Journal of comparative physiology

, Volume 127, Issue 3, pp 267–286 | Cite as

The Jamming Avoidance Response inEigenmannia revisited: The structure of a neuronal democracy

  • Walter Heiligenberg
  • Curtis Baker
  • Joanne Matsubara
Article

Summary

The Jamming Avoidance Response (JAR) is a gradual shift in frequency of the fish's electric organ pacemaker in an attempt to increase a small difference,δf, between the fundamental frequency of electric organ discharges (EODs) of a conspecific and that of the animal's own EODs. The JAR can be elicited in curarized animals by replacing the silenced EOD with a periodic electric stimulus, S1; and by simulating EODs of a conspecific with a periodic stimulus, S2, whose frequency differs byδf from the frequency of S1. Similar to the natural JAR, the frequency of the pacemaker will rise and fall in response to negative and positiveδfs respectively, provided that S1; but not S2, shares critical features with the EOD of the animal. Ambivalent or even opposite responses (Anti-JARs) may result if S1 lacks critical EOD features (Fig. 1). In search of these features the following results were obtained.
  1. 1.

    To elicit JARs, S1 need not be phaselocked to the pacemaker. The JAR can thus be driven exclusively by electroreceptive afference, without reference to the pacemaker.

     
  2. 2.

    S1 and S2 may be pure sinewaves as long as their field geometries differ sufficiently. Higher harmonics, which may be added to a sinewave to mimic the EOD wave shape, are required only if S1 and S2 have identical geometries, i.e., if they are presented through the same pair of electrodes. The animal may thus use two different strategies to determine the sign of theδf: one which is based on differences in stimulus field geometries and one which is based on the presence of higher harmonics. Only the former is considered in the following.

     
  3. 3.

    The S1, but not the S2, field geometry should approximate the natural EOD field geometry. To the extent that this condition is violated, sufficiently high S2 intensities may elicit Anti-JARs (Fig. 4).

     
  4. 4.

    Evidence is given that the JAR is controlled, in a cumulative manner, by local interactions of neighboring electroreceptive fields on the animal's body surface which, as a consequence of different S1 and S2 field geometries, experience different degrees of contamination of S1 by S2. Simultaneous stimulations of remote areas of body surface result in almost linear summation of their associated effects on the pacemaker (Figs. 5, 6). Theoretically, no unitary central EOD representation is required.

     
  5. 5.

    Based on the results in 3. und 4., we propose that correct JARs are elicited to the extent that the majority of electroreceptors is predominantly driven by Sl rather than by S2, and this condition is fulfilled to the extent that the S1 field geometry approximates that of the natural EOD.

     
  6. 6.

    Effective S2 stimuli have a periodicity near that of the EOD (S1) fundamental frequency, f. This includes all stimuli with a power peak at a frequency of n·f+δf, n=l,2,3,t (Fig. 2), with the optimalδf being 3 to 8 Hz and identical for all n. Such stimuli cause consistent distortions in successive EODs (S1 pulses), which gradually travel through the EOD (S1) cycle (Fig. 3). This “motion” leads to periodic fluctuations in the amplitude of the joint signal, EOD (S1)+S2, and the phase of its positive zero-crossings with regard to those of the EOD (S1 (Fig. 7). The modulation of these two variables can be represented by a motion along a closed graph in a two-dimensional state plane (Fig. 8), which is reproducedδf times per s. The direction of motion along this graph reflects the sign of theδf. Evidence is given that this motion is detected by a mechanism comparable to a motion detector in the realm of vision.

     

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References

  1. Briggs, B.H., Phillips, G.J., Shinn, D.H.: The analysis of observaions on spaced receivers of the fading of radio signals. Proc. Phys. Soc. London63, 106–121 (1950)Google Scholar
  2. Bullock, T.H., Behrend, K., Heiligenberg, W.: Comparison of the jamming avoidance response in gymnotoid and gymnarchid electric fish: A case of convergent evolution of behavior and its sensory basis. J. comp. Physiol.103, 97–121 (1975)Google Scholar
  3. Bullock, T.H., Chichibu, S.: Further analysis of sensory coding in electroreceptors of electric fish. Proc. Natl. Acad. Sci.54, 422–29 (1965)Google Scholar
  4. Bullock, T.H., Hamstra, R.H., Scheich, H.: The jamming avoidance response of high frequency electric fish. J. comp. Physiol.77, 1–48 (1972)Google Scholar
  5. Feng, A.S.: The effect of temperature on a social behavior of weakly electric fish,Eigenmannia virescens. Comp. Biochem. Physiol.55A, 99–102 (1976)Google Scholar
  6. Hassenstein, B., Reichardt, W.: Wie sehen Insekten Bewegungen? Umschau10, 302–305 (1959)Google Scholar
  7. Heiligenberg, W.: Electrolocation of objects in the electric fish,Eigenmannia (Rhamphichthyidae, Gymnotoidei). J. comp. Physiol.87, 137–164 (1973)Google Scholar
  8. Heiligenberg, W.: Principles of electrolocation and jamming avoidance in electric fish. Studies of brain function, Vol. 1, pp. 1–85. Berlin-Heidelberg-New York: Springer 1977Google Scholar
  9. Heiligenberg, W., Altes, R.: Phase sensitivity in electroreception. Science199, 1001–1004 (1978)Google Scholar
  10. Heiligenberg, W., Baker, C., Bastian, J.: The jamming avoidance response in gymnotoid pulse-species: A mechanism to minimize the probability of pulse-train coincidence. J. comp. Physiol.,124, 211–224 (1978)Google Scholar
  11. Hopkins, C.D.: Stimulus filtering and electroreception: Tuberous electroreceptors in three species of gymnotoid fish. J. comp. Physiol.111, 171–208 (1976)Google Scholar
  12. Matsubara, J., Heiligenberg, W.: How well do electric fish electrolocate under jamming? J. comp. Physiol.,125, 285–290 (1978)Google Scholar
  13. Mitra, S.N.: A radio method of measuring winds in the ionospere. Proc. IEEE (Part III)96, 441 (1949)Google Scholar
  14. Reichardt, W.: Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. In: Sensory communication (ed. W.A. Rosenblith), pp. 303–317. Cambridge, Massachusetts: MIT Press 1961Google Scholar
  15. Scheich, H.: Neural analysis of wave form in the time domain: Midbrain units in electric fish during social behavior. Science185, 365–367 (1974)Google Scholar
  16. Scheich, H.: Neural basis of communication in the high frequency electric fishEigenmannia virescens (Jamming avoidance response). J. comp. Physiol.113, 181–255 (1977)Google Scholar
  17. Scheich, H., Bullock, T.H.: The role of electroreceptors in the animal's life. II. The detection of electric fields from electric organs. In: Handbook of sensory physiology, Vol. 3/3 (ed. A. Fessard). Berlin-Heidelberg-New York: Springer, 1974Google Scholar
  18. Scheich, H., Maler, L.: Laminar organization of the torus semicircularis related to the input from two types of electroreceptors. Exp. Brain Res. Suppl.I, 565–567 (1976)Google Scholar
  19. Scheich, H., Bullock, T.H., Hamstra, R.H.: Coding properties of two classes of afferent nerve fibers: High frequency electroreceptors in the electric fish,Eigenmannia. J. Neurophysiol.36, 39–60 (1973)Google Scholar
  20. Scheich, H., Gottschalk, B., Nickel, B.: The jamming avoidance response inRhamphichthys rostratus: An alternative principle of time domain analysis in electric fish. Exp. Brain Res.28, 229–233 (1977)Google Scholar
  21. Schlegel, P.: Electroreceptive single units in the magnocellular mesencephalic nucleus of the weakly electric fishGymnotus carapo. Exp. Brain Res.29, 201–218 (1977)Google Scholar
  22. Watanabe, A., Takeda, K.: The change of discharge frequency by A.C. stimulus in a weakly electric fish. J. exp. Biol.40, 57–66 (1963)Google Scholar

Copyright information

© Springer-Verlag 1978

Authors and Affiliations

  • Walter Heiligenberg
    • 1
  • Curtis Baker
    • 1
  • Joanne Matsubara
    • 1
  1. 1.Neurobiology Unit, Scripps Institution of OceanographyUniversity of CaliforniaSan Diego, La JollaUSA

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