Regional differences in length change and electromyographic heterogeneity in sternohyoid muscle during infant mammalian swallowing

Journal of Applied Physiology

Volumn 109, Issue 2, 2010, Pages 439-448

  Konow, Nicolai ^a   Thexton, Allan ^b   Crompton, A W ^c   German, Rebecca Z ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c HARVARD UNIVERSITY   (United States)

Author keywords

Electromyography; Feeding; Hyolingual; Motor unit; Muscle mechanics; Sonomicrometry

Indexed keywords

ANATOMY AND HISTOLOGY; ANIMAL; BOTTLE FEEDING; ELECTROMYOGRAPHY; HYOID BONE; INNERVATION; MUSCLE CONTRACTION; NECK MUSCLE; NEWBORN; PHYSIOLOGY; STERNUM; SWALLOWING; SWINE; TIME;

ANIMALS; ANIMALS, NEWBORN; BOTTLE FEEDING; DEGLUTITION; ELECTROMYOGRAPHY; HYOID BONE; MUSCLE CONTRACTION; NECK MUSCLES; STERNUM; SWINE; TIME FACTORS;

EID: 77955633232     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00353.2010     Document Type: Article

References (68)

1. Ahn AN, Monti RJ, Biewener AA. In vivo and in vitro heterogeneity of segment length changes in the semimembranosus muscle of the toad. J Physiol 549: 877-888, 2003.
2. Azizi E, Brainerd EL, Roberts TJ. Variable gearing in pennate muscles. Proc Natl Acad Sci USA 105: 1745-1750, 2008.
3. Basmajian J, Stecko G. A new bipolar electrode for electromyography. J Appl Physiol 17: 849, 1962.
4. Berzin F. Electromyographic analysis of the sternohyoid muscle and anterior belly of the digastric muscle in head and tongue movements. J Oral Rehabil 22: 825-829, 1995.
5. Berzin F. Electromyographic analysis of the sternohyoid muscle and anterior belly of the digastric muscle in jaw movements. J Oral Rehabil 22: 463-467, 1995.
6. Carroll AM. Muscle activation and strain during suction feeding in the largemouth bass Micropterus salmoides. J Exp Biol 207: 983-991, 2004.
7. Crompton AW, Cook P, Hiiemae K, Thexton AJ. Movement of the hyoid apparatus during chewing. Nature 258: 69-70, 1975.
8. Crompton AW, German RZ, Thexton AJ. Mechanisms of swallowing and airway protection in infant mammals (Sus domesticus and Macaca fascicularis). J Zool Lond 241: 89-102, 1997.
9. Dick TE, van Lunteren E. Fiber subtype distribution of pharyngeal dilator muscles and diaphragm in the cat. J Appl Physiol 68: 2237-2240, 1990.
10. Doncaster CP, Davey AJH. Analysis of Variance and Covariance: How to Choose and Construct Models for the Life Sciences. Cambridge: Cambridge Univ. Press, 2007, p. 288.
11. Ekberg O. The normal movements of the hyoid bone during swallow. Invest Radiol 21: 408-410, 1986.
12. Fau IR, Palmer JB, Hiiemae KM. Hyoid motion during swallowing: factors affecting forward and upward. Dysphagia 17: 262-272, 2002.
13. Gans C, Gorniak GC. Functional morphology of lingual protrusion in marine toads (Bufo marinus). Am J Anat 163: 195-222, 1982.
14. Gehrking E, Klostermann W, Wessel K, Remmert S. Electromyography of the infrahyoid muscles. Part 1: normal findings. Laryngorhinootologie 80: 662-665, 2001.
15. German R, Crompton A, Thexton A. Variation in EMG activity: a hierarchical approach. Integr Comp Biol 48: 283-293, 2008.
16. German RZ, Crompton AW. Ontogeny of suckling mechanisms in opossums (Didelphis virginiana). Brain Behav Evol 48: 157-164, 1996.
17. German RZ, Crompton AW, Hertweck DW, Thexton AJ. Determinants of rhythm and rate in suckling. J Exp Zool 278: 1-8, 1997.
18. German RZ, Crompton AW, Levitch LC, Thexton AJ. The mechanism of suckling in two species of infant mammal: miniature pigs and longtailed macaques. J Exp Zool 261: 322-330, 1992.
19. German RZ, Crompton AW, Owerkowicz T, Thexton AJ. Volume and rate of milk delivery as determinants of swallowing in an infant model animal (Sus scrofia). Dysphagia 19: 147-154, 2004.
20. Heaton JT, Kobler JB, Goldstein EA, McMahon TA, Barry DT, Hillman RE. Recurrent laryngeal nerve transposition in guinea pigs. Ann Otol Rhinol Laryngol 109: 972-980, 2000.
21. Herrel A, Schaerlaeken V, Ross C, Meyers J, Nishikawa K, Virginia A, Adriana M, Aerts P. Electromyography and the evolution of motor control: limitations and insights. Integr Comp Biol 48: 261-271, 2008.
22. Herring SW, Scapino RP. Physiology of feeding in miniature pigs. J Morphol 141: 427-460, 1973.
23. Higham TE, Biewener AA, Wakeling JM. Functional diversification within and between muscle synergists during locomotion. Biol Lett 4: 41-44, 2008.
24. Hiiemae KM, Palmer JB, Medicis SW, Hegener H, Jackson BS, Lieberman DE. Hyoid and tongue surface movements in speaking and eating. Arch Oral Biol 47: 267-280, 2002.
25. Hirano M, Koike Y, von Leden H. The sternohyoid muscle during phonation. Electromyographic studies. Acta Otolaryngol 64: 500-507, 1967.
26. Kirzinger A, Jurgens U. Role of extralaryngeal muscles in phonation of subhuman primates. J Comp Physiol [A] 175: 215-222, 1994.
27. Kirzinger A, Jurgens U. Vocalization-correlated single-unit activity in the brain stem of the squirrel monkey. Exp Brain Res 84: 545-560, 1991.
28. Konow N, Camp AL, Sanford CPJ. Congruence between muscle activity and kinematics in a convergently derived prey-processing behavior. Integr Comp Biol 48: 246-260, 2008.
29. Konow N, Sanford CPJ. Is a convergently derived muscle-activity pattern driving novel raking behaviours in teleost fishes? J Exp Biol 211: 989-999, 2008.
30. Laboissiere R, Ostry DJ, Feldman AG. The control of multi-muscle systems: human jaw and hyoid movements. Biol Cybern 74: 373-384, 1996.
31. Lang IM, Dana N, Medda BK, Shaker R. Mechanisms of airway protection during retching, vomiting, and swallowing. Am J Physiol Gastrointest Liver Physiol 283: G529-G536, 2002.
32. Li L, Baum BS. Electromechanical delay estimated by using electromyography during cycling at different pedaling frequencies. J Electromyogr Kinesiol 14: 647-652, 2004.
33. Liu ZJ, Masuda Y, Inoue T, Fuchihata H, Sumida A, Takada K, Morimoto T. Coordination of cortically induced rhythmic jaw and tongue movements in the rabbit. J Neurophysiol 69: 569-584, 1993.
34. Loeb GE, Gans C. Electromyography for Experimentalists. Chicago, IL: Univ. of Chicago Press, 1986, p. P119-P120.
35. Loeb GE, Yee WJ, Pratt CA, Chanaud CM, Richmond FJ. Crosscorrelation of EMG reveals widespread synchronization of motor units during some slow movements in intact cats. J Neurosci Methods 21: 239-249, 1987.
36. Mathew OP. Upper airway negative-pressure effects on respiratory activity of upper airway muscles. J Appl Physiol 56: 500-505, 1984.
37. McFarland DH, Lund JP. An investigation of the coupling between respiration, mastication, and swallowing in the awake rabbit. J Neurophysiol 69: 95-108, 1993.
38. Megirian D, Hinrichsen CF, Sherrey JH. Respiratory roles of genioglossus, sternothyroid, and sternohyoid muscles during sleep. Exp Neurol 90: 118-128, 1985.
39. Palmer JB, Rudin NJ, Lara G, Crompton AW. Coordination of mastication and swallowing. Dysphagia 7: 187-200, 1992.
40. Paniello RC, West SE, Lee P. Laryngeal reinnervation with the hypoglossal nerve. I. Physiology, histochemistry, electromyography, and retrograde labeling in a canine model. Ann Otol Rhinol Laryngol 110: 532-542, 2001.
41. Peker T, Gulekon N, Turgut BH, Anil A, Karakose M, Mungan T, Danisman N. Observation of the relationship between the shape of skeletal muscles and their nerve distribution patterns: a transparent and microanatomic study. Plast Reconstr Surg 117: 165-176, 2006.
42. Roberts JL, Reed WR, Thach BT. Pharyngeal airway-stabilizing function of sternohyoid and sternothyroid muscles in the rabbit. J Appl Physiol 57: 1790-1795, 1984.
43. Roberts TJ, Gabaldon AM. Interpreting muscle function from EMG: lessons learned from direct measurements of muscle force. Integr Comp Biol 48: 312-320, 2008.
44. Roberts TJ, Higginson BK, Nelson FE, Gabaldon AM. Muscle strain is modulated more with running slope than speed in wild turkey knee and hip extensors. J Exp Biol 210: 2510-2517, 2007.
45. Rome LC, Sosnicki AA, Goble DO. Maximum velocity of shortening of three fibre types from horse soleus muscle: implications for scaling with body size. J Physiol 431: 173-185, 1990.
46. Roubeau B, Chevrie-Muller C, Lacau Saint Guily J. Electromyographic activity of strap and cricothyroid muscles in pitch change. Acta Otolaryngol 117: 459-464, 1997.
47. Sack WO. Pig Anatomy and Atlas. Ithaca, NY: Veterinary Textbooks, 1982.
48. Smith KK. The evolution of the mammalian pharynx. Zool J Linn Soc 104: 313-349, 1992.
49. Thexton AJ. A randomisation method for discriminating between signal and noise recordings of rhythmic electromyographic activity. J Neurosci Methods 66: 93-98, 1996.
50. Thexton AJ, Crompton AW, German RZ. Electromyographic activity during the reflex pharyngeal swallow in the pig: Doty and Bosma (1956) revisited. J Appl Physiol 102: 587-600, 2007.
51. Thexton AJ, Crompton AW, German RZ. Transition from suckling to drinking at weaning: a kinematic and electromyographic study in miniature pigs. J Exp Zool 280: 327-343, 1998.
52. Thexton AJ, Crompton AW, Owerkowicz T, German RZ. Impact of rhythmic oral activity on the timing of muscle activation in the swallow of the decerebrate pig. J Neurophysiol 101: 1386-1393, 2009.
53. Thexton AJ, McGarrick JD. The electromyographic activities of jaw and hyoid musculature in different ingestive behaviours in the cat. Arch Oral Biol 39: 599-612, 1994.
54. Toniolo L, Patruno M, Maccatrozzo L, Pellegrino MA, Canepari M, Rossi R, D'Antona G, Bottinelli R, Reggiani C, Mascarello F. Fast fibres in a large animal: fibre types, contractile properties and myosin expression in pig skeletal muscles. J Exp Biol 207: 1875-1886, 2004.
55. Uchida K, Yamada Y, Sato T. The coordination of rhythmical drinking behavior with swallowing in rabbits. Physiol Behav 55: 795-801, 1994.
56. Van de Graaff WB, Gottfried SB, Mitra J, van Lunteren E, Cherniack NS, Strohl KP. Respiratory function of hyoid muscles and hyoid arch. J Appl Physiol 57: 197-204, 1984.
57. van Lunteren E, Dick TE. Heterogeneity within geniohyoid motor unit subpopulations in firing patterns during breathing. Respir Physiol 124: 23-33, 2001.
58. van Lunteren E, Haxhiu MA, Cherniack NS. Effects of tracheal airway occlusion on hyoid muscle length and upper airway volume. J Appl Physiol 67: 2296-2302, 1989.
59. van Lunteren E, Haxhiu MA, Cherniack NS. Mechanical function of hyoid muscles during spontaneous breathing in cats. J Appl Physiol 62: 582-590, 1987.
60. van Lunteren E, Haxhiu MA, Cherniack NS. Relation between upper airway volume and hyoid muscle length. J Appl Physiol 63: 1443-1449, 1987.
61. van Lunteren E, Manubay P. Contractile properties of feline genioglossus, sternohyoid, and sternothyroid muscles. J Appl Physiol 72: 1010- 1015, 1992.
62. van Lunteren E, Martin RJ. Pharyngeal dilator muscle contractile and endurance properties in neonatal piglets. Respir Physiol 92: 65-75, 1993.
63. van Lunteren E, Salomone RJ, Manubay P, Supinski GS, Dick TE. Contractile and endurance properties of geniohyoid and diaphragm muscles. J Appl Physiol 69: 1992-1997, 1990.
64. van Lunteren E, Vafaie H, Salomone RJ. Comparative effects of aging on pharyngeal and diaphragm muscles. Respir Physiol 99: 113-125, 1995.
65. Van Wassenbergh S, Herrel A, Adriaens D, Aerts P. Interspecific variation in sternohyoideus muscle morphology in clariid catfishes: functional implications for suction feeding. J Morphol 268: 232-242, 2007.
66. Westneat MW, Hall WG. Ontogeny of feeding motor patterns in infant rats: an electromyographic analysis of suckling and chewing. Behav Neurosci 106: 539-554, 1992.
67. Wren TAL, Patrick Do K, Rethlefsen SA, Healy B. Cross-correlation as a method for comparing dynamic electromyography signals during gait. J Biomech 39: 2714-2718, 2006.
68. Zhou S, Lawson DL, Morrison WE, Fairweather I. Electromechanical delay in isometric muscle contractions evoked by voluntary, reflex and electrical stimulation. Eur J Appl Physiol 70: 138-145, 1995.