Significance of Findings on Electroreception for General Neurobiology

  • Theodore H. Bullock


Electroreceptors and their central pathways belong to the octavolateral system and offer many contrasts and similarities to lateral line, auditory, and vestibular reception. Some of the contrasts are based on the presumption that electroreception involves no mechanical steps in transduction, whereas the other octavolateral modalities are mechanical but may involve an electrical step in transduction. The finding that electroreceptors work as voltmeters and govern transmitter release by small changes in membrane potential raises a question that goes beyond these closely related modalities: Is it possible that some other sensory or central cells also come under the influence of weak extracellular fields? Among the phenomena of general neurobiological interest that are particularly obvious or accessible in electric sense cells are ultrastructural changes in ribbon synapses with activity; tight junctions around sense cells far from their equator, causing asymmetrical voltage drops across apical and basal membranes; loss of stereocilia and variations in kinocilia; absence of centrifugal nerve fibers to the sense cells; resonance of receptors at their best excitatory frequency—and the plastic alteration of such individual tuning, in development and with hormones; a variety of receptor types in respect to the way the afferent axon encodes stimulus parameters; and lifelong addition of sense cells to a presumably fixed number of afferent axons.

Central representation and processing provide examples of four parallel body maps in the first-order medullary nucleus converging on a single laminar stack of congruent maps in the midbrain nucleus equivalent to the inferior colliculus; computed maps of the best dipole axis; parallel pathways for different submodalities; and various schemes for dealing with reafference, with and without corollary discharges, some central expectations being plastic. Electrical sensing offers instructive evidence of convergence giving improved resolution, larger and more complex receptive fields, direction specificity, and best distance units; central filtering added to peripheral tuning; different amplitude modulation (AM) best frequencies that may shift with modulation depth; and an increased adaptation rate in medullary nuclei due to descending projections. One form of normal social behavior, the jamming avoidance response, is rather fully understood through some 14 orders of neurons, from receptor to effector, and illustrates a distributed, "parliamentary," high-precision mechanism.

Brain regions with equivalents in other vertebrates that have yielded particularly rich details, anatomically or physiologically, include the primary nuclei in the octavolateral medulla, torus semicircularis, tectum, and cerebellum. Each is specialized in some species, often elaborately.

Sensorimotor integration is illuminated by favorable preparations for examining parameters of response control. Electroreception includes the active mode in which electric signals are generated by the animal's own electric organ discharges (EODs), and it includes communication by modulation of EODs; therefore this volume includes some aspects of the diverse forms of electric organs and their control. High-precision biological clocks and their fine modulation; the use of electrical and chemical synapses; devices for synchronization; and extreme specialization of Ranvier nodes are among the adaptations of general interest. Regeneration of the spinal cord extends to reconstitution of the cellular detail.

Ethological comparisons among the species in respect to electroreception touch upon orientation, object location, communication, and other uses. Ecological comparisons raise general questions such as those regarding the sources of signals and noise. Evolutionary comparisons reveal a wealth of detail on convergent development of effector and receptor organs, central pathways, and physiological and behavioral adaptations.


Hair Cell Lateral Line Sense Cell Electric Organ Electric Organ Discharge 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bell, C. C. (1984). Effects of motor commands on sensory inflow, with examples from electric fish. In: Comparative Physiology of Sensory Systems ( L. Bolls, R. D. Keynes and S. H. P. Maddrell, Eds.), pp. 637 - 647. Cambridge: Cambridge Univ. Press.Google Scholar
  2. Bombardieri, R. A. and Feng, A. S. (1977). Deficit in object detection (electrolocation) following interruption of cerebellar function in the weakly electric fish Apteronotus albifrons. Brain Res. 130, 343 - 347.CrossRefGoogle Scholar
  3. Bretschneider, F., De WeiIle, J. R. and Klis, J. F. L. (1985). Functioning of catfish electroreceptors: Fractional-order filtering and non-linearity. Comp. Biochem. Physiol. 80A, 191 - 198.CrossRefGoogle Scholar
  4. Brownell, W. E., Bader, C. R., Bertrand, D. and de Ribaupierre, Y. (1985). Evoked mechanical responses of isolated cochlear outer hair cells. Science 227, 194-1%.Google Scholar
  5. Bullock, T. H. (1981). Comparisons of the electric and acoustic senses and their central sensory processing. In: Hearing and Sound Communication in Fishes (W. N. Tavolga, A. N. Popper and R. R. Fay, Eds.), pp. 525-571. New York: Springer-Verlag. Bullock, T. H. (1982). Electroreception. Annu. Rev. Neurosci. 5, 121-170.Google Scholar
  6. Bullock, T. H., Behrend, K. and Heiligenberg, W. (1975). Comparison of the jamming avoidance responses in gymnotoid and gymnarchid electric fish: A case of convergent evolution of behavior and its sensory basis. J. Comp. Physiol. 103, 97 - 121.CrossRefGoogle Scholar
  7. Electroreception for General Neurobiology 673Google Scholar
  8. Bullock, T. H., Bodznick, D. A. and Northcutt, R. G. (1983). The phvlogenetic distribution of electroreception: Evidence for convergent evolution of a primitive vertebrate sense modality. Brain Res. Rev. 6, 25 - 46.CrossRefGoogle Scholar
  9. Bullock, T. H., Northcutt, R. G. and Bodznick, D. A. (1982). Evolution of electroreception. Trends Neurosci. 5, 50 - 53.CrossRefGoogle Scholar
  10. Corwin, J. T. (1981). Postembryonic production and aging of inner ear hair cells in sharks. J. Comp. Neurol. 201, 541 - 553.CrossRefGoogle Scholar
  11. Corwin, J. T. (1985). Perpetual production of hair cells and maturational changes in hair cell ultrastructure accompany postembryonic growth in an amphibian ear. Proc. Natl. Acad. Sci. U.S.A. 82, 3911 - 3915.CrossRefGoogle Scholar
  12. Echteler, S. M. (1985). Organization of central auditory pathways in a teleost fish, Cyprinus carpio. J. Comp. Physiol. 156, 267 - 280.CrossRefGoogle Scholar
  13. Fields, R. D. (1985). Structural and functional plasticity of the ribbon synapse in the ampullae of Lorenzini. Ph.D. Thesis, University of California, San Diego.Google Scholar
  14. Fields, R. D. and Ellisman, M. H. (1985). Synaptic morphology and differences in sensitivity. Science 228, 197 - 199.CrossRefGoogle Scholar
  15. Hopkins, C. D. (1973). Lightning as background noise for communication among electric fish. Nature (Land.), 242, 268 - 270.CrossRefGoogle Scholar
  16. Kalmijn, A. J. (1974). The detection of electric fields from inanimate and animate sources other than electric organs. In: Handbook of Sensory Physiology, Vol. II1/3 ( A. Fessard, Ed.), pp. 147 - 200. Berlin: Springer-Verlag.Google Scholar
  17. Kalmijn, A. J. (1984). Theory of electromagnetic orientation: A further analysis. In: Comparative Physiology of Sensory Systems (L. Bolls, R. D. Keynes and S. H. P. Maddrell, Eds.), pp. 525 - 560. Cambridge: Cambridge Univ. Press.Google Scholar
  18. Kalmijn, A. J. (1986). Detection of weak electric fields. In: Sensory Biology of Aquatic Animals (J. Atema, R. Fay, A. Popper and W. Tavolga, Eds.). New York: Springer-Verlag, in press.Google Scholar
  19. Kleerekoper, H. and Sibakin, K. (1956). An investigation of the electrical "spike" potentials produced by the sea lamprey (Petromyzon marinus) in the water surrounding the head region. I. J. Fish. Res. Board Can. 13, 373 - 383.CrossRefGoogle Scholar
  20. Kleerekoper, H. and Sibakin, K. (1957). An investigation of the electrical "spike" potentials produced by the sea lamprey (Petromyzon marinus) in the water surrounding the head region. II. J. Fish. Res. Board. Can. 14, 145 - 151.CrossRefGoogle Scholar
  21. Knudsen, E. I. (1976a). Midbrain responses to electroreceptive input in catfish; Evidence of orientation preferences and somatotopic organization. J. Comp. Physiol. 106, 51 - 67.Google Scholar
  22. Knudsen, E. I. (1976b). Midbrain units in catfish: Response properties to electroreceptive input. J. Comp. Physiol. 109, 315 - 335.CrossRefGoogle Scholar
  23. Lee, L. T. (1984). Response of the cerebellum to stimulation of the telencephalon in the catfish (Ictalurus nebulosus). J. Neurophysiol. 51, 1394 - 1408.Google Scholar
  24. Meyer, D. L., Heiligenberg, W. and Bullock, T. H. (1976). The ventral substrate response. A new postural control mechanism in fishes. J. Comp. Physiol. 109, 59 - 68.CrossRefGoogle Scholar
  25. Meyer, J. H. (1982). Behavioral responses of weakly electric fish to complex impedances. J. Comp. Physiol. 145, 459 - 470.CrossRefGoogle Scholar
  26. Montgomery, J. C. (1984). Noise cancellation in the electrosensory system of the thomback ray: Common mode rejection of input produced by the animal's own ventilatory movement. J. Comp. Physiol. 155, 103 - 111.CrossRefGoogle Scholar
  27. Perkel, D. H. Sr Bullock, T. H. (1968). Neural coding. Neurosci. Res. Program Bull. 6, 221-348. Schaeffer, S. F. and Raviola, A. E. (1978). Membrane recycling in the cone cell endings of the turtle retina. J. Cell Biol. 79, 802 - 825.Google Scholar
  28. Scheich, H. (1974a). Pattern recognition and control of an avoidance behaviour by midbrain neurones in electric fish. Brain Res. 66, 354 - 355.CrossRefGoogle Scholar
  29. Scheich, H. (1974b). Neuronal analysis of wave form in the time domain: Midbrain units in electric fish during social behavior. Science 185, 365 - 367.CrossRefGoogle Scholar
  30. Scheich, H. and Bullock, T. H. (1974). The detection of electric fields from electric organs. In: Handbook of Sensory Physiology Vol. 1I1/3 ( A. Fessard, Ed.), pp. 201 - 256. Berlin: Springer-Verlag.Google Scholar
  31. Scheich, H., Langner, G., Tidemann, C., Coles, R. and Guppy, A. (1986). Electroreception and electrolocation in Platypus. Nature (Lund.), 319, 401 - 402.CrossRefGoogle Scholar
  32. Schweitzer, J. and Lowe, D. (1984). Mesencephalic and diencephalic cobalt-lysine injections in an elasmobranch: Evidence for two parallel electrosensory pathways. Neurosci. Lett. 44, 317 - 322.CrossRefGoogle Scholar
  33. Shambes, G. M., Gibson, J. M. and Walker, W. (1978). Fractured somatotopy in granule cell tactile areas of rat cerebellar hemispheres revealed by micromapping. Brain Behay. Evol. 15, 94 - 140.CrossRefGoogle Scholar
  34. Terzuolo, C. A. and Bullock, T. H. (1956). Measurement of imposed voltage gradient adequate to modulate neuronal firing. Proc. Natl. Acad. Sci. U.S.A. 42, 687-694.)Google Scholar
  35. Theron, J. J., Bingio, R. and Meyer, A. C. (1981). Circadian changes in microtubules, synaptic ribbons and synaptic ribbon fields in the pinealocytes of the baboon (Papio ursinus R). Cell Tissue Res. 217, 405 - 413.CrossRefGoogle Scholar
  36. Trujillo-Cenóz, O., Echague, J. A. and Macadar, O. (1984). Innervation pattern and electric organ discharge waveform in Gymnotus carapo (Teleostei; Gymnotiformes). J. Neurobiol. 15, 273 - 281.CrossRefGoogle Scholar
  37. Wagner, H.-J. (1980). Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedides of fish retinas. J. Neurocytol. 9, 591 - 602.CrossRefGoogle Scholar
  38. De Weille, J. R. (1983). Electrosensory information processing by lateral-line lobe neurons of catfish investigated by means of white noise cross-correlation. Comp. Biochem. Physiol. 74A, 677 - 680.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Theodore H. Bullock
    • 1
  1. 1.University of CaliforniaNeurobiology Unit Scripps Institution of Oceanography and Department of NeurosciencesSan Diego La JollaUSA

Personalised recommendations