The Journal of Physiological Sciences

, Volume 66, Issue 4, pp 293–301 | Cite as

Functiogenesis of cardiac pacemaker activity

Mini-review
First Online:
Received:
Accepted:

Abstract

Throughout our investigations on the ontogenesis of the electrophysiological events in early embryonic chick hearts, using optical techniques to record membrane potential probed with voltage-sensitive dyes, we have introduced a novel concept of “functiogenesis” corresponding to “morphogenesis”. This article gives an account of the framework of “functiogenesis”, focusing on the cardiac pacemaker function and the functional organization of the pacemaking area.

Keywords

Functiogenesis Voltage-sensitive dye Early embryonic chick heart Cardiac pacemaker potential Pacemaking area Optical technique 

Abbreviations

VSD

Voltage-sensitive dye

H–H

Hamburger and Hamilton

This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

The experiments on the embryonic hearts were carried out in collaboration with many members in the laboratory in Tokyo Medical and Dental University. We are grateful to Brian Salzberg for his improvement of the English version.

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflicts of interest.

References

  1. 1.
    Cohen LB, Salzberg BM (1978) Optical measurement of membrane potential. Rev Physiol Biochem Pharmacol 83:35–88PubMedGoogle Scholar
  2. 2.
    Kamino K (1991) Optical approaches to ontogeny of electrical activity and related functional organization during early heart development. Physiol Rev 71:53–91PubMedGoogle Scholar
  3. 3.
    Kamino K (2015) Personal recollections: regarding the pioneer days of optical recording of membrane potential using voltage-sensitive dyes. Neurophotonics 2:021002-1-9CrossRefGoogle Scholar
  4. 4.
    Kamino K (1990) Optical studies of early developing cardiac and neural activities using voltage-sensitive dyes. Jpn J Physiol 40:443–461CrossRefPubMedGoogle Scholar
  5. 5.
    Hirota A, Kamino K, Komuro H, Sakai T, Yada T (1985) Optical studies of excitation-contraction coupling in the early embryonic chick heart. J Physiol Lond 366:89–106CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Patten BM (1949) Initiation and early changes in the character of the heart beat in vertebrate embryos. Physiol Rev 29:31–47PubMedGoogle Scholar
  7. 7.
    Sakai T, Kamino K (2001) Optical mapping approaches to cardiac electrophysiological functions. Jpn J Physiol 51:1–18CrossRefPubMedGoogle Scholar
  8. 8.
    Thomson W (1910) The work of Aristotle. Oxford, ClarendonGoogle Scholar
  9. 9.
    Manasek FJ (1980) Organization, interactions, and environment of heart cell during myocardial ontogeny. In: Berne RM, Sperelakis N, Geiner SR (eds) Handbook of physiology sect 2, The cardiovascular system vol 1. The heart. Williams and Wikins, Baltimore, pp 29–42Google Scholar
  10. 10.
    Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92CrossRefPubMedGoogle Scholar
  11. 11.
    Hirota A, Kamino K, Komuro H, Sakai T (1987) Mapping of early development of electrical activity in the embryonic chick heart using multiple-site optical recording. J Physiol Lond 383:711–728CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Fujii S, Hirota A, Kamino K (1980) Optical signals from early embryonic chick heart stained with potential sensitive dyes: evidence for electrical activity. J Physiol Lond 304:503–518CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Fujii S, Hirota A, Kamino K (1981) Optical recording of development of electrical activity in embryonic chick heart during early phases of cardiogenesis. J Physiol Lond 311:147–160CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Kamino K, Komuro H, Sakai T, Hirota A (1988) Functional pacemaking area in the early embryonic chick heart assessed by simultaneous multiple-site optical recording of spontaneous action potentials. J Gen Physiol 91:573–591CrossRefPubMedGoogle Scholar
  15. 15.
    Kamino K, Hirota A, Fujii S (1981) Localization of pacemaking activity in early embryonic heart monitored using voltage-sensitive dye. Nat Lond 290:595–597CrossRefGoogle Scholar
  16. 16.
    Manasek FJ (1968) Embryonic development of the heart. I. A light and electron microscopic study of myocardial development in the early chick embryo. J Morphol 125:329–366CrossRefPubMedGoogle Scholar
  17. 17.
    Ojeda JL, Hurle JM (1981) Establishment of the tubular heart role of cell death. In: Pexieder T (ed) Perspectives in cardiovascular research. Mechanism of cardiac morphogenesis and teratogenesis, vol 5. Raven, New York, pp 101–113Google Scholar
  18. 18.
    Hiruma T, Hirakow R (1985) An ultrastructual topographical study on myofibrillogenesis in the heart of chick embryo during pulsation onset period. Anat Embryol 172:325–329CrossRefPubMedGoogle Scholar
  19. 19.
    Fujii S, Hirota A, Kamino K (1981) Optical indications of pace-maker potential and rhythm generation in early embryonic chick heart. J Physiol Lond 312:253–263CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Sakai T, Hirota A, Fujii S, Kamino K (1983) Flexibility of regional pacemaking priority in early embryonic heart monitored by simultaneous optical recording of action potentials from multiple sites. Jpn J Physiol 33:337–350CrossRefPubMedGoogle Scholar
  21. 21.
    Fujii S, Hirota A, Kamino K (1981) Action potential synchrony in embryonic precontractile chick heart: optical monitoring with potentiometric dyes. J Physiol Lond 319:529–541CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Fujii S, Sakai T, Hirota A, Kamino K (1983) Optical recording of the pacemaking activity of a congenital double-heart in an early chick embryo. Dev Growth Differ 25:193–200CrossRefGoogle Scholar
  23. 23.
    Hirota A, Fujii S, Sakai T, Kamino K (1984) Optical recording of spontaneous action potentials from the congenital chick embryonic pre-contractile double-heart. Proc Jpn Acad Ser B 60:281–284CrossRefGoogle Scholar
  24. 24.
    Yada T, Sakai T, Komuro H, Hirota A, Kamino K (1985) Development of electrical rhythmic activity in early embryonic cultured chick double-heart monitored optically with a voltage-sensitive dye. Dev Biol 110:455–466CrossRefPubMedGoogle Scholar
  25. 25.
    Sakai T, Yada T, Hirota A, Komuro H, Kamino K (1998) A regional gradient of cardiac intrinsic rhythmicity depicted in embryonic cultured multiple hearts. Pflüger Arch-Eur J Physiol 437:61–69CrossRefGoogle Scholar
  26. 26.
    Kamino K, Komuro H, Sakai T (1988) Regional gradient of pacemaker activity in the early embryonic chick heart monitored by multisite optical recording. J Physiol Lond 402:301–314CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Weidmann S (1970) Electrical constants of trabecular muscle from mammalian heart. J Physiol Lond 210:1041–1054CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Hirota A, Fujii S, Sakai T, Kamino K (1983) Temperature dependence of spontaneous electrical activity in early embryonic heart monitored optically with a potential-sensitive dye. Jpn J Physiol 33:85–100CrossRefPubMedGoogle Scholar
  29. 29.
    Sakai T, Fujii S, Hirota A, Kamino K (1983) Optical evidence for calcium-action potentials in early embryonic precontractile chick heart using a potential-sensitive dye. J Membr Biol 72:205–212CrossRefPubMedGoogle Scholar
  30. 30.
    Stalsberg H, DeHaan RL (1969) Precardiac areas and formation of the tubular heart in the chick embryo. Dev Biol 19:128–159CrossRefPubMedGoogle Scholar
  31. 31.
    Patten BM (1971) Early embryology of the chick. McGraw-Hill, New York, pp 113–138Google Scholar
  32. 32.
    Kamino K, Hirota A, Komuro H (1989) Optical indication of electrical activity and excitation-contraction coupling in the early embryonic heart. Adv Biophys 25:45–93CrossRefPubMedGoogle Scholar
  33. 33.
    Sakai T, Hirota A, Kamino K (1996) Video-imaging assessment of initial beating patterns of the early embryonic chick heart. Jpn J Physiol 46:465–472CrossRefPubMedGoogle Scholar
  34. 34.
    Sakai T (2003) Video-imaging visualization of blood flow dynamics in early chick embryo. Jpn J Physiol 53:385–388CrossRefPubMedGoogle Scholar
  35. 35.
    Kamino K, Katoh Y, Komuro H, Sato K (1989) Multiple-site optical monitoring of neural activity evoked by vagus nerve stimulation in the embryonic chick brainstem. J Physiol Lond 409:263–283CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Momose-Sato Y, Sato K, Kamino K (2001) Optical approaches to embryonic development of neural functions in the brainstem. Prog Neurobiol 63:151–197CrossRefPubMedGoogle Scholar
  37. 37.
    Momose-Sato Y, Sato K, Kamino K (2015) Monitoring population membrane potential signals during development of the vertebrate nervous system. In: Carpenter M, Zecevic D, Bernus O (eds) Membrane potential imaging in the nervous system and heart. Springer, New York, pp 213–242CrossRefGoogle Scholar

Copyright information

© The Physiological Society of Japan and Springer Japan 2015

Authors and Affiliations

  1. 1.Department of Systems PhysiologyUniversity of the Ryukyus Graduate School of MedicineNishiharaJapan
  2. 2.Tokyo Medical and Dental UniversityTokyoJapan

Personalised recommendations