Skip to main content
Log in

A freeze-fracture study of the skate electro receptor

  • Published:
Journal of Neurocytology

Summary

The sensory epithelium lining the ampulla of Lorenzini in the skate was examined by the freeze-fracture technique. Anastomosing tight junctions (zonula occludens) completely encircle the apex of each receptor cell joining it to neighbouring support cells. The tight junctions separate two distinctly different regions of the receptor-cell surface. The apical P-face has numerous large particles while just below the tight junctions of the lateral surface have many smaller particles. On its basal surface each receptor cell makes several evaginating ribbon synapses with an afferent nerve. Three regions of the synaptic evagination can be distinguished on the basis of membrane specializations: 1. At the tip of the evagination a regular array of large particles is found on the P-face of the receptor cell directly opposite a similar regular array of large particles on the P-face of the afferent nerve; 2. just above the tip at a narrow constriction, below which vesicles are not found, a population of large particles on the P-face of the receptor cell opposes a well-defined strip of large particles that cleaves with the E-face of the nerve fibre; 3. at the arch of the synaptic evagination randomly occurring dimples are found on the P-face and protrusions on the E-face of the receptor cell. The density of these protrusions increased in skates that were electrically stimulated. We suggest that the co-extensive arrays of particles at the tip of the ribbon synapse is an intercellular junction; that the active zone of the synapse is at or above the constriction; and that membrane retrieval occurs in the synaptic arch region.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Akert, K., Sandri, C. &Bennett, M. V. L. (1980) Ultrastructural characteristics of tuberous electroreceptors in a high frequency electric gymnotid,Sternarchus albifrons.Experientia 36, 737.

    Google Scholar 

  • Barets, A. &Szabo, T. (1962) Appareil synaptique des cellules sensorielle de l'ampoule de Lorenzini chez la torpille,Torpedo marmomta.Journal de Microscopic 1, 47–54.

    Google Scholar 

  • Bennett, M. V. L. &Clusin, W. T. (1979) Transduction at electroreceptors: origins and sensitivity. InMembrane Transduction Mechanisms (edited byCone, R. A. andDowling, J. E.), pp. 91–116. New York: Raven Press.

    Google Scholar 

  • Bullock, T. H. (1982) Electroreception.Annual Reviews of Neuroscience 5, 121–70.

    Google Scholar 

  • Clusin, W. T. &Bennett, M. V. L. (1977a) Calcium-activated conductance in skate electroreceptors. Current clamp experiments.Journal of General Physiology 69, 121–43.

    PubMed  Google Scholar 

  • Clusin, W. T. &Bennett, M. V. L. (1977b) Calcium-activated conductance in skate electroreceptors. Voltage-clamp experiments.Journal of General Physiology 69, 145–82.

    PubMed  Google Scholar 

  • Clusin, W. T. &Bennett, M. V. L. (1979a) The oscillatory response of skate electroreceptors to small voltage stimuli.Journal of General Physiology 73, 685–702.

    PubMed  Google Scholar 

  • Clusin, W. T. &Bennett, M. V. L. (1979b) The ionic basis of oscillatory responses of skate electroreceptors.Journal of General Physiology 73, 703–23.

    PubMed  Google Scholar 

  • Clusin, W. T., Spray, D. C. &Bennett, M. V. L. (1975) Activation of a voltage-sensitive conductance by inward calcium current.Nature 256, 425–7.

    PubMed  Google Scholar 

  • Derbin, C. (1970) Effets de la section du nerf lateral sur les jonctions sensorineurales des ampoules de Lorenzini de la torpille,Torpedo marmorata.Journal de Microscopie 9, 119–26.

    Google Scholar 

  • Dotterweich, H. (1931) Bau und Function der Lorenzini'sehen Ampullen.Zoologische Jahrbucher Physiologie 50, 347–417.

    Google Scholar 

  • Dragsten, P. R., Blumenthal, R. &Handler, J. S. (1981) Membrane asymmetry in epithelia: is the tight junction a barrier to diffusion in the plasma membrane?Nature 294, 718–22.

    PubMed  Google Scholar 

  • Franzini-Armstrong, C. (1976) Freeze-fracture of excitatory and inhibitory synapses at crayfish neuromuscular junctions.Journal de Microscopie et de Biologie Cellulaire 25, 217–22.

    Google Scholar 

  • GulleY, R. L. &Reese, T. S. (1976) Intercellular junctions in the reticular lamina of the organ of Corti.Journal of Neurocytology 5, 479–507.

    PubMed  Google Scholar 

  • Heuser, J. E. &Reese, T. S. (1977) Structure of the synapse. InHandbook of Physiology -The Nervous System, Vol. 1 (edited byKandel, E.). pp. 261–94. Washington DC: American Physiological Society.

    Google Scholar 

  • Heuser, J. E. &Reese, T. S. (1979) Changes in the structure of presynaptic membranes during transmitter secretion. InNeurobiology of Chemical Transmission (edited byOtsuka, M. &Hall, Z.), pp. 3–11. New York: John Wiley and Sons.

    Google Scholar 

  • Heuser, J. E. &Reese, T. S. (1981) Structural changes after transmitter release at the frog neuromuscular junction.Journal of Cell Biology 88, 564–80.

    PubMed  Google Scholar 

  • Kalmijn, A. J. (1966) Electroreception in sharks and rays.Nature 212, 1232–3.

    Google Scholar 

  • Kalmijn, A. J. (1974) The detection of electric fields from inanimate sources other than electric organs. InHandbook of Sensory Physiology. Vol III 3, Electroreceptors and other Specialized Receptors in Lower Vertebrates (edited byFessard, A.), pp. 12–58. Berlin: Springer-Verlag.

    Google Scholar 

  • Landis, D. M. D. &Reese, T. S. (1974) Differences in membrane structure between excitatory and inhibitory synapses in cerebellar cortex.Journal of Comparative Neurology 155, 93–126.

    PubMed  Google Scholar 

  • Landis, D. M. D., Reese, T. S. &Raviola, E. (1974) Differences in membrane structure between excitatory and inhibitory components of the reciprocal synapse in the olfactory bulb.Journal of Comparative Neurology 155, 67–92.

    PubMed  Google Scholar 

  • Murray, R. W. (1962) The responses of the ampullae of Lorenzini of elasmobranchs to electrical stimulation.Journal of Experimental Biology 39, 119–28.

    PubMed  Google Scholar 

  • Obara, S. &Bennett, M. V. L. (1972) Mode of operation of ampullae of Lorenzini of the skate,Raja. Journal of General Physiology 60, 534–57.

    Google Scholar 

  • Osborne, M. P. (1977) Role of vesicles with some observations on vertebrate sensory cells. InSynapses: Proceedings of an International Symposium (edited byCottrell, G. A. &Usherwood, P. N. R.), pp. 40–63. New York: John Wiley and Sons.

    Google Scholar 

  • Pumplin, D. W., Reese, T. S. &Llinas, R. (1981) Are the presynaptic membrane particles the calcium channels?Proceedings of the National Academy of Sciences USA 78, 7210–3.

    Google Scholar 

  • Raviola, E. &Gilula, N. B. (1975) Intramembrane organization of specialized contacts in the outer plexiform layer of the retina.Journal of Cell Biology 65, 192–222.

    PubMed  Google Scholar 

  • Rheuben, M. B. &Reese, T. S. (1978) Three-dimensional structure and membrane specializations of moth excitatory neuromuscular synapses.Journal of Ultrastructure Research 65, 95–111.

    PubMed  Google Scholar 

  • Saito, K. (1980) Fine structure of the sensory epithelium of the guinea pig organ of Corti: afferent and efferent synapses of hair cells.Journal of Ultrastructure Research 71, 222–32.

    PubMed  Google Scholar 

  • Schaeffer, S. F. &Raviola, E. (1978) Membrane recycling in the cone cell endings of the turtle retina.Journal of Cell Biology 79, 802–25.

    PubMed  Google Scholar 

  • Schaeffer, S. F., Raviola, E. &Heuser, J. E. (1982) Membrane specializations in the outer plexiform layer of the turtle retina.Journal of Comparative Neurology,204, 253–67.

    PubMed  Google Scholar 

  • Sejnowski, T. J. &Yodlowski, M. L. (1978) A freeze-fracture study of the skate electroreceptor.Biological Bulletin 155, 465.

    Google Scholar 

  • Staehelin, L. A. (1974) Structure and function of intercellular junctions.International Review of Cytology 39, 191–283.

    PubMed  Google Scholar 

  • Szabo, T. (1972) Ultrastructural evidence for a mechanoreceptor function of the ampullae of Lorenzini.Journal de Microscopie 14, 343–50.

    Google Scholar 

  • Szabo, T. (1974) Anatomy of the specialized lateral line organs of electroreceptors. InHandbook of Sensory Physiology. Vol III 3. Electroreceptor and other Specialized Receptors in Lower Vertebrates (edited byFessard, A.), pp. 12–58. Berlin: Springer-Verlag.

    Google Scholar 

  • Waltman, B. (1966) Electrical properties and fine structure of the ampullary canals of Lorenzini.Acta Physiologica Scandanavica 66 Suppl. 264, 1–60.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sejnowski, T.J., Yodlowski, M.L. A freeze-fracture study of the skate electro receptor. J Neurocytol 11, 897–912 (1982). https://doi.org/10.1007/BF01148307

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01148307

Keywords

Navigation