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. 1968 Mar 1;36(3):497–526. doi: 10.1083/jcb.36.3.497

CARDIAC MUSCLE

A Comparative Study of Purkinje Fibers and Ventricular Fibers

Joachim R Sommer 1, Edward A Johnson 1
PMCID: PMC2107380  PMID: 5645545

Abstract

With light and electron microscopy a comparison has been made of the morphology of ventricular (V) and Purkinje (P) fibers of the hearts of guinea pig, rabbit, cat, dog, goat, and sheep. The criteria, previously established for the rabbit heart, that V fibers are distinguished from P fibers by the respective presence and absence of transverse tubules is shown to be true for all animals studied. No evidence was found of a permanent connection between the sarcoplasmic reticulum and the extracellular space. The sarcoplasmic reticulum (SR) of V fibers formed couplings with the sarcolemma of a transverse tubule (interior coupling) and with the peripheral sarcolemma (peripheral coupling), whereas in P fibers the SR formed only peripheral couplings. The forms of the couplings were identical. The significance, with respect to excitation-contraction coupling, of the difference in the form of the couplings in cardiac versus skeletal muscle is discussed together with the electrophysiological implications of the differing geometries of bundles of P fibers from different animals.

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Selected References

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  1. Adrian R. H., Freygang W. H. The potassium and chloride conductance of frog muscle membrane. J Physiol. 1962 Aug;163(1):61–103. doi: 10.1113/jphysiol.1962.sp006959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BAUTOVICH G., GIBB D. B., JOHNSON E. A. The force of contraction of the rabbit papillary muscle preparation as a function of the frequency and pattern of stimulation. Aust J Exp Biol Med Sci. 1962 Dec;40:455–472. doi: 10.1038/icb.1962.50. [DOI] [PubMed] [Google Scholar]
  3. Becker N. H., Novikoff A. B., Zimmerman H. M. Fine structure observations of the uptake of intravenously injected peroxidase by the rat choroid plexus. J Histochem Cytochem. 1967 Mar;15(3):160–165. doi: 10.1177/15.3.160. [DOI] [PubMed] [Google Scholar]
  4. Brandt P. W., Reuben J. P., Girardier L., Grundfest H. Correlated morphological and physiological studies on isolated single muscle fibers. I. Fine structure of the crayfish muscle fiber. J Cell Biol. 1965 Jun;25(3 Suppl):233–260. doi: 10.1083/jcb.25.3.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. CAESAR R., EDWARDS G. A., RUSKA H. Electron microscopy of the impulse conducting system of the sheep heart. Z Zellforsch Mikrosk Anat. 1958;48(6):698–719. doi: 10.1007/BF00398655. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Costantin L. L., Podolsky R. J. Calcium localization and the activation of striated muscle fibers. Fed Proc. 1965 Sep-Oct;24(5):1141–1145. [PubMed] [Google Scholar]
  8. Dudel J., Peper K., Rüdel R., Trautwein W. Excitatory membrane current in heart muscle (Purkinje fibers). Pflugers Arch Gesamte Physiol Menschen Tiere. 1966;292(3):255–273. doi: 10.1007/BF00362740. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. FANBURG B., FINKEL R. M., MARTONOSI A. THE ROLE OF CALCIUM IN THE MECHANISM OF RELAXATION OF CARDIAC MUSCLE. J Biol Chem. 1964 Jul;239:2298–2305. [PubMed] [Google Scholar]
  12. FARQUHAR M. G., PALADE G. E. Junctional complexes in various epithelia. J Cell Biol. 1963 May;17:375–412. doi: 10.1083/jcb.17.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. FRANZINI-ARMSTRONG C., PORTER K. R. SARCOLEMMAL INVAGINATIONS CONSTITUTING THE T SYSTEM IN FISH MUSCLE FIBERS. J Cell Biol. 1964 Sep;22:675–696. doi: 10.1083/jcb.22.3.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Farquhar M. G., Palade G. E. Cell junctions in amphibian skin. J Cell Biol. 1965 Jul;26(1):263–291. doi: 10.1083/jcb.26.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Forssmann W. G., Girardier L. Untersuchungen zur Ultrastruktur des Rattenherzmuskels mit besonderer Berücksichtigung des sarcoplasmatischen Retikulums. Z Zellforsch Mikrosk Anat. 1966;72(2):249–275. [PubMed] [Google Scholar]
  17. Fozzard H. A. Membrane capacity of the cardiac Purkinje fibre. J Physiol. 1966 Jan;182(2):255–267. doi: 10.1113/jphysiol.1966.sp007823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. GIRARDIER L., POLLET M. D'EMONSTRATION DE LA CONTINUIT'E ENTRE L'ESPACE INTERSTITIEL ET LA LUMI'ERE DE CANAUX INTRACELLULAIRES DANS LE MYOCARDE DE RAT. Helv Physiol Pharmacol Acta. 1964;22:C72–C73. [PubMed] [Google Scholar]
  19. Gauthier G. F., Padykula H. A. Cytochemical studies of adenosine triphosphatase activity in the sarcoplasmic reticulum. J Cell Biol. 1965 Oct;27(1):252–260. doi: 10.1083/jcb.27.1.252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. HASSELBACH W., MAKINOSE M. [The calcium pump of the "relaxing granules" of muscle and its dependence on ATP-splitting]. Biochem Z. 1961;333:518–528. [PubMed] [Google Scholar]
  21. HASSELBACH W. RELAXATION AND THE SARCOTUBULAR CALCIUM PUMP. Fed Proc. 1964 Sep-Oct;23:909–912. [PubMed] [Google Scholar]
  22. HASSELBACH W. RELAXATION AND THE SARCOTUBULAR CALCIUM PUMP. Fed Proc. 1964 Sep-Oct;23:909–912. [PubMed] [Google Scholar]
  23. HODGKIN A. L., HOROWICZ P. The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol. 1959 Oct;148:127–160. doi: 10.1113/jphysiol.1959.sp006278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. HUXLEY A. F., TAYLOR R. E. Local activation of striated muscle fibres. J Physiol. 1958 Dec 30;144(3):426–441. doi: 10.1113/jphysiol.1958.sp006111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Heumann H. G., Zebe E. Uber Feinbau und Funktionsweise der Fasern aus dem Hautmuskelschlauch des Regenwurms, Lumbricus terrestris L. Z Zellforsch Mikrosk Anat. 1967;78(1):131–150. [PubMed] [Google Scholar]
  27. JOHNSON E. A., ROWE M. J., VAUGHAN P. C. A QUANTITATIVE DESCRIPTION OF THE SHORT TERM CHANGES IN THE FORCE OF CONTRACTION OF RABBIT PAPILLARY MUSCLE WITH THE PATTERN OF STIMULATION. Aust J Exp Biol Med Sci. 1964 Apr;42:197–208. doi: 10.1038/icb.1964.21. [DOI] [PubMed] [Google Scholar]
  28. JOHNSON E. A., TILLE J. Investigations of the electrical properties of cardiac muscle fibres with the aid of intracellular double-barrelled electrodes. J Gen Physiol. 1961 Jan;44:443–467. doi: 10.1085/jgp.44.3.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. JULIAN F. J., MOORE J. W., GOLDMAN D. E. Current-voltage relations in the lobster giant axon membrane under voltage clamp conditions. J Gen Physiol. 1962 Jul;45:1217–1238. doi: 10.1085/jgp.45.6.1217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. JULIAN F. J., MOORE J. W., GOLDMAN D. E. Membrane potentials of the lobster giant axon obtained by use of the sucrose-gap technique. J Gen Physiol. 1962 Jul;45:1195–1216. doi: 10.1085/jgp.45.6.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Johnson E. A., Sommer J. R. A strand of cardiac muscle. Its ultrastructure and the electrophysiological implications of its geometry. J Cell Biol. 1967 Apr;33(1):103–129. doi: 10.1083/jcb.33.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. KAWAMURA K. Electron microscope studies on the cardiac conduction system of the dog. I. The Purkinje fibers. Jpn Circ J. 1961 Jun;25:594–616. doi: 10.1253/jcj.25.594. [DOI] [PubMed] [Google Scholar]
  33. LINDNER E. Die submikroskopische Morphologie des Herzmuskels. Z Zellforsch Mikrosk Anat. 1957;45(6):702–746. [PubMed] [Google Scholar]
  34. MOORE D. H., RUSKA H. Electron microscope study of mammalian cardiac muscle cells. J Biophys Biochem Cytol. 1957 Mar 25;3(2):261–268. doi: 10.1083/jcb.3.2.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. MUIR A. R. FURTHER OBSERVATIONS ON THE CELLULAR STRUCTURE OF CARDIAC MUSCLE. J Anat. 1965 Jan;99:27–46. [PMC free article] [PubMed] [Google Scholar]
  36. MUIR A. R. Observations on the fine structure of the Purkinje fibres in the ventricles of the sheep's heart. J Anat. 1957 Apr;91(2):251–258. [PMC free article] [PubMed] [Google Scholar]
  37. McAllister R. E., Noble D. The time and voltage dependence of the slow outward current in cardiac Purkinje fibres. J Physiol. 1966 Oct;186(3):632–662. doi: 10.1113/jphysiol.1966.sp008060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. NELSON D. A., BENSON E. S. On the structural continuities of the transverse tubular system of rabbit and human myocardial cells. J Cell Biol. 1963 Feb;16:297–313. doi: 10.1083/jcb.16.2.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. NOBLE D. The voltage dependence of the cardiac membrane conductance. Biophys J. 1962 Sep;2:381–393. doi: 10.1016/s0006-3495(62)86862-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. PALADE G. E. A study of fixation for electron microscopy. J Exp Med. 1952 Mar;95(3):285–298. doi: 10.1084/jem.95.3.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Page E. The occurrence of inclusions within membrane-limited structures that run longitudinally in the cells of mammalian heart muscle. J Ultrastruct Res. 1967 Jan;17(1):63–71. doi: 10.1016/s0022-5320(67)80020-0. [DOI] [PubMed] [Google Scholar]
  42. Page E. Tubular systems in Purkinje cells of the cat heart. J Ultrastruct Res. 1967 Jan;17(1):72–83. doi: 10.1016/s0022-5320(67)80021-2. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Peachey L. D. The sarcoplasmic reticulum and transverse tubules of the frog's sartorius. J Cell Biol. 1965 Jun;25(3 Suppl):209–231. doi: 10.1083/jcb.25.3.209. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. REVEL J. P. The sarcoplasmic reticulum of the bat cricothroid muscle. J Cell Biol. 1962 Mar;12:571–588. doi: 10.1083/jcb.12.3.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. 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]
  48. 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]
  49. Rayns D. G., Simpson F. O., Bertaud W. S. Transverse tubule apertures in mammalian myocardial cells: surface array. Science. 1967 May 5;156(3775):656–657. doi: 10.1126/science.156.3775.656. [DOI] [PubMed] [Google Scholar]
  50. Rostgaard J., Behnke O. Fine structural localization of adenine nucleoside phosphatase activity in the sarcoplasmic reticulum and the T system of rat myocardium. J Ultrastruct Res. 1965 Jun;12(5):579–591. doi: 10.1016/s0022-5320(65)80049-1. [DOI] [PubMed] [Google Scholar]
  51. SIMPSON F. O., OERTELIS S. J. The fine structure of sheep myocardial cells; sarcolemmal invaginations and the transverse tubular system. J Cell Biol. 1962 Jan;12:91–100. doi: 10.1083/jcb.12.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. SIMPSON F. O. THE TRANSVERSE TUBULAR SYSTEM IN MAMMALIAN MYOCARDIAL CELLS. Am J Anat. 1965 Jul;117:1–17. doi: 10.1002/aja.1001170102. [DOI] [PubMed] [Google Scholar]
  53. SJOSTRAND F. S., ANDERSSON-CEDERGREN E., DEWEY M. M. The ultrastructure of the intercalated discs of frog, mouse and guinea pig cardiac muscle. J Ultrastruct Res. 1958 Apr;1(3):271–287. doi: 10.1016/s0022-5320(58)80008-8. [DOI] [PubMed] [Google Scholar]
  54. SOMMER J. R., SPACH M. S. ELECTRON MICROSCOPIC DEMONSTRATION OF ADENOSINETRIPHOSPHATASE IN MYOFIBRILS AND SARCOPLASMIC MEMBRANES OF CARDIAC MUSCLE OF NORMAL AND ABNORMAL DOGS. Am J Pathol. 1964 Mar;44:491–505. [PMC free article] [PubMed] [Google Scholar]
  55. Schulze W., Wollenberger A. Zytochemische Lokalisation und Charakterisierung von phosphatabspaltenden Fermenten im sarkotubulären System quergestreifter Muskeln. Histochemie. 1967;10(2):140–153. doi: 10.1007/BF00311404. [DOI] [PubMed] [Google Scholar]
  56. Seraydarian K., Mommaerts W. F. Density gradient separation of sarcotubular vesicles and other particulate constituents of rabbit muscle. J Cell Biol. 1965 Aug;26(2):641–656. doi: 10.1083/jcb.26.2.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Sommer J. R., Hasselbach W. The effect of glutaraldehyde and formaldehyde on the calcium pump of the sarcoplasmic reticulum. J Cell Biol. 1967 Sep;34(3):902–905. doi: 10.1083/jcb.34.3.902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Tice L. W., Engel A. G. Cytochemistry of phosphatases of the sarcoplasmic reticulum. II. In situ localization of the Mg-dependent enzyme. J Cell Biol. 1966 Dec;31(3):489–499. doi: 10.1083/jcb.31.3.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. VIRAGH S., PORTE A. [Fine structure of vector tissue in the rat heart]. Z Zellforsch Mikrosk Anat. 1961;55:263–281. [PubMed] [Google Scholar]
  60. WEIDMANN S. The electrical constants of Purkinje fibres. J Physiol. 1952 Nov;118(3):348–360. doi: 10.1113/jphysiol.1952.sp004799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. WINEGRAD S. AUTORADIOGRAPHIC STUDIES OF INTRACELLULAR CALCIUM IN FROG SKELETAL MUSCLE. J Gen Physiol. 1965 Jan;48:455–479. doi: 10.1085/jgp.48.3.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Walker S. M., Schrodt G. R. Continuity of the T system with the sarcolemma in rat skeletal muscle fibers. J Cell Biol. 1965 Dec;27(3):671–677. doi: 10.1083/jcb.27.3.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. ZEBE E., FALK H. ELEKTRONENMIKROSKOPISCHE LOKALISATION ATP-SPALTENDER REAKTIONEN IN QUERGESTREIFTEN MUSKELN. Exp Cell Res. 1963 Aug;31:340–344. doi: 10.1016/0014-4827(63)90011-9. [DOI] [PubMed] [Google Scholar]

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