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.
Similar content being viewed by others
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
References: Publications from the laboratory of Walter Heiligenberg (in chronological order)
1962
Heiligenberg W (1962) Die Erschließung des Wirkungsgefüges der Motivation von Instinktverhalten. Naturwissenschaften 49:68–69
1963
Heiligenberg W (1963) Ursachen für das Auftreten von Instinktbewegungen bei einem Fische (Pelmatochromis subocellatus kribensis Boul., Cichlidae). Z Vergl Physiol 47:339–380
1964
Heiligenberg W (1964) Ein Versuch zur ganzheitsbezogenen Analyse des Instinktverhaltens eines Fisches (Pelmatochromis subocellatus kribensis Boul., Cichlidae). Z Tierpsychol 21:1–52
1965
Heiligenberg W (1965) Colour polymorphism in the males of an African cichlid fish. J Zool 146:95–97
Heiligenberg W (1965) A quantitative analysis of digging movements and their relationship to aggressive behaviour in cichlids. Anim Behav 13:163–170
Heiligenberg W (1965) The effect of external stimuli on the attack readiness of a cichlid fish. Z Vergl Physiol 49:459–464
Heiligenberg W (1965) The suppression of behavioral activities by frightening stimuli. Z Vergl Physiol 50:660–672
Heiligenberg W (1965) Eine Systemanalyse tierischen Instinktverhaltens. In: Frank HG (ed) Kybernetik: Brücke zwischen den Wissenschaften. Umschau-Verlag, Frankfurt, pp 105–113
1966
Heiligenberg W (1966) The stimulation of territorial singing in house crickets (Acheta domesticus). Z Vergl Physiol 53:114–129
1968
Heiligenberg W (1968) Zum Wechselgesang der Heimchen (Acheta domesticus). In: Kybernetik 68, Beihefte zu Elektronische Rechenanlagen, Vol. 18. R. Oldenburg, München/Wien, pp 60–64
1969
Heiligenberg W (1969) The effect of stimulus chirps on a cricket’s chirping (Acheta domesticus). Z Vergl Physiol 65:70–97
Leong C-Y (1969) The quantitative effect of releasers on the attack readiness of the fish Haplochromis burtoni (Cichlidae, Pisces). Z Vergl Physiol 65:29–50
Wendler G, Heiligenberg W (1969) Relative Koordination bei gekoppelten, rhythmisch tätigen Modellneuronen. Zool. Anz., Suppl. 33:477–482
1972
Heiligenberg W, Kramer U (1972) Aggressiveness as a function of external stimulation. J Comp Physiol 77:332–340
Heiligenberg W, Kramer U, Schulz V (1972) The angular orientation of the black eye-bar in Haplochromis burtoni (Cichlidae, Pisces) and its relevance to aggressivity. Z Vergl Physiol 76:168–176
1973
Heiligenberg W (1973) Random processes describing the occurrence of behavioural patterns in a cichlid fish. Anim Behav 21:169–182
Heiligenberg W (1973) “Electromotor” response in the electric fish Eigenmannia (Rhamphichthyidae, Gymnotoidei). Nature 243:301–302
Heiligenberg W (1973) Electrolocation of objects in the electric fish Eigenmannia (Rhamphichthyidae, Gymnotoidei). J Comp Physiol 87:137–164
1974
Heiligenberg W (1974) Electrolocation and jamming avoidance in a Hypopygus (Rhamphichthyidae, Gymnotoidei), an electric fish with pulse-type discharges. J Comp Physiol 91:223–240
Heiligenberg W (1974) Processes governing behavioral states of readiness. Adv Study Behav 5:173–200
Heiligenberg W (1974) Der Einfluß spezifischer Reizmuster auf das Verhalten der Tiere. In: Immelmann K (ed) Grzimeks Tierleben. Ergänzungsband Verhaltensforschung. Kindler Verlag, München, pp 234–254
Heiligenberg W (1974) A stochastic analysis of fish behavior. In: McFarland DJ (ed) Motivational control system analysis. Academic, New York, pp 87–118
1975
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
Heiligenberg W (1975) Processes controlling aggressiveness in cichlid fish. In: Ingle DJ, Shein HM (eds) Model systems in biological psychiatry. MIT, Cambridge, pp 132–148
Heiligenberg W (1975) Electrolocation and jamming avoidance in the electric fish Gymnarchus niloticus (Gymnarchidae, Mormyriformes). J Comp Physiol 103:55–67
Heiligenberg W (1975) Theoretical and experimental approaches to spatial aspects of electrolocation. J Comp Physiol 103:247–272
1976
Heiligenberg W (1976) Electrolocation and jamming avoidance in the mormyrid fish Brienomyrus. J Comp Physiol A 109:357–372
Heiligenberg W (1976) A probabilistic approach to the motivation of behavior. In: Fentress JC (ed) Simpler networks and behavior. Sinauer, Sunderland, pp 301–329
Heiligenberg W (1976) The interaction of stimulus patterns controlling aggressiveness in the cichlid fish Haplochromis burtoni. Anim Behav 24:452–458
Meyer DL, Heiligenberg W, Bullock TH (1976) The ventral substrate response: new postural control mechanism in fishes. J Comp Physiol A 109:59–68
1977
Heiligenberg W (1977) Principles of electrolocation and jamming avoidance in electric fish: a neuroethological approach. Springer, Berlin Heidelberg New York
Heiligenberg W (1977) Releasing and motivating functions of stimulus patterns in animal behavior: the ends of a spectrum. Ann N Y Acad Sci 290:60–71
1978
Heiligenberg W, Altes RA (1978) Phase sensitivity in electroreception. Science 199:1001–1004
Heiligenberg W, Baker C, Bastian J (1978) The jamming avoidance response in gymnotoid pulse-species: a mechanism to minimize the probability of pulse-train coincidence. J Comp Physiol A 124:211–224
Heiligenberg W, Baker C, Matsubara J (1978) The jamming avoidance response in Eigenmannia revisited: the structure of a neuronal democracy. J Comp Physiol A 127:267–286
Hopkins CD, Heiligenberg WF (1978) Evolutionary design for electric signals and eletroreceptors in gymnotoid fishes of Surinam. Behav Ecol Sociobiol 3:113–134
Matsubara J, Heiligenberg W (1978) How well do electric fish electrolocate under jamming? J Comp Physiol A 125:285–290
1979
Bullock TH, Fernandes-Souza N, Graf W, Heiligenberg W, Langner G, Meyer DL, Pimentel-Sousa F, Scheich H, Viancour TA (1979) Aspects of the use of electric organ discharge and electroreception in Amazonian Gymnotoidei and other fishes. Acta Amazonica 9:549–572
1980
Baker CL (1980) Jamming avoidance behavior in gymnotoid electric fish with pulse-type discharges: sensory coding for a temporal pattern discrimination. J Comp Physiol A 136:165–181
Bastian J, Heiligenberg W (1980) The control of Eigenmannia’s pacemaker by distributed evaluation of electroreceptive afferences. J Comp Physiol A 136:113–133
Bastian J, Heiligenberg W (1980) Neural correlates of the jamming avoidance response in Eigenmannia. J Comp Physiol A 136:135–152
Bastian J, Heiligenberg W (1980) Phase-sensitive midbrain neurons in Eigenmannia: neural correlates of the jamming avoidance response. Science 209:828–831
Heiligenberg W (1980) The evaluation of eletroreceptive feedback in a gymnotoid fish with pulse-type electric organ discharges. J Comp Physiol A 138:173–185
Heiligenberg W (1980) The jamming avoidance response in the weakly electric fish Eigenmannia: a behavior controlled by distributed evaluation of electroreceptive afferences. Naturwissenschaften 67:499–507
Heiligenberg W, Bastian J (1980) Species specificity of electric organ discharges in sympatric gymnotoid fish of the Rio Negro. Acta Biol Venez 10:187–203
Partridge BL, Heiligenberg W (1980) Three’s a crowd? Predicting Eigenmannia’s response to multiple jamming. J Comp Physiol A 136:153–164
1981
Baker C (1981) Sensory control of pacemaker acceleration and deceleration in gymnotiform electric fish with pulse-type discharges. J Comp Physiol A 141:197–206
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
Heiligenberg W, Bastian J (1981) Especificidade das descargas do órgão elétrico em espécies de Gimnotóides simpátricos do Rio Negro. Acta Amazonica 11:429–437
Heiligenberg W, Finger T, Matsubara J, Carr C (1981) Input to the medullary pacemaker nucleus in the weakly electric fish, Eigenmannia (Sternopygidae, Gymnotiformes). Brain Res 211:418–423
Heiligenberg W, Partridge BL (1981) How electroreceptors encode JAR-eliciting stimulus regimes: reading trajectories in a phase-amplitude plane. J Comp Physiol A 142:295–308
Matsubara JA (1981) Neural correlates of a nonjammable electrolocation system. Science 211:722–725
Partridge BL, Heiligenberg W, Matsubara J (1981) The neural basis of a sensory filter in the jamming avoidance response: no grandmother cells in sight. J Comp Physiol A 145:153–168
1982
Carr CE, Maler L, Sas E (1982) Peripheral organization and central projections of the electrosensory nerves in gymnotiform fish. J Comp Neurol 211:139–153
Heiligenberg W, Dye J (1982) Labelling of electroreceptive afferents in a gymnotoid fish by intracellular injection of HRP: the mystery of multiple maps. J Comp Physiol A 148:287–296
Maler L, Sas E, Carr CE, Matsubara J (1982) Efferent projections of the posterior lateral line lobe in gymnotiform fish. J Comp Neurol 211:154–164
Meyer JH (1982) Behavioral responses of weakly electric fish to complex impedances. J Comp Physiol A 145:459–470
Meyer JH, Zakon HH (1982) Androgens alter the tuning of electroreceptors. Science 217:635–637
1983
Heiligenberg W (1983) The jamming avoidance response in an electric fish: algorithms in sensory information processing and their neuronal realization. In: Ewert JP, Capranica R, Ingle D (eds) Advances in vertebrate neuroethology. NATO ASI series A, Life sciences 56. Plenum, New York, pp 669–699
Heiligenberg W (1983) Zentralnervöse Informationsverarbeitung bei elektrischen Fischen. Verh Dtsch Zool Ges 1983:17–23
Meyer JH (1983) Steroid influences upon the discharge frequencies of a weakly electric fish. J Comp Physiol A 153:29–37
Meyer JH, Bell CC (1983) Sensory gating by a corollary discharge mechanism. J Comp Physiol A 151:401–406
1984
Heiligenberg W (1984) Electrosensory information processing in the electric fish Eigenmannia: the control of the jamming avoidance response. In: Aoki K, Ishii S, Morita H (eds) Animal behavior: neurophysiological and ethological approaches. Japan Science Society Press/Springer, Tokyo/Berlin Heidelberg New York, pp 161–173
Heiligenberg W (1984) Neural mechanisms of electrolocation and jamming avoidance behavior in electric fish. In: Bolis L, Keynes RD, Maddrell SHP (eds) Comparative physiology of sensory systems. Cambridge University Press, Cambridge, pp 475–495
Heiligenberg W, Bastian J (1984) The electric sense of weakly electric fish. Annu Rev Physiol 46:561–583
Meyer JH (1984) Steroid influences upon the discharge frequencies of intact and isolated pacemakers of weakly electric fish. J Comp Physiol A 154:659–668
Meyer JH, Zakon HH, Heiligenberg W (1984) Steroid influences upon the electrosensory system of weakly electric fish: direct effects upon discharge frequencies with indirect effects upon eletroreceptor tuning. J Comp Physiol A 154:625–631
1985
Carr CE, Maler L (1985) A Golgi study of the cell types of the dorsal torus semicircularis of the electric fish Eigenmannia: functional and morphological diversity in the midbrain. J Comp Neurol 235:207–240
Hagedorn M, Carr C (1985) Single electrocytes produce a sexually dimorphic signal in South American electric fish, Hypopomus occidentalis (Gymnotiformes, Hypopomidae). J Comp Physiol A 156:511–523
Hagedorn M, Heiligenberg W (1985) Court and spark: electric signals in the courtship and mating of gymnotoid electric fish. Anim Behav 33:254–265
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
Heiligenberg W, Rose G (1985) Neural correlates of jamming avoidance response (JAR) in the weakly electric fish Eigenmannia. Trends Neurosci 8:442–449
Rose G, Heiligenberg W (1985) Temporal hyperacuity in the electric sense of fish. Nature 318:178–180
Rose G, Heiligenberg W (1985) Structure and function of electrosensory neurons in the torus semicircularis of Eigenmannia: morphological correlates of phase and amplitude sensitivity. J Neurosci 5:2269–2280
1986
Bullock TH, Heiligenberg W (eds) (1986) Electroreception. Wiley, New York
Carr CE, Heiligenberg W, Rose GJ (1986) A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology. J Neurosci 6:107–119
Carr CE, Maler L (1986) Electroreception in gymnotiform fish: central anatomy and physiology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 319–373
Carr CE, Maler L, Taylor B (1986) A time-comparison circuit in the electric fish midbrain. II. Functional morphology. J Neurosci 6:1372–1383
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
Hagedorn M (1986) The ecology, courtship, and mating of gymnotiform electric fish. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 497–525
Heiligenberg W (1986) Jamming avoidance responses: model systems for neuroethology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 613–649
Heiligenberg W (1986) The control of behavioral performance in networks processing temporal and spatial patterns of sensory information. In: Guthrie D (eds) Aims and methods in neuroethology. Manchester University Press, Manchester, pp 207–230
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
Keller CH, Zakon HH, Sanchez DY (1986) Evidence for a direct effect of androgens upon electroreceptor tuning. J Comp Physiol A 158:301–310
Rose G (1986) A temporal processing mechanism for all species? Brain Behav Evol 28:134–144
Rose G, Heiligenberg W (1986) 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
Rose G, Heiligenberg W (1986) Limits of phase and amplitude sensitivity in the torus semicircularis of Eigenmannia. J Comp Physiol A 159:813–822
Zelick R (1986) Jamming avoidance in electric fish and frogs: strategies of signal oscillator timing. Brain Behav Evol 28:60–69
1987
Dye J (1987) Dynamics and stimulus-dependence of pacemaker control during behavioral modulations in the weakly electric fish, Apteronotus. J Comp Physiol A 161:175–185
Dye J, Heiligenberg W (1987) Intracellular recording in the medullary pacemaker nucleus of the weakly electric fish, Apteronotus, during modulatory behaviors. J Comp Physiol A 161:187–200
Heiligenberg W (1987) Central processing of sensory information in electric fish. J Comp Physiol A 161:621–631
Heiligenberg W, Rose GJ (1987) The optic tectum of the gymnotiform electric fish, Eigenmannia: labeling of physiologically identified cells. Neuroscience 22:331–340
Mathieson WB, Heiligenberg W, Maler L (1987) Ultrastructural studies of physiologically identified electrosensory afferent synapses in the gymnotiform fish, Eigenmannia. J Comp Neurol 255:526–537
Meyer JH, Leong M, Keller CH (1987) Hormone-induced and maturational changes in electric organ discharges and electroreceptor tuning in the weakly electric fish Apteronotus. J Comp Physiol A 160:385–394
Rose G, Keller C, 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
1988
Baldi P, Heiligenberg W (1988) How sensory maps could enhance resolution through ordered arrangements of broadly tuned receivers. Biol Cybern 59:313–318
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
Hagedorn M (1988) Ecology and behavior of a pulse-type electric fish, Hypopomus occidentalis (Gymnotiformes, Hypopomidae), in a fresh-water stream in Panama. Copeia 1988 (2):324–335
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
Heiligenberg W (1988) The neuronal basis of electrosensory perception and its control of a behavioral response in a weakly electric fish. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, Berlin Heidelberg New York, pp 851–868
Heiligenberg W (1988) Neural mechanisms of perception and motor control in a weakly electric fish. Adv Study Behav 18:73–98
Heiligenberg W (1988) Electrosensory maps form a substrate for the distributed and parallel control of behavioral responses in weakly electric fish. Brain Behav Evol 31:6–16
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
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
Kawasaki M, Rose G, Heiligenberg W (1988) Temporal hyperacuity in single neurons of electric fish. Nature 336:173–176
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
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
Shumway CA, Zelick RD (1988) Sex recognition and neuronal coding of electric organ discharge waveform in the pulse-type weakly electric fish, Hypopomus occidentalis. J Comp Physiol A 163:465–478
Zupanc GKH (1988) Fish and their behavior. 2nd edn. Tetra-Press, Melle
Zupanc GKH (ed) (1988) Praktische Verhaltensbiologie. Verlag Paul Parey, Berlin
1989
Devor M, Keller CH, Deerinck TJ, Levinson SR, Ellisman MH (1989) Na+ channel accumulation on axolemma of afferent endings in nerve-end neuromas in Apteronotus. Neurosci Lett 102:149–154
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 86:8993–8997
Heiligenberg W (1989) Coding and processing of electrosensory information in gymnotiform fish. J Exp Biol 146:255–275
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
Keller CH, 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
Shumway CA (1989) Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. I. Physiological differences. J Neurosci 9:4388–4399
Shumway CA (1989) Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. II. Anatomical differences. J Neurosci 9:4400–4415
Shumway CA, Maler L (1989) GABAergic inhibition shapes temporal and spatial response properties of pyramidal cells in the electrosensory lateral line lobe of gymnotiform fish. J Comp Physiol A 164:391–407
Szabo T, Heiligenberg W, Ravaille-Veron M (1989) HRP labeling and ultrastructural localization of prepacemaker terminals within the medullary pacemaker nucleus of the weakly electric gymnotiform fish Apteronotus leptorhynchus. J Comp Neurol 284:169–173
Vischer HA (1989) The development of lateral line receptors in Eigenmannia (Teleostei, Gymnotiformes). I. The mechanoreceptive lateral line system. Brain Behav Evol 33:205–222
Vischer HA (1989) The development of lateral-line receptors in Eigenmannia (Teleostei, Gymnotiformes). II. The electroreceptive lateral-line system. Brain Behav Evol 33:223–236
Vischer HA, Lannoo MJ, Heiligenberg W (1989) Development of the electrosensory nervous system in Eigenmannia (Gymnotiformes): I. The peripheral nervous system. J Comp Neurol 290:16–40
Zupanc GKH, Heiligenberg W (1989) Sexual maturity-dependent changes in neuronal morphology in the prepacemaker nucleus of adult weakly electric knifefish, Eigenmannia. J Neurosci 9:3816–3827
1990
Devor M, Keller CH, Ellisman MH (1990) Spontaneous discharge of afferents in a neuroma reflects original receptor tuning. Brain Res 517:245–250
Heiligenberg W (1990) Electrosensory systems in fish. Synapse 6:196–206
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
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
Lannoo MJ, Vischer HA, Maler L (1990) Development of the electrosensory nervous system of Eigenmannia (Gymnotiformes): II. The electrosensory lateral line lobe, midbrain, and cerebellum. J Comp Neurol 294:37–58
Vischer HA (1990) The morphology of the lateral line system in 3 species of Pacific cottoid fishes occupying disparate habitats. Experientia 46:244–250
Zupanc GKH (1990) Fische im Biologieunterricht. Aulis Verlag, Köln
1991
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 168:521–532
Heiligenberg W (1991a) The neural basis of behavior: a neuroethological view. Annu Rev Neurosci 14:247–267
Heiligenberg W (1991b) The jamming avoidance response of the electric fish, Eigenmannia: computational rules and their neuronal implementation. Sem Neurosci 3:3–18
Heiligenberg W (1991c) Recent advances in the study of electroreception. Curr Opin Neurobiol 1:187–191
Heiligenberg W (1991d) Sensory control of behavior in electric fish. Curr Opin Neurobiol 1:633–637
Heiligenberg W (1991e) Neural nets in electric fish. MIT, Cambridge
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
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
Metzner W, Heiligenberg W (1991) The coding of signals in the electric communication of the gymnotiform fish Eigenmannia: from electroreceptors to neurons in the torus semicircularis of the midbrain. J Comp Physiol A 169:135–150
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
Zupanc GKH (1991) Clustering of cell bodies, bundling of dendrites, and gap junctions: morphological substrate for electrical coupling in the prepacemaker nucleus. Neurosci Lett 129:29–34
Zupanc GKH (1991) The synaptic organization of the prepacemaker nucleus in weakly electric knifefish, Eigenmannia: a quantitative ultrastructural study. J Neurocytol 20:818–833
Zupanc GKH, Maler L, Heiligenberg W (1991) Somatostatin-like immunoreactivity in the region of the prepacemaker nucleus in weakly electric knifefish, Eigenmannia: a quantitative analysis. Brain Res 559:249–260
Zupanc GKH, Okawara Y, Zupanc MM, Fryer JN, Maler L (1991) In situ hybridization of putative somatostatin mRNA in the brain of electric gymnotiform fish. NeuroReport 2:707–710
1992
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 23:1446–1466
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
Zupanc GKH, Airey JA, Maler L, Sutko JL, Ellisman MH (1992) Immunohistochemical localization of ryanodine binding proteins in the central nervous system of gymnotiform fish. J Comp Neurol 325:135–151
Zupanc GKH, Heiligenberg W (1992) The structure of the diencephalic prepacemaker nucleus revisited: light microscopic and ultrastructural studies. J Comp Neurol 323:558–569
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 U S A 89:9539–9543
1993
Heiligenberg W (1993) Electrosensation. In: Evans DH (ed) The physiology of fishes. CRC, Boca Raton, pp 137–160
Heiligenberg W, Roska T (1993) On biological sensory information processing principles relevant to cellular neural networks. In: Roska T, Vandewalle J (eds) Cellular neural networks. Wiley, New York, pp 201–211
Metzner W (1993) The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways. J Neurosci 13:1862–1878
1994
Heiligenberg W (1994) The detection and generation of electric communication signals in gymnotiform fish. Fortschr Zool 39:13–24
Heiligenberg W (1994) The evolution of sensory motor interfaces in electric fish: another lesson in nature’s tinkering. In: Proceedings of the joint symposium on neural computation, University of California, San Diego and California Institute of Technology 4:122–128
Heiligenberg W (1994) The coding and processing of temporal information in the electrosensory system of fish. In: Buzsáki G, Llinás R, Singer W, Berthoz A, Christen Y (eds) Temporal coding in the brain. Springer, Berlin Heidelberg New York, pp 1–12
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
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
1995
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 12:298–318
Vischer HA (1995) Electroreceptor development in the electric fish Eigenmannia: a histological and ultrastructural study. J Comp Neurol 360:81–100
Wessel R (1995) In vitro study of phase resetting and phase locking in a time-comparison circuit in the electric fish, Eigenmannia. Biophys J 69:1880–1890
1996
Gabbiani F, Metzner W, Wessel R, Koch C (1996) From stimulus encoding to feature extraction in weakly electric fish. Nature 384:564–567
Heiligenberg W (1996) Elektrische Sinne und ihre Rolle bei der Orientierung und Kommunikation. In: Dudel J, Menzel R, Schmidt RF (eds) Neurowissenschaft: Vom Molekül zur Kognition. Springer, Berlin Heidelberg NewYork, pp 427–435
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 179:653–674
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 83:6–14
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 83:71–77
Wessel R, Koch C, Gabbiani F (1996) Coding of time-varying electric field amplitude modulations in a wave-type electric fish. J Neurophysiol 75:2280–2293
1997
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 78:835–847
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 383:18–41
Wong CJH (1997) Connections of the basal forebrain of the weakly electric fish, Eigenmannia virescens. J Comp Neurol 389:49–64
2000
Wong CJH (2000) Electrical stimulation of the preoptic area in Eigenmannia: evoked interruptions in the electric organ discharge. J Comp Physiol A 186:81–93
Other publications cited in the text
Bastian J, HH Zakon (2005) Plasticity of sense organs and brain. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, Berlin Heidelberg New York
Bullock TH, RH Hamstra H Scheich (1972) The jamming avoidance response of high-frequency electric fish. I. General features. II. Quantitative aspects. J Comp Physiol 77:1–48
Lorenz K (1963) Das sogenannte Böse: Zur Naturgeschichte der Aggression. Dr. G. Borotha-Schoeler, Vienna
Metzner W (1999) Neural circuitry for communication and jamming avoidance in gymnotiform electric fish. J Exp Biol 202:1365–1375
Seitz A (1940) Die Paarbildung bei einigen Cichliden: I. Die Paarbildung bei Astatotilapia strigigena Pfeffer. Z Tierpsychol 4:40–84
Watanabe A, K Takeda (1963) The change of discharge frequency by a.c. stimulus in a weak electric fish. J Exp Biol 40:57–66
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) 96:459–472
Zupanc GKH (2004) Behavioral neurobiology: an integrative approach. Oxford University Press, Oxford
Zupanc GKH (2006) Neurogenesis and neuronal regeneration in the adult fish brain. J Comp Physiol A (in press). DOI 10.1007/s00359-006-0104-y
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 5–46
Zupanc GKH, L Maler (1997) Neuronal control of behavioral plasticity: the prepacemaker nucleus of weakly electric gymnotiform fish. J Comp Physiol A 180:99–111
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
T. H. Bullock: deceased 2005
Rights and permissions
About this article
Cite this article
Zupanc, G.K.H., Bullock, T.H. Walter Heiligenberg: the jamming avoidance response and beyond. J Comp Physiol A 192, 561–572 (2006). https://doi.org/10.1007/s00359-006-0098-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-006-0098-5