Summary
The contractile, histochemical, morphological and electrophysiological properties of two rat laryngeal muscles, the cricothyroid and posterior cricoarytenoid, have been measured. Both muscles act during respiration to maintain upper airway patency and an even distribution of air in the lungs. The cricothyroid and posterior cricoarytenoid are fast-twitch muscles, having contraction times of 3.4 and 7.2 ms respectively, high myosin ATPase activity, abundant sarcoplasmic reticulum (with average volumes of 9% and 15%, respectively, of the fibre volume) and T-system membrane (with average areas of 0.4 and 0.5 µm2 µ−3 of fibre). The large areas of T-tubule membrane are reflected in the average specific membrane capacities of 6.5 µF cm−2 to 10.5 µF cm−2, which are high considering the small diameter of the fibres (20–30 µm). Of the two muscles, the posterior cricoarytenoid has the faster contraction time and the more abundant sarcoplasmic reticulum content. In addition, the posterior cricoarytenoid is less resistant to fatigue and demonstrates lower succinic dehydrogenase activity. The fatigability of this muscle, coupled with its general lack of functional reserve, suggest that its failure may contribute to upper airway obstruction during respiratory distress.
Similar content being viewed by others
References
ADRIAN, R. H. & ALMERS, W. (1974) Membrane capacity measurements on frog skeletal muscle in media of low ion content.J. Physiol. 237, 573–605.
BACH-Y-RITA, P. & ITO, F. (1966)In vivo studies on fast and slow muscle fibres in cat extraocular muscles.J. gen. Physiol. 49, 1177–98.
BARILLOT, J. C. & BIANCHI, A. L. (1971) Activité des motoneurones laryngés pendant les réflexes de Hering-Breuer.J. Physiol. 63, 783–92.
BARILLOT, J. C. & DUSSARDIER, M. (1973) Modalités de décharge des motoneurones laryngés inspiratoires dans diverses conditions experimentales.J. Physiol. 66, 593–629.
BERENDES, J. & VOGELL, W. (1960) Laryngeal muscles in the electron microscope picture.Arch. Ohr Nas Kehlkopfheclk 176, 730–5.
BURKE, R. E. & EDGERTON, V. R. (1975) Motor unit properties and selective involvement in movement.Exercise Sports Sci. Rev. 3, 31–81.
CAMPBELL, E. J. M. & NEWSOME-DAVIS, J. (1970) Muscles of the larynx and thyroid cartilage. InThe Respiratory Muscles (edited by CAMPBELL, E. J. M., AGOSTONI, E. and NEWSOME-DAVIS, J.), pp. 194–204, London: Lloyd-Luke Ltd.
CLOSE, R. I. (1972) Dynamic properties of mammalian skeletal muscles.Physiol. Rev. 52, 129–97.
DAVEY, D. F., DULHUNTY, A. F. & FATKIN, D. (1980) Glycerol treatment in mammalian skeletal muscle.J. membr. Biol. 53, 223–33.
DAVEY, D. F., DUNLOP, C., HOH, J. Y. F. & WONG, S. Y. P. (1981) Contractile properties and ultrastructure of extensor digitorum longus and soleus muscles in spinal chord transected rats.Aust. J. exp. Biol. Med. Sci. 59, 393–404.
DAVEY, D. F. & O'BRIEN, G. M. (1978) The sarcoplasmic reticulum and T-system of rat extensor digitorum longus muscles exposed to hypertonic solutions.Aust. J. exp. Biol. Med. Sci. 56, 409–19.
DAVEY, D. F. & WONG, S. Y. P. (1980) Morphometric analysis of rat extensor digitorum longus and soleus muscles.Aust. J. exp. Biol. Med. Sci. 58, 213–30.
DUCHEN, L. W. (1971) An electron microscope comparison of motor end plates of slow and fast skeletal muscle fibres of the mouse.J. Neurol. Sci. 14, 37–45.
DULHUNTY, A. F. (1979) Electrical and mechanical properties of dystrophic C57BL mouse muscle. InNerve Muscle and Brain Degeneration (edited by KIDMAN, A. D. and TOMPKINS, J. K.), Vol. 473, pp. 153–166. Amsterdam: Excerpta Medica.
DULHUNTY, A. F. (1980) Potassium contractures and mechanical activation in mammalian skeletal muscle.J. membr. Biol. 57, 223–33.
DULHUNTY, A. F. & DLUTOWSKI, M. (1979) Fiber types in red and white segments of rat sternomastoid muscle.Am. J. Anat. 156, 51–61.
DULHUNTY, A. F. & FRANZINI-ARMSTRONG, C. (1977) The passive electrical properties of frog skeletal muscle fibres at different sarcomere lengths.J. Physiol. 266, 687–711.
EDSTRÖM, L. & LINDQUIST, C. (1973) Histochemical fibre composition of some facial muscles in the cat in relation to their contraction properties.Acta physiol. scand. 89, 491–503.
EDSTRÖM, L., LINDQUIST, C. & MARTENSSON, A. (1974) InVentilatory and Phonatory Control Systems (edited by WYKE, B.), pp. 392–407. Oxford: Oxford University Press.
EISENBERG, B. & KUDA, A. M. (1975) Stereological analysis of mammalian skeletal muscle. II. White vastus muscle of the adult guinea pig.J. Ultrastruct. Res. 51, 176–87.
EISENBERG, B. & KUDA, A. M. (1976) Discrimination between fibre populations in mammalian skeletal muscle by using ultrastructural parameters.J. Ultrastruct. Res. 54, 76–88.
EISENBERG, B., KUDA, A. M. & PETER, J. B. (1974) Stereological analysis of mammalian skeletal muscle. I. Soleus muscle of the adult guinea pig.J. Cell Biol. 60, 732–54.
EISENBERG, B. & MOBLEY, B. A. (1975) Size changes in single muscle fibres during fixation and embedding.Tiss. Cell 7, 383–7.
ELLISMAN, M. H., RASH, J. E., STAEHELIN, L. A. & PORTER, K. R. (1976) Studies of excitable membranes. II. A comparison of specialisations at neuromuscular junctions and nonjunctional sarcolemmas of mammalian fast and slow twitch muscle fibres.J. Cell Biol. 68, 752–74.
FATT, P. & KATZ, B. (1951) Analysis of end plate potential recorded with intracellular electrode.J. Physiol. 115, 320–70.
FAWCETT, D. W. & REVEL, J. P. (1961) The sarcoplasmic reticulum of a fast-acting fish muscle.J. Biophys. Biochem. Cytol. 10, 89–109.
FINK, B. R. (1975)The Human Larynx. pp. 53–84. New York: Raven Press.
FRANZINI-ARMSTRONG, C. (1974) Membrane systems in muscle fibres. InThe Structure and Function of Muscle, Vol. 2 (edited by BOURNE, E.), pp. 532–613. London, New York: Academic Press.
FUKUDA, H., SASAKI, C. T. & KIRCHNER, J. A. (1973) Vagal afferent influences on the phasic activity of the posterior cricoarytenoid muscle.Acta otolaryngol. 75, 112–8.
GAGE, P. W. & EISENBERG, R. S. (1969) Capacitance of the surface and transverse tubular membrane of frog sartorius muscle fibres.J. gen. Physiol. 53, 265–77.
GAUTHIER, G. F. (1974) Some ultrastructural and cytochemical features of fibre populations in the soleus muscle.Anat. Rec. 180, 551–63.
GAUTHIER, G. F. & PADYKULA, H. A. (1966) Cytological studies of fibre types in skeletal muscle. A comparative study of the mammalian diaphragm.J. Cell Biol. 28, 333–54.
GOLDSPINK, G. (1971) Changes in striated muscle fibres during contraction and growth with particular reference to myofibril splitting.J. Cell. Sci. 9, 123–37.
GOLDSTEIN, M. A. (1969) A morphological and cytochemical study of sarcoplasmic reticulum and T-system of fish extraocular muscle.Z. Zellforsch. 102, 31–9.
GUILLEMINAULT, C. & DEMENT, W. C. (1978) (editors)Sleep Apnea Syndromes. p. 130 New York: Alan Liss.
HALL-CRAGGS, E. C. B. (1968) The contraction times and enzyme activity of two rabbit laryngeal muscles.J. Anat. 102, 241–55.
HAST, M. H. (1966) Mechanical properties of the cricothyroid muscle.Laryngoscope 76, 537–48.
HAST, M. H. (1967a) Mechanical properties of the vocal fold muscle.Pract. oto-rhino-laryng. 29, 53–6.
HAST, M. H. (1967b) The respiratory muscle of the larynx.Ann. Otol. Rhinol. Laryngol. 76, 489–97.
HIROSE, H., USHIJIMA, T., KOBAYASH, T. & SAWASHUM, M. (1969) An experimental study of the contraction properties of the laryngeal muscles in the cat.Ann. Otol. Rhinol. Laryngol. 78, 297–306.
HODGKIN, A. L. & NAKAJIMA, S. (1972) Analysis of the membrane capacity in frog muscle.J. Physiol. 221, 121–36.
HODGKIN, A. L. & RUSHTON, W. A. H. (1946) The electrical constants of a crustacean nerve fibre.Proc. R. Soc. 153, 444–79.
HORIUCHI, M. & SASAKI, C. T. (1978) Cricothyroid muscle in respiration.Ann. Otol. Rhinol. Laryngol. 87, 386–91.
KARLSSON, U. & SCHULTZ, R. L. (1965) Fixation of the central nervous system from electron microscopy by aldehyde perfusion. I. Preservation with aldehyde perfusates versus direct perfusion with osmium tetrachloride with special reference to membranes and the extracellular space.J. Ultrastruct. Res. 12, 160–86.
KHAN, M. A., PAPADIMITRIOU, J. M., HOLT, P. G & KAKULAS, B. A. (1972) A calcium-citro-phosphate technique for the histochemical localization of myosin ATPase.Stain Technol. 47, 277–81.
KILARSKI, W. (1967) The fine structure of straited muscles in teleosts.Z. Zellforsch. 79, 562–80.
KILARSKI, W. & BAGAJ, J. (1969) Organisation and fine structure of extraocular muscles in Carissius and Rana.Z. Zellforsch. 94, 194–204.
KONRAD, H. R. & RATTENBORG, C. C. (1969) Combined action of laryngeal muscles.Acta otolaryngol. 67, 646–9.
KOTBY, M. N. & HAUGEN, L. K. (1970) Critical evaluation of the action of the posterior crico-arytenoid muscle, utilizing direct EMG-study.Acta otolaryngol. 70, 260–8.
LANDON, D. N. (1970) The influence of fixation upon the fine structure of the Z-disk of rat striated muscle.J. Cell Sci. 6, 257–76.
LINDQUIST, C. (1973) Contraction properties of cat facial muscles.Acta physiol. scand. 89, 482–90.
LOO, D. & VAUGHAN, P. C. (1976) Muscle fibre capacity in low conductivity solution.Can. J. Physiol. Pharmacol. 54, 107–12.
LUFF, A. & ATWOOD, H. L. (1972) Membrane properties and contraction of single muscle fibers in the mouse.Am. J. Physiol. 222, 1435–40.
MARTENSSON, A. (1968) The functional organisation of the intrinsic laryngeal muscles.Ann. N.Y. Acad. Sci. 155, 91–7.
MARTENSSON, A. & SKOGLUND, C. R. (1964) Contraction properties of intrinsic laryngeal muscles.Acta physiol. scand. 60, 318–36.
NACHLAS, M. M., KWAN-CHUNG, T., DE ZOUZA, E., CHAO-SHING, C. & SELIGMAN, A. M. (1957) Cytochemical demonstration of succinic dehydrogenase by the use of a newp-nitrophenyl substituted ditetrazole.J. Histochem. Cytochem. 5, 420–37.
PADYKULA, H. A. & GAUTHIER, G. F. (1970) The ultrastructure of the neuromuscular junctions of mammalian red, white and intermediate skeletal muscle fibers.J. Cell Biol. 46, 27–41.
PEACHEY, L. D. & SCHILD, R. F. (1968) The distribution of the T-system along the sarcomeres of frog and toad sartorius muscles.J. Physiol. 194, 249–58.
REGER, J. F. (1961) The fine structure of neuromuscular junctions and the sarcoplasmic reticulum of extrinsic eye muscles ofFundulus heteroclitus.J. Biophys. Biochem. Cytol. 10, Suppl., 111–21.
REVEL, J. P. (1962) The sarcoplasmic reticulum of the bat cricothyroid muscle.J. Cell Biol. 12, 571–88.
ROSSI, G., SARTORIS, A., RAVIZZA, L., URCINDI, R. & FRA, R. (1962) The effects of a rapidly eliminated barbiturate [5-(1-methylbutyl)-5-ethyl-2-thiobarbituric acid sodium salt],d-tubocurarine and succinylcholine chloride on the laryngeal intrinsic musculature. Experimental electromyographic research.Minerva Otorinolaryng. 12, 236–40.
RUDOMIN, P. (1966) The electrical activity of the cricothyroid muscles of the cat.Arch. Int. Physiol. 74, 135–53.
RUSKELL, G. L. (1978) The fine structure of innervated myotendinous cylinders in extraocular muscles of rhesus monkeys.J. Neurocytol. 7, 693–708.
SEYMOUR, J. C. & HENRY, H. S. (1954) Some experimental observations on innervation of larynx in cats.J. Laryngol. Otol. 68, 225–8.
SHERREY, J. H. & MEGIRIAN, D. (1977) State dependence of upper airway respiratory motoneurons: functions of the cricothyroid and nasolabial muscles of the unanaesthetized rat.Electroenceph. clin. Neurophysiol. 43, 218–28.
SHERREY, J. H. & MEGIRIAN, D. (1980) Respiratory EMG activity of the posterior cricoarytenoid, cricothyroid and diaphragm muscles during sleep.Resp. Physiol. 39, 355–65.
SUZUKI, M., KIRCHNER, J. A. & MURAKAMI, Y. (1970) The cricothyroid as a respiratory muscle. Its characteristics in bilateral recuttent laryngeal nerve paralysis.Ann. Otol. Rhinol. Laryngol. 79, 976–83.
VENABLE, J. H. & COGGESHALL, R. (1965) A simplified lead citrate stain for use in electron microscopy.J. Cell Biol. 25, 407–8.
WEIBEL, E. R. (1972) A stereological method for estimating volume and surface of sarcoplasmic reticulum.J. Microscopy 95, 229–42.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hinrichsen, C., Dulhunty, A. The contractile properties, histochemistry, ultrastructure and electrophysiology of the cricothyroid and posterior cricoarytenoid muscles in the rat. J Muscle Res Cell Motil 3, 169–190 (1982). https://doi.org/10.1007/BF00711941
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00711941