Abstract
An ultrastructural comparison of the two types of intrafusal muscle fibers in muscle spindles of the rat was undertaken. Discrete myofibrils with abundant interfibrillar sarcoplasm and organelles characterize the nuclear chain muscle fiber, while a continuous myofibril-like bundle with sparse interfibrillar sarcoplasm distinguishes the nuclear bag muscle fiber. Nuclear chain fibers possess well-defined and typical M bands in the center of each sarcomere, while nuclear bag fibers contain ill-defined M bands composed of two parallel thin densities in the center of the pseudo-H zone of each sarcomere. Mitochondria of nuclear chain fibers are larger and more numerous than they are in nuclear bag fibers. Mitochondria of chain fibers, in addition, often contain conspicuous dense granules, and they are frequently intimately related to elements of the sarcoplasmic reticulum (SR). Striking differences are noted in the organization and degree of development of the sarcotubular system. Nuclear bag fibers contain a poorly developed SR and T system with only occasional junctional couplings (dyads and triads). Nuclear chain fibers, in contrast, possess an unusually well-developed SR and T system and a variety of multiple junctional couplings (dyads, triads, quatrads, pentads, septads). Greatly dilated SR cisternae are common features of nuclear chain fibers, often forming intimate associations with T tubules, mitochondria, and the sarcolemma. Such dilatations of the SR were not encountered in nuclear bag fibers. The functional significance of these structural findings is discussed.
Full Text
The Full Text of this article is available as a PDF (2.7 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- ANDERSSON-CEDERGREN E., MUSCATELLO U. The participation of the sarcotubular system in glycogen metabolism. J Ultrastruct Res. 1963 Apr;8:391–401. doi: 10.1016/s0022-5320(63)90015-7. [DOI] [PubMed] [Google Scholar]
- BRIERLEY G. P., MURER E., BACHMANN E. STUDIES ON ION TRANSPORT. III. THE ACCUMULATION OF CALCIUM AND INORGANIC PHOSPHATE BY HEART MITOCHONDRIA. Arch Biochem Biophys. 1964 Apr;105:89–102. doi: 10.1016/0003-9861(64)90239-5. [DOI] [PubMed] [Google Scholar]
- Boyd I. A. The behaviour of isolated mammalian muscle spindles with intact innervation. J Physiol. 1966 Oct;186(2):109P–110P. [PubMed] [Google Scholar]
- COSTANTIN L. L., FRANZINI-ARMSTRONG C., PODOLSKY R. J. LOCALIZATION OF CALCIUM-ACCUMULATING STRUCTURES IN STRIATED MUSCLE FIBERS. Science. 1965 Jan 8;147(3654):158–160. doi: 10.1126/science.147.3654.158. [DOI] [PubMed] [Google Scholar]
- Cornog J. L., Jr, Gonatas N. K. Ultrastructure of rhabdomyoma. J Ultrastruct Res. 1967 Oct 31;20(5):433–450. doi: 10.1016/s0022-5320(67)80111-4. [DOI] [PubMed] [Google Scholar]
- Corvaja N., Marinozzi V., Pompeiano O. Muscle spindles in the lumbrical muscle of the adult cat. Electron microscopic observations and functional considerations. Arch Ital Biol. 1969 Oct;107(4):365–543. [PubMed] [Google Scholar]
- Corvaja N., Pompeiano O. The differentiation of two types of intrafusal fibres in rabbit muscle spindles. An electron microscopic study. Pflugers Arch. 1970;317(3):187–197. doi: 10.1007/BF00586503. [DOI] [PubMed] [Google Scholar]
- ESSNER E., NOVIKOFF A. B., QUINTANA N. NUCLEOSIDE PHOSPHATASE ACTIVITIES IN RAT CARDIAC MUSCLE. J Cell Biol. 1965 May;25:201–215. doi: 10.1083/jcb.25.2.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Engel A. G. Electron microscopic observations in primary hypokalemic and thyrotoxic periodic paralyses. Mayo Clin Proc. 1966 Nov;41(11):797–808. [PubMed] [Google Scholar]
- FALK G., FATT P. LINEAR ELECTRICAL PROPERTIES OF STRIATED MUSCLE FIBRES OBSERVED WITH INTRACELLULAR ELECTRODES. Proc R Soc Lond B Biol Sci. 1964 Apr 14;160:69–123. doi: 10.1098/rspb.1964.0030. [DOI] [PubMed] [Google Scholar]
- FANBURG B. CALCIUM IN THE REGULATION OF HEART MUSCLE CONTRACTION AND RELAXATION. Fed Proc. 1964 Sep-Oct;23:922–925. [PubMed] [Google Scholar]
- FAWCETT D. W., REVEL J. P. The sarcoplasmic reticulum of a fast-acting fish muscle. J Biophys Biochem Cytol. 1961 Aug;10(4):89–109. doi: 10.1083/jcb.10.4.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fanburg B. L., Drachman D. B., Moll D., Roth S. I. Calcium transport in isolated sarcoplasmic reticulum during muscle maturation. Nature. 1968 Jun 8;218(5145):962–964. doi: 10.1038/218962a0. [DOI] [PubMed] [Google Scholar]
- Forssmann W. G., Girardier L. A study of the T system in rat heart. J Cell Biol. 1970 Jan;44(1):1–19. doi: 10.1083/jcb.44.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gauthier G. F., Padykula H. A. Cytological studies of fiber types in skeletal muscle. A comparative study of the mammalian diaphragm. J Cell Biol. 1966 Feb;28(2):333–354. doi: 10.1083/jcb.28.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gori Z., Pellegrino C., Pollera M. The castration atrophy of the dorsal bulbocavernosus muscle of rat: an electron microscopic study. Exp Mol Pathol. 1967 Apr;6(2):172–198. doi: 10.1016/0014-4800(67)90054-8. [DOI] [PubMed] [Google Scholar]
- HASSELBACH W. RELAXATION AND THE SARCOTUBULAR CALCIUM PUMP. Fed Proc. 1964 Sep-Oct;23:909–912. [PubMed] [Google Scholar]
- HENNEMAN E., OLSON C. B. RELATIONS BETWEEN STRUCTURE AND FUNCTION IN THE DESIGN OF SKELETAL MUSCLES. J Neurophysiol. 1965 May;28:581–598. doi: 10.1152/jn.1965.28.3.581. [DOI] [PubMed] [Google Scholar]
- HUXLEY H. E. EVIDENCE FOR CONTINUITY BETWEEN THE CENTRAL ELEMENTS OF THE TRIADS AND EXTRACELLULAR SPACE IN FROG SARTORIUS MUSCLE. Nature. 1964 Jun 13;202:1067–1071. doi: 10.1038/2021067b0. [DOI] [PubMed] [Google Scholar]
- James N. T. Histochemical demonstration of myoglobin in skeletal muscle fibres and muscle spindles. Nature. 1968 Sep 14;219(5159):1174–1175. doi: 10.1038/2191174a0. [DOI] [PubMed] [Google Scholar]
- Knappeis G. G., Carlsen F. The ultrastructure of the M line in skeletal muscle. J Cell Biol. 1968 Jul;38(1):202–211. doi: 10.1083/jcb.38.1.202. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nyström B. Muscle-spindle histochemistry. Science. 1967 Mar 17;155(3768):1424–1426. doi: 10.1126/science.155.3768.1424. [DOI] [PubMed] [Google Scholar]
- OGATA T., MORI M. HISTOCHEMICAL STUDY OF OXIDATIVE ENZYMES IN VERTEBRATE MUSCLES. J Histochem Cytochem. 1964 Mar;12:171–182. doi: 10.1177/12.3.171. [DOI] [PubMed] [Google Scholar]
- PEACHEY L. D., HUXLEY A. F. Structural identification of twitch and slow striated muscle fibers of the frog. J Cell Biol. 1962 Apr;13:177–180. doi: 10.1083/jcb.13.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Page S. G. A comparison of the fine structures of frog slow and twitch muscle fibers. J Cell Biol. 1965 Aug;26(2):477–497. doi: 10.1083/jcb.26.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Philpott C. W., Goldstein M. A. Sarcoplasmic reticulum of striated muscle: localization of potential calcium binding sites. Science. 1967 Feb 24;155(3765):1019–1021. doi: 10.1126/science.155.3765.1019. [DOI] [PubMed] [Google Scholar]
- REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
- RICHARDSON K. C., JARETT L., FINKE E. H. Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 1960 Nov;35:313–323. doi: 10.3109/10520296009114754. [DOI] [PubMed] [Google Scholar]
- Rayns D. G., Simpson F. O., Bertaud W. S. Surface features of striated muscle. II. Guinea-pig skeletal muscle. J Cell Sci. 1968 Dec;3(4):475–482. doi: 10.1242/jcs.3.4.475. [DOI] [PubMed] [Google Scholar]
- Schiaffino S., Margreth A. Coordinated development of the sarcoplasmic reticulum and T system during postnatal differentiation of rat skeletal muscle. J Cell Biol. 1969 Jun;41(3):855–875. doi: 10.1083/jcb.41.3.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schiaffino S., Settembrini P. Studies on the effect of denervation in developing muscle. I. Differentiation of the sarcotubular system. Virchows Arch B Cell Pathol. 1970;4(4):345–356. doi: 10.1007/BF02906089. [DOI] [PubMed] [Google Scholar]
- Schutta H. S., Armitage J. L. The sarcoplasmic reticulum in thyrotoxic hypokalemic periodic paralysis. Metabolism. 1969 Feb;18(2):81–83. doi: 10.1016/0026-0495(69)90099-7. [DOI] [PubMed] [Google Scholar]
- Smith D. S. The organization and function of the sarcoplasmic reticulum and T-system of muscle cells. Prog Biophys Mol Biol. 1966;16:107–142. doi: 10.1016/0079-6107(66)90004-6. [DOI] [PubMed] [Google Scholar]
- Thomas R. S., Greenawalt J. W. Microincineration, electron microscopy, and electron diffraction of calcium phosphate-loaded mitochondria. J Cell Biol. 1968 Oct;39(1):55–76. doi: 10.1083/jcb.39.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- WATSON M. L. Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol. 1958 Jul 25;4(4):475–478. doi: 10.1083/jcb.4.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Walker S. M., Schrodt G. R. Evidence for connections between mitochondria and the sarcoplasmic reticulum and evidence for glycogen granules within the sarcoplasmic reticulum. Am J Phys Med. 1966 Feb;45(1):25–43. [PubMed] [Google Scholar]
- Yellin H. A histochemical study of muscle spindles and their relationship to extrafusal fiber types in the rat. Am J Anat. 1969 May;125(1):31–45. doi: 10.1002/aja.1001250103. [DOI] [PubMed] [Google Scholar]
- Yellin H. Unique intrafusal and extraocular muscle fibers exhibiting dual actomyosin ATPase activity. Exp Neurol. 1969 Sep;25(1):153–163. doi: 10.1016/0014-4886(69)90078-8. [DOI] [PubMed] [Google Scholar]
- von Düring M., Andres K. H. Zur Feinstruktur der Muskelspindel von Mammalia. Anat Anz. 1969;124(5):566–573. [PubMed] [Google Scholar]