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

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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.

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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

f eod :

frequency of fish's own EOD

f jam :

frequency of jamming stimulus

GABA :

γ-amino-n -butyric acid

JAR :

jamming avoidance response

NMDA :

N-methyl-d-aspartate

NSR :

non-selective response

References

  • 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: 298–318

    Google Scholar 

  • Arbas EA, Meinertzhagen IA, Shaw SR (1991) Evolution in nervous systems. Annu Rev Neurosci 14: 9–38

    Google Scholar 

  • Baker CL (1981) Sensory control of pacemaker acceleration and deceleration in gymnotiform electric fish with pulse-type discharges. J Comp Physiol A 141: 197–206

    Google Scholar 

  • Bass AH (1986) Electric organs revisited. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 13–70

    Google Scholar 

  • Bennett MVL (1968) Neural control of electric organs. In: Ingle D (ed) The central nervous system and fish behavior. Chicago Press, Chicago, pp 147–169

    Google Scholar 

  • Bottai D, Maler L, Dunn RJ (1995) Molecular characterization of NMDA receptors in the electric fish Apteronotus leptorhynchus. Soc Neurosci Abstr 21: 197

    Google Scholar 

  • 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: 139–158

    Google Scholar 

  • Bullock TH (1970) The reliability of neurons. J Gen Physiol 55: 565–584

    Google Scholar 

  • Bullock TH, Hamstra RH, Scheich H (1972) The jamming avoidance response of high-frequency electric fish, I & II. J Comp Physiol A 77: 1–48

    Google Scholar 

  • 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: 97–121

    Google Scholar 

  • 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: 25–46

    Google Scholar 

  • Carr CE, Maler L (1986) Electroreception in gymnotiform fish: central anatomy and physiology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 319–374

    Google Scholar 

  • 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: 649–670

    Google Scholar 

  • Daw NG, Stein PSG, Fox G (1993) The role of NMDA receptors in information processing. Annu Rev Neurosci 16: 207–222

    Google Scholar 

  • Dye J (1987) Dynamics and behavioral contexts distinguishing modes of pacemaker modulations in the weakly electric fish Apteronotus. J Comp Physiol A 161: 175–185

    Google Scholar 

  • 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: 445–458

    Google Scholar 

  • 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 71–102

    Google Scholar 

  • 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: 187–200

    Google Scholar 

  • 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: 8993–8997

    Google Scholar 

  • 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 107–127

    Google Scholar 

  • Feldman JL, Smith JC (1989) Cellular mechanisms underlying modulation of breathing pattern in mammals. Annu NY Acad Sci 563: 114–130

    Google Scholar 

  • Fetcho J (1992) The spinal motor system in early vertebrates and some of its evolutionary changes. Brain Behav Evol 40: 82–97

    Google Scholar 

  • 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: 4192–4213

    Google Scholar 

  • Getting PA, Dekins MS (1985) Mechanisms of pattern generation underlying swimming in Tritonia IV. gating of a central pattern generator. J Neurophysiol 53: 466–480

    Google Scholar 

  • Grillner S, Matsushima T (1991) The neural network underlying locomotion in lamprey-synaptic and cellular mechanisms. Neuron 7: 1–15

    Google Scholar 

  • Hagedorn M, Heiligenberg W (1985) Court and spark: electric signals in the courtship and mating of gymnotoid electric fish. Anim Behav 33: 254–265

    Google Scholar 

  • Hagedorn M, Heiligenberg W, Carr C (1988) The development of the jamming avoidance response in the weakly electric fish, Eigenmannia. Brain Behav Evol 31: 161–169

    Google Scholar 

  • Harris-Warrick RM, Marder E (1991) Modulation of neural networks for behavior. Annu Rev Neurosci 14: 39–58

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • 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: 211–224

    Google Scholar 

  • 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: 267–286

    Google Scholar 

  • Heiligenberg W, Hagedorn M, Meyer JH (1986) Social communication in gymnotoid electric fish. Natl Geog Soc Res Rep

  • 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: 418–423

    Google Scholar 

  • 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: 151–164

    Google Scholar 

  • Hikosaka O, Wurtz RH (1985) Modifications of saccadic eye movements by GABA-related substances I. & II. J Neurophysiol 53: 266–308

    Google Scholar 

  • Hopkins CD (1974) Electric communication in fish. Am Sci 62: 426–437

    Google Scholar 

  • Horikawa K, Armstrong WE (1988) A versatile means of inlracellular labeling: injection of biocytin and its detection with avidin conjugates. J Neurosci Methods 25: 1–12

    Google Scholar 

  • 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: 31–43

    Google Scholar 

  • 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: 9–22

    Google Scholar 

  • 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: 731–741

    Google Scholar 

  • 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: 3896–3904

    Google Scholar 

  • 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: 113–131

    Google Scholar 

  • 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: 453–462

    Google Scholar 

  • Keller CH (1989) A sensory-motor interface in weakly electric gymnotiform fishes. PhD Thesis, University of California at San Diego

    Google Scholar 

  • 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: 565–576

    CAS  PubMed  Google Scholar 

  • 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: 347–376

    Google Scholar 

  • 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: 441–450

    Google Scholar 

  • 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: 267–280

    Google Scholar 

  • 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: 163–174

    Google Scholar 

  • Maler L, Sas E, Johnston S, Ellis W (1991) An atlas of the brain of the electric fish, Apteronotus leptorhynchus. J Chem Neuroanat 4: 1–38

    Google Scholar 

  • Matsubara JA, Heiligenberg W (1978) How well do electric fish electrolocate under jamming? J Comp Physiol A 125: 285–290

    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 

  • 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 71–77

    Google Scholar 

  • Meyrand P, Moulins M (1988a) Phylogenetic plasticity of crustacean stomatogastric circuits I. & II. J Exp Biol 138: 107–153

    Google Scholar 

  • Moortgat KT, Keller CH (1995) Network properties of a highly regular neuronal oscillator in a weakly electric fish. Soc Neurosci Abstr 21: 188

    Google Scholar 

  • Mori S (1987) Integration of posture and locomotion in acute decerebrate cats and in awake, freely moving cats. Prog Neurobiol 28: 161–195

    Google Scholar 

  • Nishikawa KC, Anderson CW, Deban SM, O'Reilly JC (1992) The evolution of neural circuits controlling feeding behavior in frogs. Brain Behav Evol 40: 125–140

    Google Scholar 

  • Nishikawa KC, Gans C (1992) The role of hypoglossal sensory feedback during feeding in the marine toad, Bufo marinus. J Exp Zool 264: 245–252

    Google Scholar 

  • Paul DH (1981a) Homologies between body movements and muscular contractions in locomotion of two decapods of different families. J Exp Biol 94: 159–168

    Google Scholar 

  • Paul DH (1981b) Homologies between neuromuscular systems serving different functions in two decapods of different familes. J Exp Biol 94: 169–187

    Google Scholar 

  • Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Annu Rev Neurosci 16: 265–297

    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 

  • Spiro JE (1994) Modulation of the electric fish pacemaker rhythm at the level of the relay cell. Soc Neurosci Abstr 20: 370

    Google Scholar 

  • 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: 6289–6299

    Google Scholar 

  • Stavenga DG, Hardie RC (eds) (1989) Facets of vision. Springer, Berlin Heidelberg

    Google Scholar 

  • Stein PS (1989) Spinal cord circuits for motor pattern selection in the turtle. Ann NY Acad Sci 563: 1–10

    Google Scholar 

  • 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: 329–357

    Google Scholar 

  • Szabo T, Enger PS (1964) Pacemaker activity of the medullary nucleus controlling electric organs in high-frequency gymnotid fish. Z V Physiol 49: 285–300

    Google Scholar 

  • 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: 261–274

    Google Scholar 

  • Vaney DI (1991) Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neurosci Lett 125: 187–190

    Google Scholar 

  • Viete S, Heiligenberg W (1991) The development of the jamming avoidance response (JAR) in Eigenmannia: an innate behavior indeed. J Comp Physiol A 169: 15–23

    Google Scholar 

  • Wong CJH (1995) Afferent and efferent connections of the diencephalic prepacemaker nucleus in the weakly electric fish, Eigenmannia virescens. Soc Neurosci Abstr 21: 187

    Google Scholar 

  • Wong CJH, Heiligenberg W (1993) Diencephalic inhibitory projections to the pacemaker nucleus of the weakly electric fish, Hypopomus. Soc Neurosci Abstr 19: 377

    Google Scholar 

  • Zupanc GKH, Heiligenberg W (1992) The structure of the diencephalic prepacemaker nucleus revisited: light microscopic and ultrastructural studies. J Comp Neurol 323: 558–569

    Google Scholar 

  • Zupanc GKH, Maler L (1993) Evoked chirping in the weakly electric fish Apteronotus leptorhynchus: a quantitative biophysical analysis. Can J Zool 71: 2301–2310

    Google Scholar 

  • 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: 9539–9543

    Google Scholar 

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Authors and Affiliations

  1. Neurobiology Unit, Scripps Institution of Oceanography, University of California at San Diego, 92093-0202, La Jolla, CA, USA

    W. Heiligenberg & C. J. H. Wong

  2. Department of Biology, University of California at Riverside, 92521-0427, Riverside, CA, USA

    W. Metzner

  3. Institute of Neuroscience University of Oregon, 97403-1254, Eugene, OR, USA

    C. H. Keller

Authors
  1. W. Heiligenberg
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  2. C. J. H. Wong
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  3. W. Metzner
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  4. C. H. Keller
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This work is based on a manuscript that was partially completed at the time of Dr. Heiligenberg's untimely death on September 8, 1994

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Heiligenberg, W., Wong, C.J.H., Metzner, W. et al. Motor control of the jamming avoidance response of Apteronotus leptorhynchus: evolutionary changes of a behavior and its neuronal substrates. J Comp Physiol A 179, 653–674 (1996). https://doi.org/10.1007/BF00216130

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