Modulation of upper airway muscle activities by bronchopulmonary afferents

Journal of Applied Physiology

Volumn 101, Issue 2, 2006, Pages 609-617

  Bailey, E Fiona ^a   Fregosi, Ralph F ^b  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Hyoid; Larynx; Tongue; Vagus

Indexed keywords

BREATHING; BREATHING MUSCLE; EXPERIMENTAL MODEL; HERING BREUER REFLEX; LARYNX; LUNG CLEARANCE; LUNG INFLATION; LUNG RECEPTOR; MUSCLE CONTRACTION; MUSCLE FUNCTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; TONGUE;

AIRWAY OBSTRUCTION; ANIMALS; BRONCHI; HUMANS; LARYNX; LUNG; MOTOR NEURONS; MUSCLE, SKELETAL; NERVE FIBERS, UNMYELINATED; NEURONS, AFFERENT; PULMONARY STRETCH RECEPTORS; RESPIRATORY MUSCLES; TONGUE;

EID: 33746732275     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00204.2006     Document Type: Review

References (115)

1. Adriaensen D, Timmermans JP, Brouns I, Berthoud HR, Neuhuber WL, and Scheuermann DW. Pulmonary intraepithelial vagal nodose afferent nerve terminals are confined to neuroepithelial bodies: an anterograde tracing and confocal microscopy study in adult rats. Cell Tissue Res 293: 395-405, 1998.
2. Amis TC, Brancatisano A, and Tully A. Thyroid cartilage movements during breathing. J Appl Physiol 78: 441-448, 1995.
3. Armstrong DJ and Luck JC. A comparative study of irritant and type J receptors in the cat. Respir Physiol 21: 47-60, 1974.
4. Bailey EF and Fregosi RF. Coordination of intrinsic and extrinsic tongue muscles during spontaneous breathing in the rat. J Appl Physiol 96: 440-449, 2004.
5. Bailey EF and Fregosi RF. Pressure-volume behaviour of the rat upper airway: effects of tongue muscle activation. J Physiol 548: 563-568, 2003.
6. 2-dependent changes in intrinsic and extrinsic tongue muscle activities in the rat. Am J Respir Crit Care Med 171: 1403-1407, 2005.
7. Bailey EF, Jones CL, Reeder JC, Fuller DD, and Fregosi RF. Effect of pulmonary stretch receptor feedback and CO(2) on upper airway and respiratory pump muscle activity in the rat. J Physiol 532: 525-534, 2001.
8. Baluk P, Nadel JA, and McDonald DM. Substance P-immunoreactive sensory axons in the rat respiratory tract: a quantitative study of their distribution and role in neurogenic inflammation. J Comp Neurol 319: 586-598, 1992.
9. Barillot JC and Bianchi AL. [Activity of laryngeal motoneurons during the Hering-Breuer reflex]. J Physiol (Paris) 63: 783-792, 1971.
10. Bartlett D Jr. Upper airway motor systems. In: Handbook of Physiology. The Respiratory System. Control of Breathing. Bethesda, MD: Am. Physiol. Soc., 1986, sect. 3, vol. II, pt. 1, chapt. 8, p. 223-245.
11. Bartlett D Jr, Knuth SL, and Knuth KV. Effects of pulmonary stretch receptor blockade on laryngeal responses to hypercapnia and hypoxia. Respir Physiol 45: 67-77, 1981.
12. Bartlett D Jr, Remmers JE, and Gautier H. Laryngeal regulation of respiratory airflow. Respir Physiol 18: 194-204, 1973.
13. Bartlett D Jr and Sant'Ambrogio G. Effects of local and systemic hypercapnia on the discharge of stretch receptors in the airways of the dog. Respir Physiol 26: 91-99, 1976.
14. Bartlett D Jr and St. John WM. Influence of lung volume on phrenic, hypoglossal and mylohyoid nerve activities. Respir Physiol 73: 97-109, 1988.
15. Begle RL, Skatrud JB, and Dempsey JA. Ventilatory compensation for changes in functional residual capacity during sleep. J Appl Physiol 62: 1299-1306, 1987.
16. Bishop B. Reflex control of abdominal muscles during positive-pressure breathing. J Appl Physiol 19: 224-232, 1964.
17. Brancatisano A, Dodd DS, and Engel LA. Posterior cricoarytenoid activity and glottic size during hyperpnea in humans. J Appl Physiol 71: 977-982, 1991.
18. Brouillette RT and Thach BT. Control of genioglossus muscle inspiratory activity. J Appl Physiol 49: 801-808, 1980.
19. Cohen MI. Phrenic and recurrent laryngeal discharge patterns and the Hering-Breuer reflex. Am J Physiol 228: 1489-1496, 1975.
20. Coleridge HM, Coleridge JC, and Luck JC. Pulmonary afferent fibres of small diameter stimulated by capsaicin and by hyperinflation of the lungs. J Physiol 179: 248-262, 1965.
21. Coleridge HM and Coleridge JCC. Reflexes evoked from the tracheobronchial tree and lungs. In: Handbook of Physiology. The Respiratory System. Control of Breathing. Bethesda, MD: Am. Physiol. Soc., 1986, sect. 3, vol. II, pt. 1, chapt. 12, p. 395-429.
22. Davies A, Dixon M, Callanan D, Huszczuk A, Widdicombe JG, and Wise JC. Lung reflexes in rabbits during pulmonary stretch receptor block by sulphur dioxide. Respir Physiol 34: 83-101, 1978.
23. Davies A, Sant'Ambrogio F, and Sant'Ambrogio G. Onset of inspiration in rabbit during artificial ventilation. J Physiol 318: 17-23, 1981.
24. Dempsey JA, Adams L, Ainsworth DM, Fregosi RF, Gallagher CG, Guz A, Johnson BD, and Powers RK. Airway, lung and respiratory muscle function during exercise. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 12, chapt. 11, p. 448-514.
25. Dobbins EG and Feldman JL. Differential innervation of protruder and retractor muscles of the tongue in rat. J Comp Neurol 357: 376-394, 1995.
26. Dutschmann M and Paton JF. Inhibitory synaptic mechanisms regulating upper airway patency. Respir Physiol Neurobiol 131: 57-63, 2002.
27. Eisele DW, Schwartz AR, Hari A, Thut DC, and Smith PL. The effects of selective nerve stimulation on upper airway airflow mechanics. Arch Otolaryngol Head Neck Surg 121: 1361-1364, 1995.
28. Eisele DW, Schwartz AR, and Smith PL. Tongue neuromuscular and direct hypoglossal nerve stimulation for obstructive sleep apnea. Otolaryngol Clin North Am 36: 501-510, 2003.
29. Eisele DW, Smith PL, Alam DS, and Schwartz AR. Direct hypoglossal nerve stimulation in obstructive sleep apnea. Arch Otolaryngol Head Neck Surg 123: 57-61, 1997.
30. Eldridge F and Millhorn D. Oscillation, gating and memory. In: Handbook of Physiology. The Respiratory System. Control of Breathing. Bethesda, MD: Am. Physiol. Soc., 1986, sect. 3, vol. II, pt. 1, chapt. 3, p. 93-114.
31. Franz DN and Iggo A. Conduction failure in myelinated and non-myelinated axons at low temperatures. J Physiol 199: 319-345, 1968.
32. Fregosi RF and Bartlett D Jr. Central inspiratory influence on abdominal expiratory nerve activity. J Appl Physiol 65: 1647-1654, 1988.
33. Fregosi RF and Fuller DD. Respiratory-related control of extrinsic tongue muscle activity. Respir Physiol 110: 295-306, 1997.
34. Fukuda H, Sasaki CT, and Kirchner JA. Vagal afferent influences on the phasic activity of the posterior cricoarytenoid muscle. Acta Otolaryngol (Stockh) 75: 112-118, 1973.
35. Fukuda Y and Honda Y. Differences in respiratory neural activities between vagal (superior laryngeal), hypoglossal, and phrenic nerves in the anesthetized rat. Jpn J Physiol 32: 387-398, 1982.
36. 2-responsiveness of efferent superior laryngeal, hypoglossal, and phrenic respiratory activities in anesthetized rats. Jpn J Physiol 32: 689-698, 1982.
37. Fuller D, Mateika JH, and Fregosi RF. Co-activation of tongue protrudor and retractor muscles during chemoreceptor stimulation in the rat. J Physiol 507: 265-276, 1998.
38. Fuller DD, Williams JS, Janssen PL, and Fregosi RF. Effect of co-activation of tongue protrudor and retractor muscles on tongue movements and pharyngeal airflow mechanics in the rat. J Physiol 519: 601-613, 1999.
39. Gestreau C, Dutschmann M, Obled S, and Bianchi AL. Activation of XII motoneurons and premotor neurons during various oropharyngeal behaviors. Respir Physiol Neurobiol 147: 159-176, 2005.
40. Glogowska M, Stransky A, and Widdicombe JG. Reflex control of discharge in motor fibres to the larynx. J Physiol 239: 365-379, 1974.
41. Green JH and Neil E. The respiratory function of the laryngeal muscles. J Physiol 129: 134-141, 1955.
42. Guz A and Trenchard DW. The role of non-myelinated vagal afferent fibres from the lungs in the genesis of tachypnoea in the rabbit. J Physiol 213: 345-371, 1971.
43. Hammouda M and Wilson WH. The presence in the vagus of fibres transmitting impulses augmenting the frequency of respiration. J Physiol (Lond) 83: 292-312, 1935.
44. Harding R, England SJ, Stradling JR, Kozar LF, and Phillipson EA. Respiratory activity of laryngeal muscles in awake and sleeping dogs. Respir Physiol 66: 315-326, 1986.
45. Hatridge J, Haji A, Perez-Padilla JR, and Remmers JE. Rapid shallow breathing caused by pulmonary vascular congestion in cats. J Appl Physiol 67: 2257-2264, 1989.
46. Haxhiu MA, Deal EC, and Cherniack NS. Influence of respiratory drive on airway responses to excitation of lung C-fibers. J Appl Physiol 67: 203-209, 1989.
47. Haxhiu MA, Deal EC Jr, Van de Graaff WB, Van Lunteren E, Salamone JA, and Cherniack NS. Bronchoconstriction: upper airway dilating muscle and diaphragm activity. J Appl Physiol 55: 1837-1843, 1983.
48. Haxhiu MA, Van Lunteren E, and Cherniack NS. Responses of upper-airway dilating muscles and diaphragm activity to end-expiratory pressure loading in anesthetized dogs. Respiration 56: 1-10, 1989.
49. Haxhiu MA, Van Lunteren E, Deal EC, and Cherniack NS. Effect of stimulation of pulmonary C-fiber receptors on canine respiratory muscles. J Appl Physiol 65: 1087-1092, 1988.
50. Higenbottam T. Narrowing of glottis opening in humans associated with experimentally induced bronchoconstriction. J Appl Physiol 49: 403-407, 1980.
51. Holmes HR and Remmers JE. Stimulation of vagal C-fibers alters timing and distribution of respiratory motor output in cats. J Appl Physiol 67: 2249-2256, 1989.
52. Horner RL, Innes JA, Morrell MJ, Shea SA, and Guz A. The effect of sleep on reflex genioglossus muscle activation by stimuli of negative airway pressure in humans. J Physiol 476: 141-151, 1994.
53. Horner RL, Innes JA, Murphy K, and Guz A. Evidence for reflex upper airway dilator muscle activation by sudden negative airway pressure in man. J Physiol 436: 15-29, 1991.
54. Huang Q, Zhou D, St. John WM, and Bartlett D Jr. Influence of lung volume on activities of branches of the recurrent laryngeal nerve. J Appl Physiol 67: 1179-1184, 1989.
55. Hudgel DW. Variable site of airway narrowing among obstructive sleep apnea patients. J Appl Physiol 61: 1403-1409, 1986.
56. Hwang JC, Bartlett D Jr, and St. John WM. Characterization of respiratory-modulated activities of hypoglossal motoneurons. J Appl Physiol 55: 793-798, 1983.
57. Hwang JC, St. John WM, and Bartlett D Jr. Receptors responding to changes in upper airway pressure. Respir Physiol 55: 355-366, 1984.
58. Hwang JC, St. John WM, and Bartlett D Jr. Afferent pathways for hypoglossal and phrenic responses to changes in upper airway pressure. Respir Physiol 55: 341-354, 1984.
59. Innes JA, Morrell MJ, Kobayashi I, Hamilton RD, and Guz A. Central and reflex neural control of genioglossus in subjects who underwent laryngectomy. J Appl Physiol 78: 2180-2186, 1995.
60. Iscoe S. Central control of the upper airway. In: Respiratory Function of the Upper Airway, edited by Mathew O and Sant'Ambrogio F. New York: Dekker, 1988, p. 125-191.
61. Iwasaki H, Ohmori H, Sumita S, Yamauchi M, and Namiki A. Influence of continuous positive airway pressure on EMG activities of the cricothyroid and posterior cricoarytenoid muscles of the canine larynx. Intensive Care Med 22: 805-808, 1996.
62. Janssen PL, Williams JS, and Fregosi RF. Consequences of periodic augmented breaths on tongue muscle activities in hypoxic rats. J Appl Physiol 88: 1915-1923, 2000.
63. Joad JP, Kott KS, and Bonham AC. Nitric oxide contributes to substance P-induced increases in lung rapidly adapting receptor activity in guinea-pigs. J Physiol 503: 635-643, 1997.
64. Jonzon A, Pisarri TE, Roberts AM, Coleridge JC, and Coleridge HM. Attenuation of pulmonary afferent input by vagal cooling in dogs. Respir Physiol 72: 19-33, 1988.
65. Kappagoda CT, Skepper JN, McNaughton L, Siew EE, and Navaratnam V. Morphology of presumptive rapidly adapting receptors in the rat bronchus. J Anat 168: 265-276, 1990.
66. Kaufman MP, Coleridge HM, Coleridge JC, and Baker DG. Bradykinin stimulates afferent vagal C-fibers in intrapulmonary airways of dogs. J Appl Physiol 48: 511-517, 1980.
67. Konrad HR and Rattenborg CC. Combined action of laryngeal muscles. Acta Otolaryngol (Stockh) 67: 646-649, 1969.
68. 67a. Kubin L, Alheid GF, Zuperku EJ, and McCrimmon DR. Central pathways of pulmonary and lower airway vagal afferents. J Appl Physiol [April 27, 2006; 10.1152/japplphysiol.00252.2006].
69. Kuna ST. Effects of pharyngeal muscle activation on airway size and configuration. Am J Respir Crit Care Med 164: 1236-1241, 2001.
70. Kuna ST. Inhibition of inspiratory upper airway motoneuron activity by phasic volume feedback. J Appl Physiol 60: 1373-1379, 1986.
71. Kuna ST. Interaction of hypercapnia and phasic volume feedback on motor control of the upper airway. J Appl Physiol 63: 1744-1749, 1987.
72. Kuna ST. Respiratory-related activation and mechanical effects of the pharyngeal constrictor muscles. Respir Physiol 119: 155-161, 2000.
73. Kuna ST and Brennick MJ. Effects of pharyngeal muscle activation on airway pressure-area relationships. Am J Respir Crit Care Med 166: 972-977, 2002.
74. Lee KZ, Lu IJ, Ku LC, Lin JT, and Hwang JC. Response of respiratory-related hypoglossal nerve activity to capsaicin-induced pulmonary C-fiber activation in rats. J Biomed Sci 10: 706-717, 2003.
75. Lu IJ, Lee KZ, Lin JT, and Hwang JC. Capsaicin administration inhibits the abducent branch but excites the thyroarytenoid branch of the recurrent laryngeal nerves in the rat. J Appl Physiol 98: 1646-1652, 2005.
76. Mathew OP, Sant'Ambrogio FB, Woodson GE, and Sant'Ambrogio G. Respiratory activity of the cricothyroid muscle. Ann Otol Rhinol Laryngol 97: 680-687, 1988.
77. Miller AJ. Oral and pharyngeal reflexes in the mammalian nervous system: their diverse range in complexity and the pivotal role of the tongue. Crit Rev Oral Biol Med 13: 409-425, 2002.
78. Miserocchi G and Sant'Ambrogio G. Responses of pulmonary stretch receptors to static pressure inflations. Respir Physiol 21: 77-85, 1974.
79. Murakami Y and Kirchner JA. Respiratory movements of the vocal cords. An electromyographic study in the cat. Laryngoscope 82: 454-467, 1972.
80. Orem J, Netick A, and Dement WC. Increased upper airway resistance to breathing during sleep in the cat. Electroencephalogr Clin Neurophysiol 43: 14-22, 1977.
81. Paintal AS. Mechanism of stimulation of type J pulmonary receptors. J Physiol 203: 511-532, 1969.
82. Polacheck J, Strong R, Arens J, Davies C, Metcalf I, and Younes M. Phasic vagal influence on inspiratory motor output in anesthetized human subjects. J Appl Physiol 49: 609-619, 1980.
83. Richardson CA, Herbert DA, and Mitchell RA. Modulation of pulmonary stretch receptors and airway resistance by parasympathetic efferents. J Appl Physiol 57: 1842-1849, 1984.
84. Richardson PS, Sant'Ambrogio G, Mortola J, and Bianconi R. The activity of lung afferent nerves during tracheal occlusion. Respir Physiol 18: 273-283, 1973.
85. Roberts AM, Schultz HD, Green JF, Armstrong DJ, Kaufman MP, Coleridge HM, and Coleridge JC. Reflex tracheal contraction evoked in dogs by bronchodilator prostaglandins E2 and I2. J Appl Physiol 58: 1823-1831, 1985.
86. Ryan S, McNicholas WT, O'Regan RG, and Nolan P. Effect of upper airway negative pressure and lung inflation on laryngeal motor unit activity in rabbit. J Appl Physiol 92: 269-278, 2002.
87. Sant'Ambrogio G. Information arising from the tracheobronchial tree of mammals. Physiol Rev 62: 531-569, 1982.
88. Sant'Ambrogio G, Remmers JE, de Groot WJ, Callas G, and Mortola JP. Localization of rapidly adapting receptors in the trachea and main stem bronchus of the dog. Respir Physiol 33: 359-366, 1978.
89. Sant'Ambrogio G and Widdicombe J. Reflexes from airway rapidly adapting receptors. Respir Physiol 125: 33-45, 2001.
90. Schwartz AR, O'Donnell CP, Baron J, Schubert N, Alam D, Samadi SD, and Smith PL. The hypotonic upper airway in obstructive sleep apnea: role of structures and neuromuscular activity. Am J Respir Crit Care Med 157: 1051-1057, 1998.
91. 2. J Appl Physiol 74: 1597-1605, 1993.
92. Schwartz AR, Thut DC, Russ B, Seelagy M, Yuan X, Brower RG, Permutt S, Wise RA, and Smith PL. Effect of electrical stimulation of the hypoglossal nerve on airflow mechanics in the isolated upper airway. Am Rev Respir Dis 147: 1144-1150, 1993.
93. Seeley RR, Stephens TD, and Tate P. Anatomy and Physiology. Boston, MA: McGraw Hill, 2006.
94. Sibuya M, Kanamaru A, and Homma I. Inspiratory prolongation by vagal afferents from pulmonary mechanoreceptors in rabbits. Jpn J Physiol 43: 669-684, 1993.
95. Sica AL, Cohen MI, Donnelly DF, and Zhang H. Hypoglossal motoneuron responses to pulmonary and superior laryngeal afferent inputs. Respir Physiol 56: 339-357, 1984.
96. Sica AL, Cohen MI, Donnelly DF, and Zhang H. Responses of recurrent laryngeal motoneurons to changes of pulmonary afferent inputs. Respir Physiol 62: 153-168, 1985.
97. St. John WM and Zhou D. Reductions of neural activities to upper airway muscles after elevations in static lung volume. J Appl Physiol 73: 701-707, 1992.
98. Stanchina ML, Malhotra A, Fogel RB, Trinder J, Edwards JK, Schory K, and White DP. The influence of lung volume on pharyngeal mechanics, collapsibility, and genioglossus muscle activation during sleep. Sleep 26: 851-856, 2003.
99. Stransky A, Szereda-Przestaszewska M, and Widdicombe JG. The effects of lung reflexes on laryngeal resistance and motoneurone discharge. J Physiol 231: 417-438, 1973.
100. Takemoto H. Morphological analyses of the human tongue musculature for three-dimensional modeling. J Speech Lang Hear Res 44: 95-107, 2001.
101. Travers JB and Rinaman L. Identification of lingual motor control circuits using two strains of pseudorabies virus. Neuroscience 115: 1139-1151, 2002.
102. Van de Graaff WB, Gottfried SB, Mitra J, Van Lunteren E, Cherniack NS, and Strohl KP. Respiratory function of hyoid muscles and hyoid arch. J Appl Physiol 57: 197-204, 1984.
103. Van Lunteren E and Dick TE. Motor unit regulation of mammalian pharyngeal dilator muscle activity. J Clin Invest 84: 577-585, 1989.
104. Van Lunteren E, Haxhiu MA, and Cherniack NS. Effects of tracheal airway occlusion on hyoid muscle length and upper airway volume. J Appl Physiol 67: 2296-2302, 1989.
105. Van Lunteren E, Strohl KP, Parker DM, Bruce EN, Van de Graaff WB, and Cherniack NS. Phasic volume-related feedback on upper airway muscle activity. J Appl Physiol 56: 730-736, 1984.
106. Van Lunteren E, Van de Graaff WB, Parker DM, Strohl KP, Mitra J, Salamone J, and Cherniack NS. Activity of upper airway muscles during augmented breaths. Respir Physiol 53: 87-98, 1983.
107. Wheatley JR, Brancatisano A, and Engel LA. Cricothyroid muscle responses to increased chemical drive in awake normal humans. J Appl Physiol 70: 2233-2241, 1991.
108. Wheatley JR, Brancatisano A, and Engel LA. Respiratory-related activity of cricothyroid muscle in awake normal humans. J Appl Physiol 70: 2226-2232, 1991.
109. Widdicombe J. Functional morphology and physiology of pulmonary rapidly adapting receptors (RARs). Anat Rec A Discov Mol Cell Evol Biol 270: 2-10, 2003.
110. Widdicombe JG and Glogowska M. Relative roles of irritant, type-J and pulmonary stretch receptors in lung reflexes. Acta Neurobiol Exp (Warsz) 33: 21-31, 1973.
111. Woodson GE, Sant'Ambrogio F, Mathew O, and Sant'Ambrogio G. Effects of cricothyroid muscle contraction on laryngeal resistance and glottic area. Ann Otol Rhinol Laryngol 98: 119-124, 1989.
112. Xi L, Smith CA, Saupe KW, and Dempsey JA. Effects of memory from vagal feedback on short-term potentiation of ventilation in conscious dogs. J Physiol 462: 547-561, 1993.
113. Younes M, Iscoe S, and Milic-Emili J. A method for the assessment of phasic vagal influence on tidal volume. J Appl Physiol 38: 335-343, 1975.
114. Zhou D, Huang Q, St. John WM, and Bartlett D Jr. Respiratory activities of intralaryngeal branches of the recurrent laryngeal nerve. J Appl Physiol 67: 1171-1178, 1989.
115. Zhou D, St. John WM, and Bartlett D Jr. Activities of pulmonary stretch receptors during ventilatory cycles without lung inflation. Respir Physiol 77: 187-194, 1989.