Journal of Comparative Physiology A

, Volume 192, Issue 6, pp 561–572 | Cite as

Walter Heiligenberg: the jamming avoidance response and beyond

Review

Abstract

Walter Heiligenberg (1938–1994) was an exceptionally gifted behavioral physiologist who made enormous contributions to the analysis of behavior and to our understanding of how the brain initiates and controls species-typical behavioral patterns. He was distinguished by his rigorous analytical approach used in both behavioral studies and neuroethological investigations. Among his most significant contributions to neuroethology are a detailed analysis of the computational rules governing the jamming avoidance response in weakly electric fish and the elucidation of the principal neural pathway involved in neural control of this behavior. Based on his work, the jamming avoidance response is perhaps the best-understood vertebrate behavior pattern in terms of the underlying neural substrate. In addition to this pioneering work, Heiligenberg stimulated research in a significant number of other areas of ethology and neuroethology, including: the quantitative assessment of aggressivity in cichlid fish; the ethological analysis of the stimulus–response relationship in the chirping behavior of crickets; the exploration of the neural and endocrine basis of communicatory behavior in weakly electric fish; the study of cellular mechanisms of neuronal plasticity in the adult fish brain; and the phylogenetic analysis of electric fishes using a combination of morphology, electrophysiology, and mitochondrial sequence data.

Keywords

Cichlid fish Astatotilapia (Haplochromis) burtoni Law of heterogenous summation Electric fish Eigenmannia sp. Electrolocation Parallel processing 

Abbreviations

CP/PPn

Central posterior/prepacemaker nucleus

dF

Frequency of a neighboring fish’s electric organ discharge minus frequency of the fish’s own discharge

ELL

Electrosensory lateral line lobe

EOD

Electric organ discharge

nE

Nucleus electrosensorius

P

P-type electroreceptor

Pn

Pacemaker nucleus

SPPn

Sublemniscal prepacemaker nucleus

T

T-type electroreceptor

TSd

Torus semicircularis pars dorsalis

Notes

Acknowledgments

We thank Masashi Kawasaki, Mark Konishi, and Marianne M. Zupanc for helpful comments on the manuscript. This article was written while G. K. H. Z. was a visiting scholar at the Department of Neurosciences of UCSD in La Jolla.

References: Publications from the laboratory of Walter Heiligenberg (in chronological order)

1962

  1. Heiligenberg W (1962) Die Erschließung des Wirkungsgefüges der Motivation von Instinktverhalten. Naturwissenschaften 49:68–69Google Scholar

1963

  1. Heiligenberg W (1963) Ursachen für das Auftreten von Instinktbewegungen bei einem Fische (Pelmatochromis subocellatus kribensis Boul., Cichlidae). Z Vergl Physiol 47:339–380Google Scholar

1964

  1. Heiligenberg W (1964) Ein Versuch zur ganzheitsbezogenen Analyse des Instinktverhaltens eines Fisches (Pelmatochromis subocellatus kribensis Boul., Cichlidae). Z Tierpsychol 21:1–52Google Scholar

1965

  1. Heiligenberg W (1965) Colour polymorphism in the males of an African cichlid fish. J Zool 146:95–97CrossRefGoogle Scholar
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1966

  1. Heiligenberg W (1966) The stimulation of territorial singing in house crickets (Acheta domesticus). Z Vergl Physiol 53:114–129Google Scholar

1968

  1. Heiligenberg W (1968) Zum Wechselgesang der Heimchen (Acheta domesticus). In: Kybernetik 68, Beihefte zu Elektronische Rechenanlagen, Vol. 18. R. Oldenburg, München/Wien, pp 60–64Google Scholar

1969

  1. Heiligenberg W (1969) The effect of stimulus chirps on a cricket’s chirping (Acheta domesticus). Z Vergl Physiol 65:70–97Google Scholar
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1972

  1. Heiligenberg W, Kramer U (1972) Aggressiveness as a function of external stimulation. J Comp Physiol 77:332–340Google Scholar
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1973

  1. Heiligenberg W (1973) Random processes describing the occurrence of behavioural patterns in a cichlid fish. Anim Behav 21:169–182Google Scholar
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1974

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1975

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1976

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1977

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1978

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1979

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1980

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1981

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1982

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1983

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1984

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1985

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1986

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1987

  1. Dye J (1987) Dynamics and stimulus-dependence of pacemaker control during behavioral modulations in the weakly electric fish, Apteronotus. J Comp Physiol A 161:175–185PubMedGoogle Scholar
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1988

  1. Baldi P, Heiligenberg W (1988) How sensory maps could enhance resolution through ordered arrangements of broadly tuned receivers. Biol Cybern 59:313–318PubMedGoogle Scholar
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1989

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  2. 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 U S A 86:8993–8997PubMedGoogle Scholar
  3. Heiligenberg W (1989) Coding and processing of electrosensory information in gymnotiform fish. J Exp Biol 146:255–275PubMedGoogle Scholar
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1990

  1. Devor M, Keller CH, Ellisman MH (1990) Spontaneous discharge of afferents in a neuroma reflects original receptor tuning. Brain Res 517:245–250PubMedGoogle Scholar
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1991

  1. Dye J (1991) Ionic and synaptic mechanisms underlying a brainstem oscillator: an in vitro study of the pacemaker nucleus of Apteronotus. J Comp Physiol A 168:521–532PubMedGoogle Scholar
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1992

  1. Hagedorn M, Vischer HA, Heiligenberg W (1992) Development of the jamming avoidance response and its morphological correlates in the gymnotiform electric fish, Eigenmannia. J Neurobiol 23:1446–1466PubMedGoogle Scholar
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1993

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1994

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1995

  1. Alves-Gomes JA, Ortí 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. Mol Biol Evol 12:298–318PubMedGoogle Scholar
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1996

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  3. Heiligenberg W, Metzner W, Wong CJH, Keller CH (1996) Motor control of the jamming avoidance response of Apteronotus leptorhynchus: evolutionary changes of a behavior and its neuronal substrates. J Comp Physiol A 179:653–674PubMedGoogle Scholar
  4. Metzner W, Viete S (1996) The neuronal basis of communication and orientation in the weakly electric fish, Eigenmannia. I. Communication behavior or: seeking a conspecific’s response. Naturwissenschaften 83:6–14Google Scholar
  5. Metzner W, Viete S (1996) The neuronal basis of communication and orientation in the weakly electric fish, Eigenmannia. II. Electrolocation and avoidance of jamming by neighboring conspecifics. Naturwissenschaften 83:71–77Google Scholar
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1997

  1. Spiro JE (1997) Differential activation of glutamate receptor subtypes on a single class of cells enables a neural oscillator to produce distinct behaviors. J Neurophysiol 78:835–847PubMedGoogle Scholar
  2. Wong CJH (1997) Afferent and efferent connections of the diencephalic prepacemaker nucleus in the weakly electric fish, Eigenmannia virescens: interactions between the electromotor system and the neuroendocrine axis. J Comp Neurol 383:18–41PubMedGoogle Scholar
  3. Wong CJH (1997) Connections of the basal forebrain of the weakly electric fish, Eigenmannia virescens. J Comp Neurol 389:49–64PubMedGoogle Scholar

2000

  1. Wong CJH (2000) Electrical stimulation of the preoptic area in Eigenmannia: evoked interruptions in the electric organ discharge. J Comp Physiol A 186:81–93PubMedGoogle Scholar

Other publications cited in the text

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  5. Seitz A (1940) Die Paarbildung bei einigen Cichliden: I. Die Paarbildung bei Astatotilapia strigigena Pfeffer. Z Tierpsychol 4:40–84Google Scholar
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  7. Zupanc GKH (2002) From oscillators to modulators: behavioral and neural control of modulations of the electric organ discharge in the gymnotiform fish, Apteronotus leptorhynchus. J Physiol (Paris) 96:459–472Google Scholar
  8. Zupanc GKH (2004) Behavioral neurobiology: an integrative approach. Oxford University Press, OxfordGoogle Scholar
  9. Zupanc GKH (2006) Neurogenesis and neuronal regeneration in the adult fish brain. J Comp Physiol A (in press). DOI 10.1007/s00359-006-0104-yGoogle Scholar
  10. Zupanc GKH, TH Bullock (2005) From electrogenesis to electroreception: an overview. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, Berlin Heidelberg New York, pp 5–46Google Scholar
  11. Zupanc GKH, L Maler (1997) Neuronal control of behavioral plasticity: the prepacemaker nucleus of weakly electric gymnotiform fish. J Comp Physiol A 180:99–111Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.School of Engineering and ScienceInternational University BremenBremenGermany
  2. 2.Department of NeurosciencesUniversity of California at San DiegoLa JollaUSA

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