Slow tonic muscle fibers in the thyroarytenoid muscles of human vocal folds; a possible specialization for speech

Anatomical Record

Volumn 256, Issue 2, 1999, Pages 146-157

  Han, Yingshi ^a   Wang, Jun ^a   Fischman, Donald A ^b   Biller, Hugh F ^a   Sanders, Ira ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Larynx; Phonation; Slow tonic myosin heavy chain isoform; Speech; Thyroarytenoid muscle; Voice

Indexed keywords

ADULT; AGED; ARTICLE; BIOMECHANICS; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; MALE; PHONATION; PRIORITY JOURNAL; SLOW MUSCLE FIBER; SPEECH; THYROARYTENOID MUSCLE; VOCAL CORD; VOICE;

ADULT; AGED; ANIMALS; ANTIBODIES, MONOCLONAL; ARYTENOID CARTILAGE; BIOMECHANICS; FEMALE; GENE EXPRESSION; HUMANS; MALE; MAMMALS; MICE; MICROSCOPY, FLUORESCENCE; MIDDLE AGED; MUSCLE CONTRACTION; MUSCLE FIBERS, SLOW-TWITCH; MYOSIN HEAVY CHAINS; PROTEIN ISOFORMS; SPEECH; VOCAL CORDS;

MAMMALIA; PRIMATES;

EID: 0033215209     PISSN: 0003276X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0185(19991001)256:2<146::AID-AR5>3.0.CO;2-8     Document Type: Article

References (98)

1. Alway SE. 1993. Stretch induces non-uniform isomyosin expression in the quail anterior latissimus dorsi muscle. Anat Rec 237:1-7.
2. Ashmore CR, Kikuchi T, Doerr L. 1978. Some observations on the innervation patterns of different fiber types of chick muscle. Exp Neurol 58:272-281.
3. Ausoni S, Gorza L, Schiaffino S, Gundersen K, Lomo T. 1990. Expression of myosin heavy chain isoforms in stimulated fast and slow rat muscles. J Neurosci 10:153-160.
4. Bader D, Masaki T, Fischman DA. 1982. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J Cell Biol 95:763-770.
5. Barker D. 1974. The morphology of muscle receptors. In: C.C. Hunt, editor. Handbook of sensory physiology. Vol III/2. New York: Springer-Verlag, pp 1-190.
6. Beermann DH, Cassens RG. 1976. A combined silver and acetyl cholinesterase method for staining intramuscular innervation. Stain Technol 51:173-177.
7. Bendiksen FS, Dahl HA, Teig E. 1981. Innervation pattern of different types of muscle fibers in the human thyroarytenoid muscle. Acta Otolaryngol 91:391-397,
8. Bollag DM, Rozycki MD, Edelstein SJ, editor. 1996. Protein Methods. New York: Wiley-Liss Inc., pp 107-134, 195-212.
9. Bondi AY, Chiarandini DJ. 1988. Morphologic and electrophysiologic identification of multiply innervated fibers in rat extra-ocular muscles. Invest Ophthalmol & Vis Sci 24:516-519.
10. Boyd IA. 1980. The isolated mammalian muscle spindle. Trends Neurosci 3:258.
11. Bradford MM. 1976. Arapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
12. Cheng K, Breinin GM. 1966. A comparison of the fine structure of extraocular and interosseus muscles in the monkey. Invest Ophthalmol 5:535-549.
13. Durrant I, Fowler S. 1994. Chemiluminescent detection system for protein blotting. In: Dunbar BS, editor. Protein blotting. A practical approach. New York: IRL Press at Oxford University Press.
14. Eriksson P, Butler-Browne GS, Thornell L. 1994. Immunohistochemical characterization of human masseter muscle spindles. Muscle & Nerve 17:31-41.
15. Erulkar SD, Shelanski ML, Whitsel BL, Ogle P. 1964. Studies of muscle fibers of the tensor tympani of the cat. Anat Rec 149:279-298.
16. Fant G. 1978. Laryngeal mechanisms and features. Phonetica 34:252-255.
17. Fernand VSV, Hess A. 1969. The occurrence, structure and innervation of slow and twitch muscle fibers in the tensor tympani and stapedius of the cat. J Physiol 200:547-554.
18. Franzini-Armstrong C. 1984. Freeze fracture of frog slow tonic fibers. Structure of surface and internal membranes. Tissue Cell 16:647-664.
19. Gonzalez-Sanchez A, Bader D. 1985. Characterization of a myosin heavy chain in the conductive system of the adult and developing chicken heart. J Cell Biol 100:270-275.
20. Gunning P, Hardeman E. 1991. Multiple mechanisms regulate muscle fiber diversity. FASEB J 5:3064-3070.
21. Harker DW. 1972. The structure and innervation of sheep superior rectus and levator palpebrae extra-ocular muscles. I. Extrafusal muscle fibers. Invest Ophthalmol 11:956-969.
22. Hess A, Pilar G. 1963. Slow fibers in the extra-ocular muscles of the cat. J Physiol 169:780-798.
23. Hess A. 1970. Vertebrate slow muscle fibers. Physiol Reviews 50: 40-62.
24. Hikida RS. 1987. Quantitative ultrastructure of histochemically identified avian skeletal muscle fiber types. Anat Rec 218:128-135.
25. Hikida RS, Bock WL. 1974. Analysis of fiber types in the pigeon's metapatagialis muscle. 1, Histochemistry, end plates and ultrastructure. Tissue Cell 6:411-430.
26. Ishizaka K, Flanagan JF. 1972. Synthesis of voooooice sound from the two mass model of the vocal cord. Bell, Syst. Tech J 51:1233-1267.
27. Izumo S, Nadal-Ginard B, Mahdavi V. 1986. All members of the MHC multigene family respond to thyroid hormone in a high tissue-specific manner. Science 231:597-600.
28. Jung HH, Lieber RL, Ryan AF. 1998. Quantification of myosin heavy chain mRNA in somatic and branchial arch muscles using competitive PCR. Am J Physiol 275 (Cell Physiol. 44): C68-74.
29. Kennedy JM., Kamel S, Tambone WW, Vrbova G, Zak R. 1986. The expression of myosin heavy chain isoforms in normal and hypertrophied chicken slow muscle. J Cell Biol 103:977-983.
30. Kennedy JM, Eisenberg BR, Reid SK, Sweeney LJ, Zak R. 1988. Nascent muscle fiber appearance in overloaded chicken slow tonic muscle. Am J Anat 181:203-215.
31. Kennedy JM, Zak R, Gao L. 1991. Myosin expression in hypertrophied fast twitch and slow tonic muscles of normal and dystrophic chickens. Muscle & Nerve 14:166-177.
32. Koike Y, Nunomura S. 1987. A histochemical study of the composition of myosin and the metabolic enzyme activities in human thyroarytenoid muscle. In: Hirano M, Kirchhner JA, Bless DM, editors. Neurolaryngology. Recent advances. A College-Hill Publication, Little, Brown and Company Boston/Toronto/San Diego.
33. Konig WF, Leden HV. 1961. The peripheral nervous system of the human larynx. Part II: The thyroarytenoid (vocalis) muscle. Arch Otol 74:153-163.
34. Kucera J, Walro JM. 1989a. Non-uniform expression of myosin heavy chain isoforms along the length of cat intrafusal muscle fibers. Histochemistry. 92:291-299.
35. Kucera J, Walro JM. 1989b. Postnatal expression of myosin heavy chains in muscle spindles of the rat. Anat & Embryol (Berl) 179:369-376.
36. Kucera J, Walro JM. 1993. Transient expression of a slow-tonic MHC isoform by extrafusal fibers in the developing rat. Anat Embryol (Berl) 188:409-418.
37. Kucera J, Walro JM, Gorza L. 1992. Expression of type-specific MHC isoforms in rat intrafusal muscle fibers. J Histochem Cytochem 40:293-307.
38. Kuffler SW Williams EMV. 1953. Properties of the slow skeletal muscle fibers of the frog. J Physiol (Lond.) 121:318-340.
39. Kuyper HGJM. 1958a. Corticobulbar connections to the pons and lower brain-stem in man. Brain 81:364-388.
40. Kuyper HGJM. 1958b. Some projections from the peri-central cortex to the pons and lower brain stem in monkey and chimpanzee. J. Comp Neurol 110:221-256.
41. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
42. Lannergren J. 1987. Contractile properties and myosin isoforms of various kinds of Xenopus twitch muscle fibers J Muscle Res Cell Motil 8:260-273.
43. Leinwand LA, Fournier REK, Nadal-Ginard B, Shows TB. 1983. Multigene family for sarcomeric myosin heavy chain in mouse and human DNA: location on a single chromosome. Science 221:766-769.
44. Liden G, Nordlund B, Hawkins JE. 1964. Significance of the stapedius reflex for the understanding of speech. Acta Otolaryngol. (Stockh) Suppl. 188:275-279.
45. Loughna PT, Izumo S, Goldspink G, Nadal-Ginard B. 1990. Disuse and passive stretch cause rapid alterations in expression of developmental and adult contractile protein genes in skeletal muscle. Development 109:217-223.
46. Lucas CA, Rughani A, Hoh JFY. 1995. Expression of extraocular myosin heavy chain in rabbit laryngeal muscle. J Muscle Res Cell Motil 16:368-78.
47. Lundell MJ, Hirsh J. 1994. A new visible light DNA fluorochrome for confocal microscope. Bio Tech 16:434-440.
48. Mahdavi V, Chambers AP, Nadal-Ginard B. 1984. Cardiac - and -myosin heavy chain genes are organized in tandem. Proc Natl Acad Sci USA 81:2626-2630.
49. Maier A. Differences in muscle spindle structure between pigeon muscles used in aerial and terrestrial locomotion. Am J Anat 168:27-36.
50. Maier A. 1994. Type and regional diversity in the distribution of myosin heavy chains in chicken intrafusal muscle fibers. Anat Rec 240:507-515.
51. Mascarello F, Carpene E, Veggetti A, Rowlerson A, Jenny E. 1982. The tensor tympani muscle of cat and dog contains IIM and slow tonic fibers: an unusual combination of fibre types. J Muscle Res Cell Motil 3:363-374.
52. Mascarello F, Rowlerson AM. 1992. Myosin isoform transitions during development of extra-ocular and masticatory muscles in the fetal rat. Anat Embryol Berl 185:143-153.
53. Mascarello F, Veggetti A, Carpene E, Rowlerson A. 1983. An immunohistochemical study of the middle ear muscles of some carnivores and primates, with special reference to the IIM and slow-tonic fibre types. J Anat 137:95-108.
54. Matsuda R, Bandman E, Strohman RC. 1982. The two myosin heavy chain encoded by separated mRNA. Differentiation 23:36-42.
55. Mayr R. 1971. Structure and distribution of fiber types in external eye muscles of the rat. Tissue & Cell 3:433-462.
56. McVean A, Stelling J, Rowlerson A. 1987. Muscle fibre types in the external eye muscles of the pigeon, Columba livia J Anat 154:91-101.
57. Merati AL, Bodine SC, Bennett T, Jung HH, Furuta H, Ryan AF. 1996. Identification of a novel myosin heavy chain gene expressed in the rat larynx. Biochim Biophys Acta 1306:153-159.
58. Miller JE. 1967. Cellular organization of rhesus extra-ocular muscle. Invest Ophthalmol 6:18-39.
59. Morgan DL, Proske U. 1984. Vertebrate slow muscle: I structure, pattern of innervation and mechanical properties. Physiol. Reviews 64:103-168.
60. Morris LG, Hooper SL. 1998. Muscle response to changing neuronal input in the lobster (Panulirus interruptus) stomatogastric system: slow muscle properties can transform rhythmic input into tonic output J Neurosci 18:3433-3442.
61. Oda K. 1984. Age changes of motor innervation and acetylcholine receptor distribution on human skeletal muscle fibers. J Neurol Sci 66:327-338.
62. Olkowski Z, Manocha SL. 1973. Muscle spindle. In: Bourne GH, editors. The structure and function of muscle. New York: Academic Press, pp 365-482.
63. Ovalle WK. 1978. Histochemical dichotomy of extrafusal and intrafusal fibers in an avian slow muscle. Am J Anat 152:587-598.
64. Ovalle WK. 1982. Ultrastructural duality of extrafusal fibers in a slow (tonic) skeletal muscle. Cell Tissue Res 222:261-267.
65. Pachter BR. 1982. Fiber composition of the superior rectus extraocular muscle of the Rhesus Macaque. J Morphol 174:237-250.
66. Pachter BR. 1983. Rat extraocular muscle 1. Three dimensional cytoarchitecture, component fibre populations and innervation. J Anat 137:143-159.
67. Pedrosa F, Butler-Browne GS, Dhoot GK, Fischman DA, Thornell LE. 1989. Diversity in expression of myosin heavy chain isoforms and M-band proteins in rat muscle spindles. Histochemistry 92:185-194.
68. Pedrosa-Domellof F, Thornell LE. 1994. Expression of myosin heavy chain isoforms in developing humam muscle spindles. J Histochem Cytochem 42:77-88.
69. Pette D, Vrbova G. 1985. Invited review: neural control of phenotypic expression in mammalian muscle fibers. Muscle & Nerve 8:676-689.
70. Pierobon-Bormioli S, Sartore S, Vitadello M, Schiaffino S. 1980. "Slow" myosin in vertebrate skeletal muscle. An immunofluorescence study. J Cell Biol 85:672-681.
71. Pierobon-Bormioli S, Torresan P, Sartore S, Moschini GB, Schiaffino S. 1979. Immunohistochemical identification of slow-tonic fibers in human extrinsic eye muscles. Invest. Ophthalmol. Visual Sci 18: 303-306.
72. Pliszka B, Strzelecka-Golaszewska H. 1981. Comparison of myosin isoenzymes from slow tonic and fast-twitch fibers of frog muscle. Eur J Cell Biol 25:144-149.
73. Reiser PJ, Moss RL, Giulian GG, Greaser L. 1985. Shortening velocity in single fiber from adult rabbit soleus muscle is correlated with myosin heavy chain composition. J Biol Chem 266:9077-9080.
74. Rosser BWC, George JC. 1984. Some histochemical properties of the fiber types in the pectoralis muscle of an emu (Dromaius novaehollandiae). Anat Rec 209:301-305.
75. Rosser BWC, George J. 1985. An exceptionally high density of muscle spindles in a slow tonic pigeon muscle. Anat Rec 212:118-122
76. Rossi G, Cortesina G. 1965. Multi-motor end-plate muscle fibres in the human vocalis muscle. Nature 206:629-630.
77. Saez LJ, Gianola KM, McNally E, Feghali R, Eddy R, Shows T, Leinwand L. 1987. Human cardiac myosin heavy chain genes and their linkage in the genome. Nucleic Acid Res 15:5443-5459.
78. Sanders I, Han Y, Wang J, Biller HF. 1998a. Muscle spindles are concentrated in the superior vocalis sub-compartment of the human thyroarytenoid muscle. J Voice 12:7-16.
79. Sanders I, Wu BL, Biller HF. 1994. Phonatory specializations of human laryngeal muscles (abstract). Trans Am Laryngol Assoc 115:153.
80. Sanders I, Rai S, Han Y, Biller HF. 1998b. Human vocalis contains distinct superior and inferior subcompartments: possible candidates for the two masses of vocal fold vibration. Otol Rhinol Laryngol 107:826-833.
81. Sartore S, Mascarello F, Rowlerson A, Gorza L, Ausoni S, Vianello M, Schiaffino S. 1987. Fiber types in extraocular muscles: A new myosin isoform in the fast fibers. J Muscle Res Motil. 8:161-170.
82. Scapolo PA, Costerbosa GL, Barazzoni AM, Lucchi ML, Bortolami R. 1990. An immunohistochemical approach to the intrafusal fibres of extraocular muscle spindles in sheep, cow, and pig. Anat Rec 227:314-320.
83. Schiaffino S, Reggiani C. 1994. Myosin isoforms in mammalian skeletal muscle. J Appl Physiol 77:493-501.
84. Shafiq SA, Shimizu T, Fischman DA. 1984. Heterogeneity of type I skeletal muscle fibers revealed by monoclonal antibody to slow myosin. Muscle & Nerve 7:380-387.
85. Simpson S. 1979. The distribution of tonic and twitch muscle fibers in the avian wing. Am. Zoologist 19:929.
86. Sonesson B. 1960. On the anatomy and vibratory pattern of the human vocal folds. With special reference to a photo-electrical method for studying the vibratory movement. Acta Otolaryngol Suppl. 156.
87. Soukup T, Pedrosa-Domellof F, Thornell LE. 1995. Expression of myosin heavy chain isoforms and myogenesis of intrafusal fibres in rat muscle spindles. Microsc Res Tech 30:390-407.
88. Teig E. 1973. Differential effect of graded contraction of middle ear muscles on the sound transmission of the ear. Acta Physiol Scand 88:382-391.
89. Termin A, Staron RS, Pette D. 1989. Changes in myosin heavy chain isoforms during chronic low-frequency stimulation of rat fast hind-limb muscles. A single-fiber study. Eur. J Biochem 186:749-754.
90. Thornell LE, Eriksson PO, Fischman DA, Grove BK, Butler-Browne GS, Virtanen I. 1988. Human muscle spindle development. In: Hnik P, Soukup T, Vejsada R and Zelena J, editors. Mechanoreceptors, development, structure and function. New York: Plenum Press, p. 39
91. Van den Berg J. 1958. Myoelastic-aerodyanmic theory of voice production. J. Speech Hear Res 1:227-243.
92. Walro JM, Wang J, Story GM. 1997. Afferent-inherent regulation of myosin heavy chain isoforms in rat muscle spindles. Muscle & Nerve 20:1549-1560.
93. Wang J, Han Y, Sanders I. 1998. The superior vocalis of the human thyroarytenoid muscle contains a specialized and possibly unique muscle fiber architecture. Bulletin Am Academy of Otolaryngol-Head Neck Surgery 17:49.
94. Weydert A, Daubas P, Lazaridis I, Barton P, Garner I, Leader D, Bonhomme F, Catalan J, Simon D, Guenet J, Gros F, Buckingham M. 1985. Genes for skeletal muscle myosin heavy chains are clustered and are not located on the same mouse chromosome as a cardiac myosin heavy chain gene. Proc Natl Acad Sci USA 82:7183-7187.
95. Yoshimura A, Fujitsuka N, Sokabe M, Naruse K, Nomura K, Diwan FH, Ito F. 1990. Classification of the intrafusal muscle fibres in the frog muscle spindle: histochemical and immunofluorescent studies. J Anat 172:89-101.
96. Zadeh BJ, Gonzalez-Sanchez A, Fischman DA, Bader DM. 1986. Myosin heavy chain expression in embryonic cardiac cell cultures. Develop Biol 115:204-214.
97. Zhang Y, Rushbrook JI, Shafiq SA. 1985. Avian adductor profundus muscle: characterization of a pure slow tonic region by histochemical, monoclonal antibody and peptide mapping studies. J Muscle Res Cell Motil 6:333-345.
98. Zhang Y, Shafig SA, Bader D. 1986. Detection of a ventricular-specific myosin heavy chain in adult and developing chicken heart. J Cell Biol 102:1480-1484.