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Correlation of electrophysiological, histochemical, and mechanical properties in fibres of the coxa rotator muscle of the locust, Locusta migratoria

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Summary

The fibre composition of the anterior coxa rotator muscle of the locust middle leg (M92) was examined. The muscle is composed of 90–100 fibres. Muscle fibres were characterized with regard to innervation pattern, electrophysiological properties, and morphological parameters. Activity and isoenzyme composition of myofibrillar ATPase, succinic acid dehydrogenase (SDH) activity and glycogen content were examined employing histochemical techniques. Shortening velocity and the dependence of tension on intracellular Ca2+ were determined in skinned fibre experiments. A close match was observed between the innervation pattern of the muscle fibres and their histochemical and physiological properties. The combination of all parameters examined allowed an accurate classification of the muscle fibres into three types. Within a given type, broad variability of some properties was observed (SDH activity, Ca2+ sensitivity) while others assumed distinct values (innervation pattern, shortening velocity). The comprehensive characterization of muscle fibre properties permits a functional interpretation of fibre heterogeneity with regard to muscle performance. Fibres with the same innervation pattern may be recruited specifically, according to their electric properties and Ca2+ sensitivities. The resulting specific recruitment of fibres with different mechanical responses should allow a subtle control of muscular force, with regard to force amplitude, temporal characteristics of contraction, and metabolic cost.

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Abbreviations

CI1 :

common inhibitory neurone one

ejp:

ijp excitatory, inhibitory junctional potential

EGTA:

ethylene glycol-bis[β-aminoethyl ether] N,N,N′,N′-tetraacetic acid

mATPase:

myofibrillar adenosinetriphosphatase

MOPSO:

3-[N-morpholino]-2-hydroxypropanesulfonic acid

M92:

anterior rotator muscle of the coxa

n:

Hill coefficient

pCa50 :

pCa corresponding to half-maximal tension

P0 :

maximal isometric tension

SDH:

succinic acid dehydrogenase

V max :

maximal shortening velocity

References

  • Albrechts FO (1953) The anatomy of migratory locust. Athlone Press, London

    Google Scholar 

  • Atwood HL (1973) An attempt to account for diversity of crustacean muscles. Am Zool 11:357–378

    Google Scholar 

  • Bacon DP, Altman JS (1977) A silver intensification method for cobalt-filled neurones in wholemount preparations. Brain Res 138:359–363

    Google Scholar 

  • Barany M (1967) ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 50:197–218

    Google Scholar 

  • Brooke MH, Kaiser KK (1970) Three “myosin adenosine triphosphatase” systems: The nature of their pH lability and sulfhydryl dependence. J Histochem Cytochem 18:670–672

    Google Scholar 

  • Burns MD, Usherwood PNR (1979) The control of walking in Orthoptera: II. Motor neurone activity in normal free walking animals. J Exp Biol 79:69–98

    Google Scholar 

  • Campbell JI (1961) The anatomy of the nervous system of the mesothorax of Locusta migratoria migratorioides. Proc R Zool Soc Lond 137:403–432

    Google Scholar 

  • Cochrane DG, Elder HY, Usherwood PNR (1972) Physiology and ultrastrusture of phasic and tonic skeletal muscle fibres in the locust, Schistocerca gregaria. J Cell Sci 10:419–441

    Google Scholar 

  • Galler S, Hutzler C, Haller T (1990) Effects of taurine on force development of skinned muscle preparations. J Exp Biol 152:255–264

    Google Scholar 

  • Galler S, Rathmayer W (1991) Shortening velocity and pCa-tension relationship in skinned crab muscle fibres of different type. Pflügers Arch (in press)

  • Govind CK, Atwood HL (1982) Organization of neuromuscular systems. In: Bliss D (ed) The biology of Crustacea, vol 3. Academic Press, New York, pp 63–103

    Google Scholar 

  • Griffiths PJ, Duchateau JJ, Maeda Y, Potter JD, Ashley CC (1990) Mechanical characteristics of skinned and intact muscle fibres from the giant barnacle, Balanus nubilus. Pflügers Arch 415:554–565

    Google Scholar 

  • Guth L, Samaha FJ (1970) Procedure for the histochemical demonstration of actomyosin ATPase. Exp Neurol 28:365–367

    Google Scholar 

  • Hale JP, Burrows M (1985) Innervation patterns of inhibitory motor neurones in the thorax of the locust. J Exp Biol 117:401–413

    Google Scholar 

  • Harrington WF, Rodgers ME (1984) Myosin. Annu Rev Biochem 53:35–73

    Google Scholar 

  • Hart TF, Fourtner CR (1979) Histochemical analysis of physiologically and morphologically identified muscles in an insect leg. Comp Biochem Physiol 64A:437–440

    Google Scholar 

  • Henneman E, Somjen G, Carpenter DO (1965) Functional significance of cell size in spinal motoneurons. J Neurophysiol 28:560–580

    Google Scholar 

  • Hoyle G (1966) An isolated insect ganglion-nerve-muscle preparation. J Exp Biol 44:413–427

    Google Scholar 

  • Hoyle G (1978) Distribution of nerve and muscle fibre types in locust jumping muscle. J Exp Biol 78:205–233

    Google Scholar 

  • Jahromi SS, Atwood HL (1969a) Structural features of muscle fibres in the cockroach leg. J Insect Physiol 13:2255–2262

    Google Scholar 

  • Jahromi SS, Atwood HL (1969b) Correlation of structure, speed of contraction, and total tension in fast and slow abdominal muscle fibres of the lobster (Homarus americanus). J Exp Zool 171:25–38

    Google Scholar 

  • Josephson RK (1975) Extensive and intensive factors determining the performance of striated muscle. J Exp Zool 194:135–154

    Google Scholar 

  • Josephson RK, Young D (1987) Fiber ultrastructure and contraction kinetics in insect fast muscles. Am Zool 27:991–1000

    Google Scholar 

  • Jutsum AR, Goldsworthy GJ (1976) Fuels for flight in locusts. J Insect Physiol 22:243–249

    Google Scholar 

  • Maier L, Rathmayer W, Pette D (1984) pH lability of myosin ATPase activity permits discrimination of different muscle fibre types in crustaceans. Histochemistry 81:75–77

    Google Scholar 

  • Martell AE, Smith RM (1977) Critical stability constants. Academic Press, New York London

    Google Scholar 

  • Moisescu DG, Thieleczek R (1979) Calcium and strontium concentrations changes within skinned muscle preparations following a change in the external bathing solution. J Physiol (Lond) 275:241–262

    Google Scholar 

  • Morgan CR, Stokes DR (1979) Ultrastructural heterogeneity of the mesocoxal muscles of Periplaneta americana. Cell Tissue Res 201:305–314

    Google Scholar 

  • Morgan CR, Tarras MS, Stokes DR (1980) Histochemical demonstration of enzymatic heterogeneity within the mesocoxal and metacoxal muscles of Periplaneta americana. J Insect Physiol 26:481–486

    Google Scholar 

  • Moss RL, Giulian GG, Greaser ML (1985) The effect of partial extraction of TnC upon the tension-pCa relationship in rabbit skinned skeletal muscle fibers. J Gen Physiol 86:585–600

    Google Scholar 

  • Müller AR, Wolf H, Galler S, Rathmayer W (1990) Matching of mechanical responses with neuromuscular properties in insect muscle fibres. In: Elsner N, Roth G (eds) Brain-perception, cognition. Proc 18th Göttingen Neurobiol Conf. Thieme Verlag, Stuttgart, New York, p 43

    Google Scholar 

  • Nemeth P, Pette D, Vrbova G (1981) Comparison of enzyme activities among single muscle fibres within defined motor units. J Physiol (Lond) 311:489–495

    Google Scholar 

  • Nolte J, Pette D (1972) Applications of gel film technique to microphotometry and studies on the intralobular distribution of succinate dehydrogenase and lactate dehydrogenase activities in rat liver. J Histochem Cytochem 20:567–576

    Google Scholar 

  • Padykula HA, Herman E (1955) The specificity of the histochemical method for adenosine triphosphatase. J Histochem Cytochem 3:170–195

    Google Scholar 

  • Peckham M, Molloy JE, Sparrow JC, White DCS (1990) Physiological properties of the dorsal longitudinal flight muscle and the tergal depressor of the trochanter muscle of Drosophila melanogaster. J Musc Res Cell Mot 11:203–215

    Google Scholar 

  • Peckham M, White DCS (1989) Mechanical responses of skinned flight muscle fibres from the dragonfly (Aeshna juncea). J Physiol (Lond) 414:122P

    Google Scholar 

  • Peter JB, Barnard RJ, Edgerton VR, Gillespie CA, Stempel KE (1972) Metabolic profiles of three fiber types of skeletal muscle in guinea pigs and rabbits. Biochemistry 11:2627–2633

    Google Scholar 

  • Pette D, Schnez U (1977) Myosin light chain patterns of individual fast- and slow-twitch fibres of rabbit muscles. Histochemistry 54:97–107

    Google Scholar 

  • Pitman RM, Tweedle CD, Cohen MJ (1972) Branching of central neurones: Intracellular cobalt injection for light and electron microscopy. Science 176:412–414

    Google Scholar 

  • Rathmayer W (1990) Inhibition through neurons of the common inhibitory type (CI-neurons) in crab muscles. In: Wiese K, Krenz WD, Tautz J, Reichert H, Mulloney B (eds) Frontiers in crustacean neurobiology. Birkhäuser, Basel Boston Berlin pp 271–278

    Google Scholar 

  • Rathmayer W, Maier L (1987) Muscle fiber types in crabs: Studies on single identified muscle fibers. Am Zool 27:1067–1077

    Google Scholar 

  • Reiser PJ, Moss RL, Giulian GG, Greaser ML (1985) Shortening velocity in single fibers from adult rabbit soleus muscles is correlated with myosin heavy-chain composition. J Biol Chem 260:9077–9080

    Google Scholar 

  • Romeis B (1968) Mikroskopische Technik. Oldenburg, Munich, pp 275–276

    Google Scholar 

  • Snodgrass RE (1929) The thoracic mechanism of a grasshopper and its antecedents. Smithson Misc Collect 82:1–112

    Google Scholar 

  • Staron RS, Pette D (1988) Molecular basis of the phenotypic characteristics of mammalian muscle fibres. Ciba Found Symp 138:22–34

    Google Scholar 

  • Stephenson DG, Williams DA (1980) Activation of skinned arthropod muscle fibres by Ca2+ and Sr2+. J Musc Res Cell Mot 1:73–87

    Google Scholar 

  • Stephenson DG, Williams DA (1982) Effects of sarcomere lenght on the force-pCa relation in fast- and slow-twitch skinned muscle fibres from the rat. J Physiol (Lond) 33:637–653

    Google Scholar 

  • Stienen GJM, Güth K, Rüegg JC (1983) Force and force transients in skeletal muscle fibers of the frog skinned by freeze-drying. Pflügers Arch 397:272–276

    Google Scholar 

  • Stokes DR (1987) Insect muscles innervated by single motoneurones: structural and biochemical features. Am Zool 27:1001–1010

    Google Scholar 

  • Stokes DR, Josephson RK, Price RB (1975) Structural and functional heterogeneity in an insect muscle. J Exp Zool 194:379–408

    Google Scholar 

  • Stokes DR, Vitale AJ, Morgan CR (1979) Enzyme histochemistry of the mesocoxal muscles of Periplaneta americana. Cell Tissue Res 198:175–189

    Google Scholar 

  • Termin A, Staron RS, Pette D (1989) Myosin heavy chain isoforms in histochemically defined fiber types of rat muscle. Histochemistry 92:453–457

    Google Scholar 

  • Usherwood PNR, Grundfest H (1965) Peripheral inhibition in skeletal muscle of insects. J Neurophysiol 28:497–518

    Google Scholar 

  • Watson AHD, Burrows M, Hale JP (1985) The morphology and ultrastructure of common inhibitory motor neurones in the thorax of the locust. J Comp Neurol 239:341–359

    Google Scholar 

  • Werman R, Grundfest H (1961) Graded or all=or-none electrogenesis in arthropod muscle. II. The effects of alkali-earth and onium ions on lobster muscle fibers. J Gen Physiol 44:997–1027

    Google Scholar 

  • Wiens TJ (1989) Common and specific inhibition in leg muscles of decapods: sharpened distinctions. J Neurobiol 20:458–469

    Google Scholar 

  • Wiens TJ, Maier L, Rathmayer W (1988) The distribution of the common inhibitory neuron in brachyuran limb musculature. J Comp Physiol A 163:651–664

    Google Scholar 

  • Wilson JA (1979) The structure and function of serially homologous leg motor neurons in the locust: I. Anatomy. J Neurobiol 10:41–65

    Google Scholar 

  • Woledge RC, Curtin NA, Homsher E (1985) Energetic aspects of muscle contraction. Academic Press, New York London

    Google Scholar 

  • Zite-Ferenczi F, Rüdel R (1978) A diffractometer using a lateral effect photodiode for the rapid determination of sarcomere length changes in cross-striated muscles. Pflügers Arch 374:97–100

    Google Scholar 

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Author notes

  1. S. Galler

    Present address: Institut für Zoologie, Universität Salzburg, A-5020, Salzburg, Österreich

Authors and Affiliations

  1. Fakultät für Biologie, Universität Konstanz, Postfach 5560, W-7750, Konstanz, Fed. Rep. Germany

    Antje R. Müller, H. Wolf, S. Galler & W. Rathmayer

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  1. Antje R. Müller
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  2. H. Wolf
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  3. S. Galler
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  4. W. Rathmayer
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Müller, A.R., Wolf, H., Galler, S. et al. Correlation of electrophysiological, histochemical, and mechanical properties in fibres of the coxa rotator muscle of the locust, Locusta migratoria . J Comp Physiol B 162, 5–15 (1992). https://doi.org/10.1007/BF00257930

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