Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Gap junctions and impulse propagation in embryonic epithelium of Amphibia

A freeze-etching study

  • 28 Accesses

  • 6 Citations


Epithelium of amphibian embryos (Cynops orientalis, Xenopus laevis) was found in preceding experiments to generate and conduct impulses during a limited stage (26–37) of development. In order to elucidate the structural basis of impulse propagation, epithelial cells of four stages were examined by the freeze-etching method: (I) before and (II) during acquisition of conductivity; (III) when propagation was fully established, and (IV) when it was no longer present. Only few gap junctions (GJ) of small size were found in groups I and IV. GJ in epithelia of group III were increased in number and size, and appeared morphologically “coupled”, i.e., with more loosely arranged connexons. The size of gap-junctional particles did not differ significantly between coupled and uncoupled stages. Zonulae occludentes seemed “leaky” in stage I, and “tight” in stages II–IV. Thus, the morphological characteristics of specialized junctions between “non excitable cells” correlated with the opening and closing of low resistance intercellular current pathways during embryonic development.

Gap junctions in particular seem to form an essential link in the non-neural stimulus-response system, which may facilitate the mobility of the embryo during early phases of aquatic life before the reflex pathways have been established. Coupling and uncoupling of gap junctions may also play an important role in the regulation of cell differentiation and morphogenetic movement. The experimental model used in this study provides a useful tool for further investigations of structural correlates of gap junctional permeability under physiological conditions.

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


  1. Bennett MVL (1973) Function of electrotonic junctions in embryonic and adult tissues. Fed Proc 32:65–75

  2. Bennett MVL, Trinkaus JP (1970) Electrical coupling between embryonic cells by way of extracellular space and specialized junctions. J Cell Biol 44:592–610

  3. Bennett MVL, Goodenough DA (1978) Gap junctions, electrotonic coupling and intercellular communication. NRP Neurosci Res Progr Bull 16:373–486

  4. Blackshaw SE, Warner AE (1976) Low resistance junctions between mesoderm cells during development of trunk muscles. J Physiol 255:209–230

  5. Branton D, Bullivant S, Gilula NB, Karnovsky MJ, Moor H, Mühlethaler K, Norhtcote DH, Packer L, Satir B, Satir P, Staehelin LA, Steere RL, Weinstein RS (1975) Freeze-etching nomenclature. Science 190:54–56

  6. Chuang HH, Dai RX (1961) Concerning the conductivity of the embryonic epithelium in amphibian (inChinese). Kexue Tongbao 12:41–43

  7. Claude Ph, Goodenough DA (1973) Fracture faces of zonulae occludentes from “tight” and “leaky” epithelia. J Cell Biol 58:390–400

  8. Coghill GE (1929) Anatomy and the problem of behavior. Cambr Univ Press Cambridge

  9. Decker RS, Friend DS (1974) Assembly of gap junctions during amphibian neurulation. J Cell Biol 62:32–47

  10. Fan SF, Dai RX (1962) Electric activity of embryonic epithelium in urodeles (in Chinese). Kexue Tongbao 10:38–39

  11. Hanna RB, Spray DC, Model PG, Harris AL, Bennett MVL (1978) Ultrastructure and physiology of gap junctions of an amphibian embryo, effects of CO2. Biol Bull 155:442

  12. Harris JE, Whiting HP (1954) Structure and function in the locomotory system of the dogfish embryo. The myogenic stage of movement. J Exp Biol 31:501–524

  13. Hayes BP (1976) The distribution of intercellular gap junctions in the developing retina and pigment epithelium of Xenopus laevis. Anat Embryol 150:99–111

  14. Hirakow R, DeHaan RL (1970) Synchronization and the formation of nexal junctions between isolated chick embryonic heart myocytes beating in culture. J Cell Biol 47:88 a

  15. Keeter JS, Pappas GS, Model PG (1975) Inter- and intramyotomal gap junctions in the axolotl embryo. Dev Biol 45:21–33

  16. Moor H, Mühlethaler K (1963) Fine structure in frozen-etched yeast cells. J Cell Biol 17:609–628

  17. Nieuwkoop PD, Faber J (1956) Normal tables of Xenopus laevis (Daudin). Amsterdam North Holland Publishing Co.

  18. Peracchia C (1977) Gap junctions. Structural changes after uncoupling procedures. J Cell Biol 72:628–641

  19. Peracchia C (1978) Calcium effects on gap junction structure and cell coupling. Nature (Lond) 271:669–671

  20. Peracchia C (1980) Structural correlates of gap junction permeation. Int Rev Cytol 66:81–146

  21. Peracchia, Dulhunty AF (1976) Low resistance junctions in crayfish. Structural changes with functional uncoupling. J Cell Biol 70:419–439

  22. Potter DD, Furshpan ED, Lennon ES (1966) Connections between cells of the developing squid as revealed by electrophysiological methods. Proc Natl Acad Sci (USA) 55:328–336

  23. Revel JP, Yip P, Chang LL (1973) Cell junctions in the early chick embryo. A freeze etch study. Dev Biol 35:302–317

  24. Roberts A (1969) Conducted impulses in the skin of young tadpoles. Nature (Lond) 222:1265–1266

  25. Roberts A, Stirling ChA (1971) The properties and propagation of a cardiac-like impulse in the skin of young tadpoles. Z vergl Physiol 71:295–310

  26. Sanders EJ, Dicaprio RA (1976) Intercellular junctions in the Xenopus embryo prior to gastrulation. JExp Zool 167:415–421

  27. Sheridan JD (1977) Cell coupling and cell communication during embryogenesis. In: (G Poste, GL Nicholson) Cell surface in animal embryogenesis and development. Cell Surface Reviews, Vol I, pp409–447. Amsterdam Elsevier North-Holland Co

  28. Sheridan JD, Hammer-Wilson M, Preus D, Johnson RG (1978) Quantitative analysis of low-resistance junctions between cultured cells and correlation with gap-junctional areas. J Cell Biol 76:532–544

  29. Turin L, Warner A (1977) Carbon dioxide reversibly abolishes ionic communication between cells of early amphibian embryo. Nature 270:56–57

  30. Warner AE (1973) The electrical properties of the ectoderm in the amphibian embryo during induction and early development of the nervous system. J Physiol (Lond) 235:267–286

  31. Wintrebert MB (1904) Sur l'existence d'une irritabilité excito-motrice primitive, indépendante des voies nerveuse chez les embryons ciliés de batraciens. CR Soc Biol (Paris) 57:645–647

  32. Wintrebert MP (1905) Nouvelles recherches sur la sensibilité primitive des batraciens. CR Soc Biol (Paris) 59:58–59

  33. Wolpert L (1978) Gap junctions: Channels for communication in development. In: (JD Feldman, NB Gilula, JD Pitts) Intercellular junctions and synapses. London: Chapman and Hall, pp 83–96

Download references

Author information

Correspondence to K. Akert.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Chuang-Tseng, M.P., Chuang, H.H., Sandri, C. et al. Gap junctions and impulse propagation in embryonic epithelium of Amphibia. Cell Tissue Res. 225, 249–258 (1982).

Download citation

Key words

  • Skin epithelium
  • Impulse conduction
  • Gap junctions, coupling and uncoupling
  • Amphibian larvae
  • Freeze-etching