Journal of Comparative Physiology A

, Volume 179, Issue 5, pp 653–674 | Cite as

Motor control of the jamming avoidance response of Apteronotus leptorhynchus: evolutionary changes of a behavior and its neuronal substrates

  • W. Heiligenberg
  • C. J. H. Wong
  • W. Metzner
  • C. H. Keller
Original Paper
Accepted:

Abstract

The two closely related gymnotiform fishes, Apteronotus and Eigenmannia, share many similar communication and electrolocation behaviors that require modulation of the frequency of their electric organ discharges. The premotor linkages between their electrosensory system and their medullary pacemaker nucleus, which controls the repetition rate of their electric organ discharges, appear to function differently, however. In the context of the jamming avoidance response, Eigenmannia can raise or lower its electric organ discharge frequency from its resting level. A normally quiescent input from the diencephalic prepacemaker nucleus can be recruited to raise the electric organ discharge frequency above the resting level. Another normally active input, from the sublemniscal prepacemaker nucleus, can be inhibited to lower the electric organ discharge frequency below the resting level (Metzner 1993). In contrast, during a jamming avoidance response, Apteronotus cannot lower its electric organ discharge frequency below the resting level. The sublemniscal prepacemaker is normally completely inhibited and release of this inhibition allows the electric organ discharge frequency to rise during the jamming avoidance response. Further inhibition of this nucleus cannot lower the electric organ discharge frequency below the resting level. Lesions of the diencephalic prepacemaker do not affect performance of the jamming avoidance response. Thus, in Apteronotus, the sublemniscal prepacemaker alone controls the change of the electric organ discharge frequency during the jamming avoidance response.

Key words

Electric fish Pacemaker nucleus Central pattern generator Glutamate receptors Social communication 

Abbreviations

aCSF

artificial cerebrospinal fluid

APV

d(-)2-amino-5-phosphonovaleric acid (NMDA receptor blocker)

CNQX

6-cyano-7-nitroquinoxaline-2,3-dione (non-NMDA receptor blocker)

CPP

3-(2-carboxypiperazine-4-yl)-propyl-1 -phosphonic acid (NMDA receptor blocker)

Df

frequency difference between jamming signal and EOD

EOD

electric organ discharge

feod

frequency of fish's own EOD

fjam

frequency of jamming stimulus

GABA

γ-amino-n -butyric acid

JAR

jamming avoidance response

NMDA

N-methyl-d-aspartate

NSR

non-selective response

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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alves-Gomes JA, Orti G, Haygood M, Heiligenberg W, Meyer A (1995) Phylogenetic analysis of the South American electric fishes (order Gymnotiformes) and the evolution of their electrogenic system: a synthesis based on morphology, electrophysiology, and mitochondrial sequence data. J Mol Biol Evol 12: 298–318Google Scholar
  2. Arbas EA, Meinertzhagen IA, Shaw SR (1991) Evolution in nervous systems. Annu Rev Neurosci 14: 9–38Google Scholar
  3. Baker CL (1981) Sensory control of pacemaker acceleration and deceleration in gymnotiform electric fish with pulse-type discharges. J Comp Physiol A 141: 197–206Google Scholar
  4. Bass AH (1986) Electric organs revisited. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 13–70Google Scholar
  5. Bennett MVL (1968) Neural control of electric organs. In: Ingle D (ed) The central nervous system and fish behavior. Chicago Press, Chicago, pp 147–169Google Scholar
  6. Bottai D, Maler L, Dunn RJ (1995) Molecular characterization of NMDA receptors in the electric fish Apteronotus leptorhynchus. Soc Neurosci Abstr 21: 197Google Scholar
  7. Brodin L, Grillner S (1985) The role of putative excitatory amino acid neurotransmission in the initiation of locomotion in the lamprey spinal cord. I & II. The effects of excitatory amino acid antagonists. Brain Res 360: 139–158Google Scholar
  8. Bullock TH (1970) The reliability of neurons. J Gen Physiol 55: 565–584Google Scholar
  9. Bullock TH, Hamstra RH, Scheich H (1972) The jamming avoidance response of high-frequency electric fish, I & II. J Comp Physiol A 77: 1–48Google Scholar
  10. Bullock TH, Behrend K, Heiligenberg W (1975) 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 A 103: 97–121Google Scholar
  11. Bullock TH, Bodznick DA, Northcutt RG (1983) The phylogenetic distribution of electroreception: evidence for convergent evolution of a primitive vertebrate sense modality. Brain Res Rev 6: 25–46Google Scholar
  12. Carr CE, Maler L (1986) Electroreception in gymnotiform fish: central anatomy and physiology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 319–374Google Scholar
  13. Carr CE, Maler L, Heiligenberg W, Sas E (1981) Laminar organization of the afferent and efferent systems of the torus semicircularis of gymnotiform fish: morphological substrates for parallel processing in the electrosensory system. J Comp Neurol 203: 649–670Google Scholar
  14. Daw NG, Stein PSG, Fox G (1993) The role of NMDA receptors in information processing. Annu Rev Neurosci 16: 207–222Google Scholar
  15. Dye J (1987) Dynamics and behavioral contexts distinguishing modes of pacemaker modulations in the weakly electric fish Apteronotus. J Comp Physiol A 161: 175–185Google Scholar
  16. Dye J (1988) An in vitro physiological preparation of a vertebrate communicatory behavior: chirping in the weakly electric fish Apteronotus. J Comp Physiol A 163: 445–458Google Scholar
  17. Dye JC, Meyer JH (1986) Central control of the electric organ discharge in weakly electric fish. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 71–102Google Scholar
  18. Dye J, Heiligenberg W (1987) Intracellular recording during behavioral modulations in the medullary pacemaker nucleus of the weakly electric fish Apteronotus. J Comp Physiol A 161: 187–200Google Scholar
  19. Dye J, Heiligenberg W, Keller CH, Kawasaki M (1989) Different classes of glutamate receptors mediate distinct behaviors in a single brainstem nucleus. Proc Natl Acad Sci USA 86: 8993–8997Google Scholar
  20. Elekes K, Szabo T (1981) Comparative synaptology of the pacemaker nucleus in the brain of weakly electric fish (Gymnotidae). In: Szabo T, Czeh G (eds) Sensory physiology of aquatic lower vertebrates. Akademiai Kiado, Budapest, pp 107–127Google Scholar
  21. Feldman JL, Smith JC (1989) Cellular mechanisms underlying modulation of breathing pattern in mammals. Annu NY Acad Sci 563: 114–130Google Scholar
  22. Fetcho J (1992) The spinal motor system in early vertebrates and some of its evolutionary changes. Brain Behav Evol 40: 82–97Google Scholar
  23. Fetcho J, Faber DS (1988) Identification of motoneurons and interneurons in the spinal network for escapes initiated by Mauthner cell in goldfish. J Neurosci 8: 4192–4213Google Scholar
  24. Getting PA, Dekins MS (1985) Mechanisms of pattern generation underlying swimming in Tritonia IV. gating of a central pattern generator. J Neurophysiol 53: 466–480Google Scholar
  25. Grillner S, Matsushima T (1991) The neural network underlying locomotion in lamprey-synaptic and cellular mechanisms. Neuron 7: 1–15Google Scholar
  26. Hagedorn M, Heiligenberg W (1985) Court and spark: electric signals in the courtship and mating of gymnotoid electric fish. Anim Behav 33: 254–265Google Scholar
  27. Hagedorn M, Heiligenberg W, Carr C (1988) The development of the jamming avoidance response in the weakly electric fish, Eigenmannia. Brain Behav Evol 31: 161–169Google Scholar
  28. Harris-Warrick RM, Marder E (1991) Modulation of neural networks for behavior. Annu Rev Neurosci 14: 39–58CrossRefPubMedGoogle Scholar
  29. Heiligenberg W (1991) Neural nets in electric fish. MIT Press, Cambridge, MAGoogle Scholar
  30. Heiligenberg W, Baker C, Bastian J (1978a) The jamming avoidance response in gymnotoid pulse species: a mechanism to minimize the probability of pulsetrain coincidences. J Comp Physiol A 124: 211–224Google Scholar
  31. Heiligenberg W, Baker C, Matsubara J (1978b) The jamming avoidance response in Eigenmannia revisited: the structure of a neuronal democracy. J Comp Physiol A 127: 267–286Google Scholar
  32. Heiligenberg W, Hagedorn M, Meyer JH (1986) Social communication in gymnotoid electric fish. Natl Geog Soc Res RepGoogle Scholar
  33. Heiligenberg W, Finger T, Matsubara J, Carr CE (1981) Input to the medullary pacemaker nucleus in the weakly electric fish, Eigenmannia (Sternopygidae, Gymnotiformes). Brain Res 211: 418–423Google Scholar
  34. Heiligenberg W, Keller CH, Metzner W, Kawasaki M (1991) Structure and function of neurons in the complex of the nucleus electrosensorius of the gymnotiform fish Eigenmannia: detection and processing of electric signals in social communication. J Comp Physiol A 169: 151–164Google Scholar
  35. Hikosaka O, Wurtz RH (1985) Modifications of saccadic eye movements by GABA-related substances I. & II. J Neurophysiol 53: 266–308Google Scholar
  36. Hopkins CD (1974) Electric communication in fish. Am Sci 62: 426–437Google Scholar
  37. Horikawa K, Armstrong WE (1988) A versatile means of inlracellular labeling: injection of biocytin and its detection with avidin conjugates. J Neurosci Methods 25: 1–12Google Scholar
  38. Huang Q, Zhou D, DiFiglia M (1992) Neurobiotin, a useful neuroanatomical tracer for in vivo anterograde, retrograde and transneuronal tract-tracing and for in vitro labeling of neurons. J Neurosci Methods 41: 31–43Google Scholar
  39. Kawasaki M (1993) Independently evolved jamming avoidance responses employ identical computational algorithms: a behavioral study of the African electric fish, Gymnarchus niloticus. J Comp Physiol A 173: 9–22Google Scholar
  40. Kawasaki M, Heiligenberg W (1989) Distinct mechanisms of modulation in a neuronal oscillator generate different social signals in the electric fish Hypopomus. J Comp Physiol A 165: 731–741Google Scholar
  41. Kawasaki M, Heiligenberg W (1990) Different classes of glutamate receptors and GABA mediate distinct modulations of a neuronal oscillator, the medullary pacemaker of a gymnotiform electric fish. J Neurosci 10: 3896–3904Google Scholar
  42. Kawasaki M, Maler L, Rose GJ, Heiligenberg W (1988) Anatomical and functional organization of the prepacemaker nucleus in gymnotiform electric fish: the accommodation of two behaviors in one nucleus. J Comp Neurol 276: 113–131Google Scholar
  43. Kawasaki M, Prather J, Guo Y-X (1996) Sensory cues for the gradual frequency fall responses of the gymnotiform electric fish, Rhamphichthys rostratus. J Comp Physiol A 178: 453–462Google Scholar
  44. Keller CH (1989) A sensory-motor interface in weakly electric gymnotiform fishes. PhD Thesis, University of California at San DiegoGoogle Scholar
  45. Keller C, Heiligenberg W (1989) From distributed sensory processing to discrete motor representations in the diencephalon of the electric fish, Eigenmannia. J Comp Physiol A 164: 565–576PubMedGoogle Scholar
  46. Keller CH, Maler L, Heiligenberg W (1990) Structural and functional organization of a diencephalic sensory-motor interface in the gymnotiform fish, Eigenmannia. J Comp Neurol 293: 347–376Google Scholar
  47. Keller CH, Kawasaki M, Heiligenberg W (1991) The control of pacemaker modulations for social communication in the weakly electric fish Sternopygus. J Comp Physiol A 169: 441–450Google Scholar
  48. Kennedy G, Heiligenberg W (1994) Ultrastructural evidence of GABA-ergic inhibition and glutamatergic excitation in the pacemaker nucleus of the gymnotiform electric fish, Hypopomus. J Comp Physiol A 174: 267–280Google Scholar
  49. Lapper SR, Bolam JP (1991) The anterograde and retrograde transport of neurobiotin in the central nervous system of the rat: comparison with biocytin. J Neurosci Methods 39: 163–174Google Scholar
  50. Maler L, Sas E, Johnston S, Ellis W (1991) An atlas of the brain of the electric fish, Apteronotus leptorhynchus. J Chem Neuroanat 4: 1–38Google Scholar
  51. Matsubara JA, Heiligenberg W (1978) How well do electric fish electrolocate under jamming? J Comp Physiol A 125: 285–290Google Scholar
  52. Metzner W (1993) The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways. J Neurosci 13: 1862–1878Google Scholar
  53. Metzner W, Viete S (1996) The neuronal basis of communication and orientation in the weakly electric fish, Eigenmannia. I & II. Naturwissenschaften 83: 6–14 and 71–77Google Scholar
  54. Meyrand P, Moulins M (1988a) Phylogenetic plasticity of crustacean stomatogastric circuits I. & II. J Exp Biol 138: 107–153Google Scholar
  55. Moortgat KT, Keller CH (1995) Network properties of a highly regular neuronal oscillator in a weakly electric fish. Soc Neurosci Abstr 21: 188Google Scholar
  56. Mori S (1987) Integration of posture and locomotion in acute decerebrate cats and in awake, freely moving cats. Prog Neurobiol 28: 161–195Google Scholar
  57. Nishikawa KC, Anderson CW, Deban SM, O'Reilly JC (1992) The evolution of neural circuits controlling feeding behavior in frogs. Brain Behav Evol 40: 125–140Google Scholar
  58. Nishikawa KC, Gans C (1992) The role of hypoglossal sensory feedback during feeding in the marine toad, Bufo marinus. J Exp Zool 264: 245–252Google Scholar
  59. Paul DH (1981a) Homologies between body movements and muscular contractions in locomotion of two decapods of different families. J Exp Biol 94: 159–168Google Scholar
  60. Paul DH (1981b) Homologies between neuromuscular systems serving different functions in two decapods of different familes. J Exp Biol 94: 169–187Google Scholar
  61. Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Annu Rev Neurosci 16: 265–297Google Scholar
  62. 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: 759–772Google Scholar
  63. Spiro JE (1994) Modulation of the electric fish pacemaker rhythm at the level of the relay cell. Soc Neurosci Abstr 20: 370Google Scholar
  64. Spiro JE, Brose N, Heinemann SF, Heiligenberg W (1994) Immunolocalization of NMDA receptors in the central nervous system of weakly electric fish: functional implications for the modulation of a neuronal oscillator. J Neurosci 14: 6289–6299Google Scholar
  65. Stavenga DG, Hardie RC (eds) (1989) Facets of vision. Springer, Berlin HeidelbergGoogle Scholar
  66. Stein PS (1989) Spinal cord circuits for motor pattern selection in the turtle. Ann NY Acad Sci 563: 1–10Google Scholar
  67. Striedter GF (1992) Phylogenetic changes in the connections of the lateral preglomerular nucleus in ostariophysan teleosts: a pluralistic view of brain evolution. Brain Behav Evol 39: 329–357Google Scholar
  68. Szabo T, Enger PS (1964) Pacemaker activity of the medullary nucleus controlling electric organs in high-frequency gymnotid fish. Z V Physiol 49: 285–300Google Scholar
  69. Turner RW, Moroz LL (1995) Localization of nicotinamide adenine dinucleotide phosphate-diaphorase activity in electrosensory and electromotor systems of a gymnotiform teleost, Apteronotus leptorhynchus. J Comp Neurol 356: 261–274Google Scholar
  70. Vaney DI (1991) Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neurosci Lett 125: 187–190Google Scholar
  71. Viete S, Heiligenberg W (1991) The development of the jamming avoidance response (JAR) in Eigenmannia: an innate behavior indeed. J Comp Physiol A 169: 15–23Google Scholar
  72. Wong CJH (1995) Afferent and efferent connections of the diencephalic prepacemaker nucleus in the weakly electric fish, Eigenmannia virescens. Soc Neurosci Abstr 21: 187Google Scholar
  73. Wong CJH, Heiligenberg W (1993) Diencephalic inhibitory projections to the pacemaker nucleus of the weakly electric fish, Hypopomus. Soc Neurosci Abstr 19: 377Google Scholar
  74. Zupanc GKH, Heiligenberg W (1992) The structure of the diencephalic prepacemaker nucleus revisited: light microscopic and ultrastructural studies. J Comp Neurol 323: 558–569Google Scholar
  75. Zupanc GKH, Maler L (1993) Evoked chirping in the weakly electric fish Apteronotus leptorhynchus: a quantitative biophysical analysis. Can J Zool 71: 2301–2310Google Scholar
  76. Zupanc GKH, Zupanc MM (1992) Birth and migration of neurons in the central posterior/prepacemaker nucleus during adulthood in weakly electric knifefish (Eigenmannia sp.) Proc Natl Acad Sci USA 89: 9539–9543Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • W. Heiligenberg
    • 1
  • C. J. H. Wong
    • 1
  • W. Metzner
    • 2
  • C. H. Keller
    • 3
  1. 1.Neurobiology UnitScripps Institution of Oceanography, University of California at San DiegoLa JollaUSA
  2. 2.Department of BiologyUniversity of California at RiversideRiversideUSA
  3. 3.Institute of Neuroscience University of OregonEugeneUSA

Personalised recommendations