Summary
When fast-twitch skeletal muscles of the adult rabbit are subjected to continuous low-frequency activity by electrical stimulation of the corresponding motor nerves, the fibers undergo an ultrastructural transformation, so that after 6 weeks they have acquired an appearance typical of slow-twitch fibers. In the present study, stimulation was discontinued at this stage in order to follow the reverse transformation, in which the fibers recovered their original morphological characteristics under conditions of normal endogenous activity. Stereological techniques were used to assess the time course of this process over a period of 20 weeks in terms of fiber cross-sectional area, extent of T-system, thickness of the Z-band, and volume fraction of mitochondria in the fiber core. Fibers of transformed muscles were smaller than those of control muscles, but the differences were no longer evident after 9 weeks of recovery. After 2 weeks the T-system was still of limited extent, as is characteristic of slow-twitch fibers; it increased toward the amount typical of fast-twitch fibers between 2 and 4 weeks, and had reached its full extent by 12 weeks. The wide Z-bands characteristic of slow-twitch fibers were retained for 4 weeks, but the thickness had begun to decrease by 8 weeks and recovery was complete by 12 weeks. The mitochondrial volume did not increase during recovery, in contrast to the large increases which had been observed to take place between 2 and 6 weeks during the fast-to-slow transformation. Overall, the recovery of fast-twitch ultrastructural characteristics was complete, but followed a more extended time course, and involved less myofibrillar disruption at an intermediate stage, than the original fast-to-slow transformation.
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Alpert NR, Mulieri LA, Litten RZ (1983) Isoenzyme contribution to economy of contraction and relaxation in normal and hypertrophied hearts. In: Cardiac adaptation to hemodynamic overload, training and stress. Steinkopff Verlag, pp 147–157
Brown J, Salmons S (1981) Percutaneous switching of an implantable muscle stimulator via an optical link. J Biomed Eng 3:206–208
Brown WE, Salmons S, Whalen RG (1983) The sequential replacement of myosin subunit isoforms during muscle type transformation induced by long term electrical stimulation. J Biol Chem 258:14686–14692
Buller AJ, Eccles JC, Eccles RM (1960) Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. J Physiol 150:417–439
Burke RE, Edgerton VR (1975) Motor unit properties and selective involvement in movement. Exerc Sport Sci Rev 3:31–81
Czeh G, Gallego R, Kudo N, Kuno M (1978) Evidence for the maintenance of motoneurone properties by muscle activity. J Physiol (Lond) 281:239–252
Damiani E, Betto R, Salvotore S, Volpe P, Salviati G, Margreth A (1981) Polymorphism of sarcoplasmic-reticulum adenosine triphosphatase of rabbit skeletal muscle. Biochem J 197:245–248
Eisenberg BR (1983) Quantitative ultrastructure of mammalian skeletal muscle. In: Peachey LD, Adrian RH (eds) Handbook of physiology: Section 10, skeletal muscle Chapter 3. Williams and Wilkins, Baltimore, MD pp 73–112
Eisenberg BR, Kuda AM (1976) Discrimination between fiber populations in mammalian skeletal muscle by using ultrastructural parameters. J Ultrastruct Res 54:76–88
Eisenberg BR, Salmons S (1981) The reorganization of subcellular structure in muscle undergoing fast-to-slow type transformation: a stereological study. Cell Tissue Res 220:449–471
Eisenberg BR, Kuda AM, Peter JB (1974) Stereological analysis of mammalian skeletal muscle. I. Soleus muscle of the adult guinea pig. J Cell Biol 60:732–754
Franzini-Armstrong C (1977) The comparative ultrastructure of intracellular junctions in striated muscle fibers. In: Rowland LP (ed) Pathogenesis of muscular dystrophies. Excerpta Medica, Amsterdam pp 612–625
Gallego R, Huizar P, Kudo N, Kuno M (1978) Disparity of motoneurone and muscle differentiation following spinal transection in the kitten. J Physiol (Lond) 281:253–265
Gauthier GF, Padykula HA (1966) Cytological studies of fiber types in skeletal muscle. A comparative study of the mammalian diaphragm. J Cell Biol 28:333–354
Gillis JM, Thomason D, Lefevre J, Kretsinger RH (1982) Parvalbumins and muscle relaxation: a computer simulation study. J Muscle Res Cell Motil 3:377–398
Goldberg AL, Jablecki C, Li JB (1974) Effects of use and disuse on amino acid transport and protein turnover in muscle. Ann NY Acad Sci 228:190–201
Goldspink DF (1977) The influence of immobilization and stretch on protein turnover of rat skeletal muscle. J Physiol (Lond) 264:267–282
Goldspink G (1975) Biochemical energetics for fast and slow muscles. In: Bolis L, Maddrell SHP, Schmidt-Nielsen K (eds) Comparative physiology: Functional aspects of structural materials. Amsterdam, Elsevier pp 173–185
Goldspink G (1983) Alteration of myofibril size and structure during growth, exercise, and changes in environmental temperature. In: Peachy LD, Adrian RH (eds) Handbook of physiology section 10, skeletal muscle. Williams and Wilkins, Baltimore, MD pp 539–555
Heilmann C, Pette D (1979) Molecular transformations in sarcoplasmic reticulum of fast-twitch muscle by electro-stimulation. Eur J Biochem 93:437–446
Hoh JFY, Kwan BTS, Dunlop C, Kim BH (1980) Effects of nerve cross-union and cordotomy on myosin isoenzymes in fasttwitch and slow-twitch muscles of the rat. In: Pette D (ed) Plasticity of muscle, Walter de Gruyter, Berlin, pp 339–352
Hoppeler H, Mathieu O, Krauer R, Claassen H, Armstrong RB, Weibel ER (1981) Design of the mammalian respiratory system. VI. Distribution of mitochondria and capillaries in various muscles. Respir Physiol 44:87–111
Klug G, Wiehrer W, Reichmann H, Leberer E, Pette D (1983) Relationships between early alterations in parvalbumins, sarcoplasmic reticulum and metabolic enzymes in chronically stimulated fast twitch muscle. Pflüger's Arch 399:280–284
Kugelberg E, Thornell L-E (1983) Contraction time, histochemical type, and terminal cisternae volume of rat motor units. Muscle Nerve 6:149–153
Lømo T, Rosenthal J (1972) Control of ACh sensitivity by muscle activity in the rat. J Physiol (Lond) 221:493–513
Lømo T, Westgaard RH, Dahl HA (1974) Contractile properties of muscle: control by pattern of muscle activity in the rat. Proc R Soc B 187:99–103
Lorković H (1979) Effects of motor nerve anesthesia and tenotomy on muscle membrane properties. Pfluegers Arch 379:89–93
McGurk B, Salmons S (1982) Effects of long term electrical stimulation on protein synthesis in skeletal muscle. Fifth Int Cong Neuromusc Diseases, Marseilles, France TH 63
Mastri C, Salmons S, Thomas GH (1982) Early events in the response of fast skeletal muscle to chronic low-frequency stimulation. Polyamine synthesis and protein phosphorylation. Biochem J 206:211–219
Pette D, Müller W, Leisner E, Vrbová G (1976) Time dependent effects on contractile properties, fibre population, myosin light chains and enzymes of energy metabolism in intermittently and continuously stimulated fast twitch muscles of the rabbit. Pfluegers Arch 364:103–112
Salmons S, Henriksson J (1981) The adaptive response of skeletal muscle to increased use. Muscle Nerve 4:94–105
Salmons S, Vrbová G (1969) The influence of activity on some characteristics of mammalian fast and slow muscles. J Physiol (Lond) 201:535–549
Salmons S, Gale DR, Sréter FA (1978) Ultrastructural aspects of the transformation of muscle fibre type by long term stimulation: changes in Z discs and mitochondria. J Anat 127:17–31
Vandenburgh HH, Kaufman S (1981) Stretch-induced growth of skeletal myotubes correlates with inactivation of the sodium pump. J Cell Physiol 109:205–214
Weibel ER (1979) Stereological Methods. I. Practical Methods for Biological Morphometry. Academic Press, New York
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Eisenberg, B.R., Brown, J.M.C. & Salmons, S. Restoration of fast muscle characteristics following cessation of chronic stimulation. Cell Tissue Res. 238, 221–230 (1984). https://doi.org/10.1007/BF00217292
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DOI: https://doi.org/10.1007/BF00217292