Summary
Sternarchus emits low voltage biphasic pulses at about 700–900/s. These signals (and changes in them caused by external objects) are detected by the tuberous or phasic electroreceptors. We used electron microscopy to examine extracellular compartments in the current pathway to the receptor cells, which are delineated by cells joined by tight junctions. Highly specialized accessory cells were found to separate the receptor cells from the extracellular space continuous with the exterior. Except for synaptic specializations complements of intramembrane particles of cell membranes were unremarkable and did not correlate with presumed high and low resistivity. We propose an equivalent electrical circuit that is consistent with the morphological and physiological observations.
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References
Akert, K., Sandri, C., Weibel, E. R., Peper, K. &Moor, H. (1976). The fine structure of the perineural endothelium.Cell and Tissue Research 165, 281–95.
Bennett, M. V. L. (1967) Mechanisms of electroreception. InLateral Line Detectors (edited byP. Cahin), pp. 313–93. Bloomington: Indiana University Press.
Bennett, M. V. L. (1971a) Electric organs. InFish Physiology, Vol. 5 (edited byW. S. Hoar &D. J. Randall), pp. 347–491. New York: Academic Press.
Bennett, M. V. L. (1971b) Electroreception. InFish Physiology, Vol. 5 (edited byW. S. Hoar &D. J. Randall), pp. 493–568. New York: Academic Press.
Bennett, M. V. L., Pappas, G. D., Gimenez, M. &Nakajima, Y. (1967) Physiology and ultrastructure of elec-trotonic junctions. IV. Medullary electromotor nuclei in gymnotid fish.Journal of Neurophysiology 30, 236–300.
Bullock, T. H. &Heiligenberg, W. (1986)Electroreception. New York: Wiley.
Bullock, T. H., Behrend, K. &Heiligenberg, W. (1975) Comparison of the jamming avoidance responses in gymnotid and gymnarchid electric fish: a case of convergent evolution of behaviour and its sensory basis.Journal of Comparative Physiology 103, 97–121.
Ellis, M. M. (1913) The gymnotid eels of tropical America.Memoirs of the Carnegie Museum 6, 109–204.
Enger, P. S. &Szabo, T. (1965) Activity of central neurons involved in electroreception in some weakly electric fish (Gymnotidae).Journal of Neurophysiology 28, 800–18.
Gulley, R. L. &Reese, T. S. (1977) Freeze-fracture studies on the synapses in the organ of Corti.Journal of Comparative Neurology 171, 517–543.
Hagiwara, S., Szabo, T. &Enger, P. S. (1965) Electro-receptor mechanisms in a high frequency weakly electric fish.Sternarchus albifrons. Journal of Neurophysiology 28, 784–99.
Hamilton, D. W. (1968) The caliceal synapse of Type I vestibular hair cells.Journal of Ultrastructure Research 23, 98–114.
Highstein, S. M. &Bennett, M. V. L. (1975) Fatigue and recovery of transmission at the Mauthner fiber-giant fiber synapse of the hatchetfish.Brain Research 98, 229–42.
Hopkins, C. D. (1976) Stimulus filtering and electro-reception: tuberous electroreceptors in three species of gymnotoid fish.Journal of Comparative Physiology 111, 171–207.
Kristol, C., Akert, K., Sandri, C., Wyss, U. R., Bennett, M. V. L. &Moor, H. (1977) The Ranvier nodes in the neurogenic electric organ of the knifefishSternarchus: A freeze-etching study on the distribution of membrane-associated particles.Brain Research 125, 197–212.
Lissmann, H. W. &Mullinger, A. M. (1968) Organization of ampullary electric receptors inGymnotidae (pisces).Proceedings of the Royal Society London B 169, 345–78.
Luciano, L., Franke, K., Iurata, S. &Reale, E. (1977) Freeze-fracture study of the cell junctions in the utricle and saccule.Acta Otolaryngologica 83, 79–84.
Moor, H. &Muehlethaler, K. (1963) Fine structure in frozen etched yeast cells.Journal of Cell Biology 17, 609–628.
Mullinger, A. M. (1969) The organization of ampullary sense organs in the electric fish,Gymnarchus niloticus.Tissue and Cell 1, 31–52.
Neeman, Z., Spira, M. E. &Bennett, M. V. L. (1980) Formation of gap and tight junctions between reaggre-gated blastomeres of the killifish,Fundulus.American Journal of Anatomy 158, 251–62.
Pappas, G. D., Waxman, S. G. &Bennett, M. V. L. (1975) Morphology of spinal electromotor neurons and presy-naptic coupling in the gymnotidSternarchus albifrons.Journal of Neurocytology 4, 469–478.
Raviola, E. &Gilula, N. B. (1975) Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits.Journal of Cell Biology 65, 192–222.
Sardet, C., Pisam, M. &Maetz, J. (1977) The surface epithelium of teleostean fish gills. Cellular and junctional adaptations of the chloride cell in relation to salt adaptation.Journal of Cell Biology 80, 96–117.
Scheich, H. &Bullock, T. H. (1974) The role of electro-receptors in the animal's life. II. The detection of electric fields from electric organs. InHandbook of Sensory Physiology, Vol. II/3 (edited byFessard, A.), pp. 200–256. New York: Springer.
Srivastava, C. B. L. (1972) Morphological evidence for electrical synapse of ‘gap’ junction type in another vertebrate receptor.Experientia 28, 1029–30.
Srivastava, C. B. L. (1973) Peripheral nerve ending types in tuberous electroreceptors of a high frequency gymnotid,Sternarchus albifrons.Journal of Neurocytology 2, 77–83.
Srivastava, C. B. L. &Szabo, T. (1974) Auxiliary structures of tuberous organ (electroreceptor) ofSternarchus albifrons (Gymnotidae).Journal of Ultrastructure Research 48, 69–91.
Szabo, T. (1965) Sense organs of the lateral line system in some electric fish of the Gymnotidae, Mormyridae and Gymnarchidae.Journal of Morphology 117, 229–50.
Szabo, T. &Fessard, A. (1974) Physiology of electroreceptors. InHandbook of Sensory Physiology III/3 (edited byFessard, A.), pp. 57–124. New York: Springer.
Szamier, R. B. &Bennett, M. V. L. (1974) Special cutaneous receptor organs of fish. VII. Arnpullary organs of mormyrids.Journal of Morphology 143, 365–84.
Szamier, R. B. &Wachtel, A. W. (1970) Special cutaneous receptors of fish. VI. Ampullary and tuberous organs ofHypopomus.Journal of Ulstrastructure Research 30, 450–71.
Tokunaga, A., Akert, K., Sandri, C. &Bennett, M. V. L. (1980) Cell types and synaptic organization of the medullary electromotor nucleus in a constant frequency weakly electric fish,Sternarchus albifrons.Journal of Comparative Neurology 192, 407–26.
Viancour, T. A. (1979) Peripheral electrosense physiology: a review of recent findings.Journal de Physiologie, Paris 75, 321–33.
Wachtel, A. W. &Szamier, R. B. (1966) Special cutaneous receptor organs of fish: The tuberous organs ofEigen-mannia.Journal of Morphology 119, 51–80.
Waxman, S. G., Pappas, G. D. &Bennett, M. V. L. (1972) Morphological correlates of functional differentiation of nodes of Ranvier along single fibers in the neurogenic electric organic of the knife fishSternarchus.Journal of Cell Biology 53, 210–24.
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Bennett, M.V.L., Sandri, C. & Akert, K. Fine structure of the tuberous electroreceptor of the high-frequency electric fish,Sternarchus albifrons (gymnotiformes). J Neurocytol 18, 265–283 (1989). https://doi.org/10.1007/BF01206667
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DOI: https://doi.org/10.1007/BF01206667