SLEEP/19.SUPPL_10.184
Structural basis for alterations in upper airway collapsibility.
A. R. Schwartz (1996)
10.1016/S0030-6665(02)00178-0
Tongue neuromuscular and direct hypoglossal nerve stimulation for obstructive sleep apnea.
D. Eisele (2003)
S. Cheng and others J Physiol
10.1152/JAPPL.1980.49.4.638
Activation of upper airway muscles before onset of inspiration in normal humans.
K. Strohl (1980)
10.1164/RCCM.200203-214OC
Effects of pharyngeal muscle activation on airway pressure-area relationships.
S. Kuna (2002)
10.1152/JAPPL.1995.79.6.2132
Advancement of the mandible improves velopharyngeal airway patency.
S. Isono (1995)
10.1152/JAPPL.1998.85.5.1884
MRI study of regional variations of pharyngeal wall compliance in cats.
M. Brennick (1998)
10.1111/j.1469-7793.1998.265bu.x
Co‐activation of tongue protrudor and retractor muscles during chemoreceptor stimulation in the rat
D. Fuller (1998)
10.1113/jphysiol.1991.sp018536
Evidence for reflex upper airway dilator muscle activation by sudden negative airway pressure in man.
R. Horner (1991)
10.1016/0014-4886(76)90061-3
The human tongue during sleep: Electromyographic activity of the genioglossus muscle
E. Sauerland (1976)
10.1152/JAPPLPHYSIOL.00379.2006
Anatomic consequences of intrinsic tongue muscle activation.
E. F. Bailey (2006)
10.1152/JAPPL.1998.85.3.908
Activity of respiratory pump and upper airway muscles during sleep onset.
C. Worsnop (1998)
10.1002/jmri.1068
Determination of regional pulmonary parenchymal strain during normal respiration using spin inversion tagged magnetization MRI
V. Napadow (2001)
10.1183/09031936.00063406
Upper airway collapsibility, dilator muscle activation and resistance in sleep apnoea
R. Pierce (2007)
10.1152/JAPPLPHYSIOL.00942.2001
Modulation of upper airway collapsibility during sleep: influence of respiratory phase and flow regimen.
H. Schneider (2002)
10.1152/JN.1995.74.2.547
Contractile properties of the tongue muscles: effects of hypoglossal nerve and extracellular motoneuron stimulation in rat.
E. E. Gilliam (1995)
10.1164/AJRCCM.164.7.2011030
Effects of pharyngeal muscle activation on airway size and configuration.
S. Kuna (2001)
10.1152/JAPPL.1997.82.4.1319
Anatomy of pharynx in patients with obstructive sleep apnea and in normal subjects.
S. Isono (1997)
10.1152/JAPPL.1982.52.2.438
Influence of upper airway pressure changes on genioglossus muscle respiratory activity.
O. Mathew (1982)
10.1016/S0012-3692(15)33498-X
Breathing patterns. 1. Normal subjects.
M. Tobin (1983)
10.1164/AJRCCM.154.3.8810623
Mechanical properties of the velopharynx in obese patients with obstructive sleep apnea.
C. Ryan (1996)
Online supplemental material for this paper can be accessed at: http://jp.physoc.org/cgi/content/full/jphysiol.2008.156430/DC1 C 2008 The Authors
(2008)
Trunks, Tongues, and Tentacles: Moving with Skeletons of Muscle
K. Smith (1989)
10.1152/JAPPLPHYSIOL.00733.2003
Coordination of intrinsic and extrinsic tongue muscles during spontaneous breathing in the rat.
E. F. Bailey (2004)
10.1164/AJRCCM.157.4.9706067
The hypotonic upper airway in obstructive sleep apnea: role of structures and neuromuscular activity.
A. R. Schwartz (1998)
10.1111/j.1469-7793.2003.00563.x
Pressure‐volume behaviour of the rat upper airway: effects of tongue muscle activation
E. F. Bailey (2003)
10.1164/AJRCCM.162.3.9912067
Genioglossal but not palatal muscle activity relates closely to pharyngeal pressure.
A. Malhotra (2000)
10.1152/JAPPLPHYSIOL.00772.2005
Pathogenesis of obstructive sleep apnea.
C. Ryan (2005)
10.1152/JAPPL.1991.70.5.2242
Pressure-diameter relationships of the upper airway in awake supine subjects.
J. Wheatley (1991)
10.1183/09031936.99.14612589
Effects of tongue electrical stimulation on pharyngeal mechanics in anaesthetized patients with obstructive sleep apnoea.
S. Isono (1999)
10.1002/1097-0185(20001201)260:4<378::AID-AR70>3.0.CO;2-A
Functional anatomy of the hypoglossal innervated muscles of the rat tongue: A model for elongation and protrusion of the mammalian tongue
J. McClung (2000)
10.1152/JAPPLPHYSIOL.00204.2006
Modulation of upper airway muscle activities by bronchopulmonary afferents.
E. F. Bailey (2006)
10.1152/JAPPL.1995.78.6.2180
Central and reflex neural control of genioglossus in subjects who underwent laryngectomy.
J. Innes (1995)
10.1152/JAPPL.1992.72.3.925
Mechanisms of control of alae nasi muscle activity.
W. Mezzanotte (1992)
10.1093/SLEEP/20.4.278
Night-to-night variability in CPAP use over the first three months of treatment.
T. Weaver (1997)
10.1111/j.1469-7793.1999.0601m.x
Effect of co‐activation of tongue protrudor and retractor muscles on tongue movements and pharyngeal airflow mechanics in the rat
D. Fuller (1999)
10.1152/JAPPL.2000.88.5.1831
Effect of age on sleep onset-related changes in respiratory pump and upper airway muscle function.
C. Worsnop (2000)
10.1001/ARCHOTOL.1995.01890120021004
The effects of selective nerve stimulation on upper airway airflow mechanics.
D. Eisele (1995)
10.1111/j.1469-7793.2001.0525f.x
Effect of pulmonary stretch receptor feedback and CO2 on upper airway and respiratory pump muscle activity in the rat
E. F. Bailey (2001)
10.1152/JAPPL.1995.78.5.1950
Dilatory effects of upper airway muscle contraction induced by electrical stimulation in awake humans.
R. Schnall (1995)
10.1164/AJRCCM.160.6.9903001
Response of human tongue protrudor and retractors to hypoxia and hypercapnia.
J. Mateika (1999)
10.1183/09031936.01.17100790
Magnetic resonance imaging of the pharynx in OSA patients and healthy subjects.
M. Ciscar (2001)
Deformation of the upper airway musculature during quiet breathing in humans
S Cheng (2007)
10.1113/jphysiol.2004.073502
Pharyngeal airway wall mechanics using tagged magnetic resonance imaging during medial hypoglossal nerve stimulation in rats
M. Brennick (2004)
10.1164/RCCM.200412-1631SO
Pathogenesis of obstructive and central sleep apnea.
D. White (2005)
Upper airway imaging in relation to obstructive sleep apnea.
Fleetham Ja (1992)
The modulation of upper airway critical pressures during sleep.
P. Smith (1990)
10.1152/JN.00940.2005
Tonic and phasic respiratory drives to human genioglossus motoneurons during breathing.
J. P. Saboisky (2006)
10.1109/42.845177
Imaging heart motion using harmonic phase MRI
N. Osman (2000)
10.1152/JAPPL.1980.49.5.801
Control of genioglossus muscle inspiratory activity.
R. Brouillette (1980)
10.1111/j.1469-7793.1999.293ad.x
Oral airway flow dynamics in healthy humans
T. Amis (1999)
10.1152/ajpgi.1999.277.3.G695
Biomechanical basis for lingual muscular deformation during swallowing.
V. Napadow (1999)
10.1152/JAPPL.1993.74.5.2198
Pattern of breathing and upper airway mechanics during wakefulness and sleep in healthy elderly humans.
D. Hudgel (1993)
10.1152/JAPPL.1996.81.2.643
Electrical stimulation of the lingual musculature in obstructive sleep apnea.
A. R. Schwartz (1996)
10.1152/JAPPL.1993.75.1.148
Static mechanics of the velopharynx of patients with obstructive sleep apnea.
S. Isono (1993)
10.1044/1092-4388(2001/009)
Morphological analyses of the human tongue musculature for three-dimensional modeling.
H. Takemoto (2001)
10.1164/AJRCCM.152.5.7582313
Upper airway and soft tissue anatomy in normal subjects and patients with sleep-disordered breathing. Significance of the lateral pharyngeal walls.
R. Schwab (1995)



This paper is referenced by
10.2147/JMDH.S45443
Anatomic connections of the diaphragm: influence of respiration on the body system
Bruno Bordoni (2013)
10.2217/EBO.13.343
Pathophysiology of upper airway collapse
J. Carberry (2014)
10.1371/journal.pone.0164252
Correction: Effects of Aging on Genioglossus Motor Units in Humans
J. P. Saboisky (2016)
10.1093/SLEEP/33.3.379
Discharge patterns of human genioglossus motor units during arousal from sleep.
V. Wilkinson (2010)
10.1111/jsr.13032
Dynamic tongue area measurements in ultrasound images for adults with obstructive sleep apnea
C. O. Manlises (2020)
10.1152/jn.00686.2009
Tonically discharging genioglossus motor units show no evidence of rate coding with hypercapnia.
P. Richardson (2010)
10.1097/SCS.0b013e31821d4c25
Pneumomediastinum secondary to isolated orbital floor fracture.
Stefan Loretan (2011)
10.1016/j.ultrasmedbio.2018.12.003
Sagittal Measurement of Tongue Movement During Respiration: Comparison Between Ultrasonography and Magnetic Resonance Imaging.
B. Kwan (2019)
10.1517/14728220903005608
Potential therapeutic targets in obstructive sleep apnoea
J. P. Saboisky (2009)
10.1152/japplphysiol.00382.2015
Effect of head and jaw position on respiratory-related motion of the genioglossus.
Mingshu Cai (2016)
10.23838/PFM.2018.00100
Fast upper airway magnetic resonance imaging for assessment of speech production and sleep apnea
Yoon-Chul Kim (2018)
10.1152/japplphysiol.00373.2010
The effect of increased genioglossus activity and end-expiratory lung volume on pharyngeal collapse.
A. Jordan (2010)
10.1016/J.JDSR.2011.12.003
Tongue and upper airway function in subjects with and without obstructive sleep apnea
Takashi Ono (2012)
10.1371/journal.pone.0104572
Effects of Aging on Genioglossus Motor Units in Humans
J. P. Saboisky (2014)
10.1113/jphysiol.2008.160317
Going to the movies can make all the difference
M. Morrell (2008)
10.1007/978-1-4614-4466-4_13
Tongue Biomechanics and Motor Control
Mary Snyder Shall (2012)
breathingminimal respiratory activity during quiet Single motor unit recordings in human geniohyoid
E. Bilston (2015)
10.14219/JADA.ARCHIVE.2011.0325
The effects of mouthpiece use on gas exchange parameters during steady-state exercise in college-aged men and women.
D. Garner (2011)
10.1007/978-94-007-6627-3_28
Dynamics of upper airways during the Müller maneuver in healthy subjects: a cine MRI study.
Isato Fukushi (2013)
10.1002/mrm.24608
Novel retrospective, respiratory‐gating method enables 3D, high resolution, dynamic imaging of the upper airway during tidal breathing
M. Wagshul (2013)
10.1016/j.ijpharm.2019.118773
Does Upper Airway Deformation Affect Drug Deposition?
S. Cheng (2019)
Investigation of the availability of tongue movements in Mallampati classification.
Alkin Çolak (2011)
10.1152/japplphysiol.01257.2013
A novel ultrasound technique to measure genioglossus movement in vivo.
B. Kwan (2014)
10.1152/japplphysiol.01245.2013
Peripharyngeal tissue deformation and stress distributions in response to caudal tracheal displacement: pivotal influence of the hyoid bone?
J. Amatoury (2014)
10.1016/j.jbiomech.2012.04.027
Passive movement of human soft palate during respiration: A simulation of 3D fluid/structure interaction.
Jian Zhu (2012)
10.1007/978-3-662-59210-6_3
Kiefer und Kauen aus funktionell therapeutischer Sicht
Ulrike Albrecht (2019)
10.1007/978-1-4614-4466-4
Craniofacial Muscles
L. McLoon (2013)
10.14814/phy2.14175
Measurement of maximum tongue protrusion force (MTPF) in healthy young adults
Jayoung Kim (2019)
10.1002/CNM.1487
Computational model of soft tissues in the human upper airway.
J-P. V. Pelteret (2012)
10.1002/cphy.c110023
Neural control of the upper airway: integrative physiological mechanisms and relevance for sleep disordered breathing.
R. Horner (2012)
10.1016/B978-0-7020-6294-0.00005-8
Chapter 5 – Pulmonary Ventilation
Andrew B Lumb (2017)
10.15713/ins.jcri.217
Investigations for diseases of the tongue: A review
C. David (2018)
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