Skip to main content
Log in

Independently evolved jamming avoidance responses employ identical computational algorithms: a behavioral study of the African electric fish, Gymnarchus niloticus

  • Original Articles
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

An African electric fish, Gymnarchus, and a South American electric fish, Eigenmannia, are believed to have evolved their electrosensory systems independently. Both fishes, nevertheless, gradually shift the frequency of electric organ discharge away when they encounter a neighbor of a similar discharge frequency. Computational algorithms employed by Gymnarchus for this jamming avoidance response have been identified in this study for comparison with those of extensively studied Eigenmannia.

  1. 1.

    Gymnarchus determines whether it should raise or lower its discharge frequency based solely upon the signal mixture of its own reafferent and the exafferent signal from a neighbor, and does not internally refer to the pacemaker command signal which drives its own discharge.

  2. 2.

    The signal mixture is analyzed in terms of the time courses of amplitude modulation and phase modulation at each area of the body surface.

  3. 3.

    Phase of the signal mixture at each area is compared with that of another area for the detection of phase modulation.

  4. 4.

    Unambiguous information necessary for the jamming avoidance response is extracted by integrating information from all body areas each of which yields ambiguous information.

  5. 5.

    These computational features are identical to those of Eigenmannia, suggesting that the neural circuit for jamming avoidance responses may have evolved from preexisting mechanisms for electrolocation in both fishes.

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

Abbreviations

EOD:

Electric Organ Discharge

Δf :

frequency difference between f 2 and f 1. Δf=f 2f 1

f 1 :

frequency of S1 or of fish's own EOD

f 2 :

frequency of S2, or of neighbor's EOD

JAR:

Jamming Avoidance Response

S1 :

sinusoidal stimulus simulating fish's own EOD

S2 :

sinusoidal stimulus simulating neighbor's EOD

References

  • Bass AH, Hopkins CD (1982) Comparative aspects of brain organization of an African “wave” electric fish, Gymnarchus niloticus. J Morphol 174:313–334

    Google Scholar 

  • Bastian J, Heiligenberg W (1980) Neural correlates of the jamming avoidance response of Eigenmannia. J Comp Physiol 136:135–152

    Google Scholar 

  • Bell CC (1986a) Electroreception in mormyrid fish: Central anatomy. In: Bullock TH, Heiligenberg W (eds) Electroreception. John Wiley and Sons, New York, pp 375–421

    Google Scholar 

  • Bell CC (1986b) Electroreception in mormyrid fish: Central physiology. In: Bullock TH, Heiligenberg W (eds) Electroreception. John Wiley and Sons, New York, pp 423–464

    Google Scholar 

  • Bullock TH, Hamstra RH, Scheich H (1972a) The jamming avoidance response of high frequency electric fish. I. General features. J Comp Physiol 77:1–22

    Google Scholar 

  • Bullock TH, Hamstra RH, Scheich H (1972b) The jamming avoidance response of high frequency electric fish. II. Quantitative aspects. J Comp Physiol 77:23–48

    Google Scholar 

  • Bullock TH, Behrend K, 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

    Google Scholar 

  • Carr CE, Heiligenberg W, Rose GJ (1986a) A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology. J Neurosci 6(1): 107–119

    Google Scholar 

  • Carr CE, Maler L, Taylor B (1986b) A time-comparison circuit in the electric fish midbrain. II. Functional morphology. J Neurosci 6(5): 1372–1383

    Google Scholar 

  • Dumont JPC, Robertson RM (1986) Neuronal circuits: An evolutionary perspective. Science 233:849–853

    Google Scholar 

  • Finger TE, Bell CC, Carr CE (1986) Comparisons among electroreceptive teleosts: Why are electrosensory systems so similar? In: Bullock TH, Heiligenberg W (eds) Electroreception. John Wiley and Sons, New York, pp 465–481

    Google Scholar 

  • Getting PA (1988) Comparative analysis of invertebrate central pattern generators. In: Cohen AH, Rosignol S, Grillner S (eds) Neural control of rhythmic movements. Wiley, New York, pp 101–128

    Google Scholar 

  • Getting PA (1989) Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12:185–204

    Google Scholar 

  • Heiligenberg W (1975) Electrolocation and jamming avoidance in the electric fish Gymnarchus niloticus (Gymnarchidae, Mormyriformes). J Comp Physiol 103:55–67

    Google Scholar 

  • Heiligenberg W (1977) Principles of electrolocation and jamming avoidance in electric fish — A neuroethological approach. Studie of Brain Function, vol.1. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Heiligenberg W (1987) Central processing of sensory information in electric fish. J Comp Physiol A 161:621–631

    Google Scholar 

  • Heiligenberg W (1989) Coding and processing of electrosensory information in gymnotiform fish. J Exp Biol 146:255–275

    Google Scholar 

  • Heiligenberg W (1991) Neural nets in electric fish. The MIT Press, Cambridge

    Google Scholar 

  • Heiligenberg W, Bastian J (1980) The control of Eigenmannia's pacemaker by distributed evaluation of electroreceptive afferences. J Comp Physiol 136:113–133

    Google Scholar 

  • Heiligenberg W, Kawasaki M (1992) An internal current source yields immunity of electrosensory information processing to unusually strong jamming in electric fish. J Comp Physiol A 171:309–316

    Google Scholar 

  • Heiligenberg W, Rose G (1985) Phase and amplitude computations in the midbrain of an electric fish: Intracellular studies of neurons participating in the jamming avoidance response of Eigenmannia. J Neurosci 5:515–531

    Google Scholar 

  • Heiligenberg W, Rose G (1986) Gating of sensory information: Joint computations of phase and amplitude data in the midbrain of the electric fish, Eigenmannia. J Comp Physiol A 159:311–324

    Google Scholar 

  • Heiligenberg W, Baker C, Matsubara J (1978) The jamming avoidance response in Eigenmannia revisited: The structure of a neuronal democracy. J Comp Physiol 127:267–286

    Google Scholar 

  • Kawasaki M (1993a) Comparative studies on the motor control mechanisms for electrocommunication in gymnotiform fishes. J Comp Physiol A (submitted)

  • Kawasaki M (1993b) Temporal hyperacuity in the gymnotiform electric fish, Eigenmannia. Am Zool 33:86–93

    Google Scholar 

  • Kawasaki M, Heiligenberg W (1988) Individual prepacemaker neurons can modulate the pacemaker cycle of the gymnotiform electric fish, Eigenmannia. J Comp Physiol A 162:13–21

    Google Scholar 

  • Kawasaki M, Rose GJ, Heiligenberg W (1988a) Temporal hyperacuity in single neurons of electric fish. Nature 336:173–176

    Google Scholar 

  • Kawasaki M, Maler L, Rose GJ, Heiligenberg W (1988b) Anatomical and functional organization of the prepacemaker nucleus in gymnotiform electric fish: The accommodation of two behaviors in one nucleus. J Comp Neurol 276:113–131

    Google Scholar 

  • Keller CH (1988) Stimulus discrimination in the diencephalon of Eigenmannia: the emergence and sharpening of a sensory filter. J Comp Physiol A 162:747–757

    Google Scholar 

  • Konishi M, Takahashi TT, Wagner H, Sullivan WE, Carr CE (1988) Neurophysiological and anatomical substrates of sound localization in the owl. In: Edelman GM, Gall WE, Cowan WM (eds) Auditory function. Wiley, New York, pp 721–745

    Google Scholar 

  • Larimer JL, MacDonald JA (1968) Sensory feedback from electroreceptors to electromotor pacemaker centers in gymnotids. Am J Physiol 214:1253–1261

    Google Scholar 

  • Lauder GV, Liem KF (1983) Patterns of diversity and evolution in ray-finned fishes. In: Northcutt RG, Davis RE (eds) Fish neurobiology, vol.1. Univ. of Michigan Press, Ann Arbor, pp 1–24

    Google Scholar 

  • Lissmann HW (1958) On the function and evolution of electric organs in fish. J Exp Biol 35:156–191

    Google Scholar 

  • Lissmann HW, Machin KE (1958) The mechanism of object location in Gymnarchus niloticus and similar fish. J Exp Biol 35:451–486

    Google Scholar 

  • Metzner W (1993) The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways. J Neurosci 13:1862–1878

    Google Scholar 

  • Rose GJ, Heiligenberg W (1985a) Temporal hyperacuity in the electric sense of fish. Nature 318:178–180

    Google Scholar 

  • Rose GJ, Heiligenberg W (1985b) Structure and function of electrosensory neurons in the torus semicircularis of Eigenmannia: Morphological correlates of phase and amplitude sensitivity. J Neurosci 5:2269–2280

    Google Scholar 

  • Rose GJ, Heiligenberg W (1986a) Neural coding of difference frequencies in the midbrain of the electric fish Eigenmannia: Reading the sense of rotation in an amplitude-phase plane. J Comp Physiol A 158:613–624

    Google Scholar 

  • Rose GJ, Heiligenberg W (1986b) Limits of phase and amplitude sensitivity in the torus semicircularis of Eigenmannia. J Comp Physiol A 159:813–822

    Google Scholar 

  • Rose GJ, Keller CH, Heiligenberg W (1987) “Ancestral” neural mechanisms of electrolocation suggest a substrate for the evolution of the jamming avoidance response. J Comp Physiol A 160:491–500

    Google Scholar 

  • Rose GJ, Kawasaki M, Heiligenberg W (1988) ‘Recognition units’ at the top of a neuronal hierarchy? Prepacemaker neurons in Eigenmannia code the sign of frequency differences unambiguously. J Comp Physiol A 162:759–772

    Google Scholar 

  • Selverston AI, Moulins M (eds) (1987) The crustacean stomatogastric system: A model for the study of central nervous systems. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Szabo T (1959) Organisation particulière de la comande nerveuse centrale de la décharge chez un Poisson èlectrique, Gymnarchus niloticus. C R Acad Sci Paris 248:2488–2489

    Google Scholar 

  • Szabo T (1965) Sense organs of the lateral line system in some electric fish of the Gymnotidae, Mormyridae and Gymnarchidae. J Morphol 117:229–250

    Google Scholar 

  • Szabo T (1974) Anatomy of the specialized lateral line organs of electroreception. In: Fessard A (ed) Handbook of sensory physiology, vol. III/3: Electroreceptors and other specialized receptors in lower vertebrates. Springer, Berlin Heidelberg New York, pp 13–58

    Google Scholar 

  • Watanabe A, Takeda K (1963) The change of discharge frequency by A.C. stimulus in a weakly electric fish. J Exp Biol 40:57–66

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kawasaki, M. Independently evolved jamming avoidance responses employ identical computational algorithms: a behavioral study of the African electric fish, Gymnarchus niloticus . J Comp Physiol A 173, 9–22 (1993). https://doi.org/10.1007/BF00209614

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00209614

Key words

Navigation