Electric signaling behavior and the mechanisms of electric organ discharge production in mormyrid fish

Journal of Physiology Paris

Volumn 96, Issue 5-6, 2002, Pages 405-419

  Carlson, Bruce A ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Central pattern generator; Command; Communication; Electric fish; Pacemaker

Indexed keywords

AGGRESSION; CELL MEMBRANE; CELL SIZE; COURTSHIP; ELECTRIC FISH; ELECTRIC ORGAN; EXPLORATORY BEHAVIOR; FEEDBACK SYSTEM; INNERVATION; MOTOR CONTROL; NONHUMAN; PATTERN GENERATOR; REPRODUCTION; REVIEW; SEX DIFFERENCE; SPECIES DIFFERENCE;

EID: 0011872032     PISSN: 09284257     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0928-4257(03)00019-6     Document Type: Article

References (83)

1. J. Alves-Gomes, C.D. Hopkins, Molecular insights into the phylogeny of mormyriform fishes and the evolution of their electric organs, Brain Behav. Evol 49 (1997) 324-350.
2. A.H. Bass, Species differences in electric organs of mormyrids: Substrates for species-typical electric organ discharge waveforms, J. Comp. Neurol. 244 (1986) 313-330.
3. A.H. Bass, A hormone-sensitive communication system in an electric fish, J. Neurobiol. 17 (1986) 131-156.
4. A.H. Bass, C.D. Hopkins, Hormonal control of sexual differentiation: changes in electric organ discharge waveform, Science 220 (1983) 971-974.
5. A.H. Bass, C.D. Hopkins, Hormonal control of sex differences in the electric organ discharge of mormyrid fishes, J. Comp. Physiol. A 156 (1985) 587-604.
6. A.H. Bass, S.F. Volman, From behavior to membranes: testosterone-induced changes in action potential duration in electric organs, Proc. Natl. Acad. Sci. USA 84 (1987) 9295-9298.
7. A.H. Bass, J.P. Denizot, M.A. Marchaterre, Ultrastructural features and hormone-dependent sex differences of mormyrid electric organs, J. Comp. Neurol. 254 (1986) 511-528.
8. R. Bauer, High electrical discharge frequency during aggressive behavior in a mormyrid fish (Gnathonemus petersii), Experientia 28 (1972) 669-670.
9. R. Bauer, Electric organ discharge activity of resting and stimulated Gnathonemus petersii (Mormyridae), Behav. 50 (1974) 306-323.
10. C.C. Bell, J.P. Myers, C.J. Russell, Electric organ discharge patterns during dominance related behavioral displays in Gnathonemus petersii (Mormyridae), J. Comp. Physiol 92 (1974) 201-228.
11. C.C. Bell, S. Libouban, T. Szabo, Pathways of the electric organ discharge command and its corollary discharges in mormyrid fish, J. Comp. Neurol. 216 (1983) 327-338.
12. C. Bell, D. Bodznick, J. Montgomery, J. Bastian, The generation and subtraction of sensory expectations within cerebellum-like structures, Brain Behav. Evol. 50 (1997) 17-31.
13. M.V.L. Bennett, Electric organs, in: W.S. Hoar, D.J. Randall (Eds.), Fish Physiology, Academic Press, London, 1971, pp. 347-491.
14. M.V.L. Bennett, H. Grundfest, Studies on the morphology and electrophysiology of electric organs. III. Electrophysiology of electric organs in mormyrids, in: C. Chagas, A. Carvalho (Eds.), Bioelectrogenesis, Elsevier, New York, 1961, pp. 113-135.
15. M.V.L. Bennett, E. Aljure, Y. Nakajima, G.D. Pappas, Electrotonic junctions between teleost spinal neurons: electrophysiology and ultrastructure, Science 141 (1963) 262-264.
16. M.V.L. Bennett, G. Pappas, E. Aljure, Y. Nakajima, Physiology and ultrastructure of electrotonic junctions, II. Spinal and medullary electromotor nuclei in mormyrid fish. J. Neurophysiol. 30 (1967) 180-208.
17. B.O. Bratton, B. Kramer, Patterns of the electric organ discharge during courtship and spawning in the mormyrid fish Pollimyrus isidori, Behav. Ecol. Sociobiol. 24 (1989) 349-368.
18. B.A. Carlson, C.D. Hopkins. Neural mechanisms in the generation of electric signals in mormyrid fish, in: Society for Neuroscience, New Orleans, 2000, p. 567.15.
19. B.A. Carlson, C.D. Hopkins, Extracellular stimulation of descending electromotor nuclei in the mormyrid Brienomyrus brachyistius and the control of electric signaling behavior, in: 6th International Congress for Neuroethology, Bonn, Germany, 2001, p. 221.
20. B.A. Carlson, C.D. Hopkins, P. Thomas, Androgen correlates of socially induced changes in the electric organ discharge waveform of a mormyrid fish, Horm. Behav. 38 (2000) 177-186.
21. J.D. Crawford, Sex recognition by electric cues in a sound-producing mormyrid fish Pollimyrus isidori, Brain Behav. Evol. 38 (1991) 20-38.
22. J.D. Crawford, Individual and sex specificity in the electric organ discharges of breeding mormyrid fish (Pollimyrus isidori), J. Exp. Biol. 164 (1992) 79-102.
23. J.D. Crawford, M. Hagedorn, C.D. Hopkins, Acoustic communication in an electric fish, Pollimyrus isidori (Mormyridae), J. Comp. Physiol. A 159 (1986) 297-310.
24. K. Elekes, T. Szabo, The mormyrid brainstem III. Ultrastructure and synaptic organization of the medullary 'pacemaker' nucleus, Neuroscience 15 (1985) 431-444.
25. K. Elekes, M. Ravaille, C.C. Bell, S. Libouban, T. Szabo, The mormyrid brainstem II. The medullary electromotor relay nucleus: an ultrastructural horseradish peroxidase study, Neuroscience 15 (1985) 417-430.
26. E.G. Freedman, J. Olyarchuk, M, Marchaterre, A.H. Bass, A temporal analysis of testosterone-induced changes in electric organs and electric organ discharges of mormyrid fishes, J. Neurobiol. 20 (1989) 619-634.
27. M.A. Friedman, C.D. Hopkins, Tracking individual mormyrid electric fish in the field using electric organ discharge waveforms, Anim. Behav. 51 (1996) 391-407.
28. L. Gomez, K. Grant, G. von der Emde, R. Budelli, A model of the electromotor command system in Gnathonemus petersii, in: 5th International Congress for Neuroethology, San Diego, CA, 1998, p. 333.
29. C. Graff, B. Kramer, Trained weakly electric fishes Pollimyrus isidori and Gnathonemus petersii (Mormyridae, Teleostei) discriminate between waveforms of electric pulse discharges, Ethol. 90 (1992) 279-292.
30. K. Grant, C.C. Bell, S. Clausse, M. Ravaille, Morphology and physiology of the brainstem nuclei controlling the electric organ discharge in mormyrid fish, J. Comp. Neurol. 245 (1986) 514-530.
31. K. Grant, S. Clausse, S. Libouban, T. Szabo, Serotoninergic neurons in the mormyrid brain and their projection to the pre-electromotor and primary electrosensory centers: immunohistochemical study, J. Comp. Neurol. 281 (189) 114-128.
32. K. Grant, G. von der Emde, L.G. Sena, C. Mohr, Neural command of electromotor output in mormyrids, J. Exp. Biol. 202 (1999) 1399-1407.
33. W. Heiligenberg, Electrolocation and jamming avoidance in the mormyrid fish Brienomyrus niger, J. Comp. Physiol. A 109 (1976) 357-372.
34. W. Heiligenberg, Principles of Electrolocation and Jamming Avoidance in Electric Fish, A Neuroethological Approach, Springer-Verlag, New York, 1977.
35. W.F. Heiligenberg, Computational Neuroscience Series Neural Nets in Electric Fish, 1991.
36. S. Herfeld, P. Moller, Effects of 17-α-methyltestosterone on sexually dimorphic characters in the weakly discharging electric fish, Brienomyrus niger (Günther, 1866) (Mormyridae): electric organ discharge, ventral body wall indentation, and anal-fin ray bone expansion, Horm. Behav. 34 (1998) 303-319.
37. C.D. Hopkins, Evolution of electric communication channels of mormyrids, Behav. Ecol. Sociobiol. 7 (1980) 1-13.
38. C.D. Hopkins, On the diversity of electric signals in a community of mormyrid electric fish in west Africa, Amer. Zool. 21 (1981) 211-222.
39. C.D. Hopkins, Neuroethology of species recognition in electroreception, in: J.P. Ewert, R.R. Capranica, D.J. Ingle (Eds.), Advances in Vertebrate Neuroethology, Plenum, New York, 1983, pp. 871-881.
40. C.D. Hopkins, Behavior of Mormyridae, in: T.H. Bullock, W. Heiligenberg (Eds.), Electroreception, John Wiley and Sons, New York, 1986, pp. 527-576,
41. C.D. Hopkins, Design features for electric communication, J. Exp. Biol. 202 (1999) 1217-1228.
42. C.D. Hopkins, A.H. Bass, Temporal coding of species recognition signals in an electric fish, Science 212 (1981) 85-87.
43. J. Juranek, W. Metzner, Segregation of behavior-specific synaptic inputs to a vertebrate neuronal oscillator, J. Neurosci. 18 (1998) 9010-9019.
44. M. Kawasaki, The African wave-type electric fish, Gymnarchus niloticus, lacks corollary discharge mechanisms for electrosensory gating, J. Comp. Physiol. A 174 (1994) 133-144.
45. M. Kawasaki, Sensory hyperacuity in the jamming avoidance response of weakly electric fish, Curr. Opin. Neurobiol. 7 (1997) 473-479.
46. Kawasaki, M., Premotor mechanisms for pacemaker control in Gymnarchus niloticus, in: 6th International Congress for Neuroethology, Bonn, Germany, 2001, p. 220.
47. M. Kawasaki, W. Heiligenberg, Distinct mechanisms of modulation in a neuronal oscillator generate different social signals in the electric fish Hypopomus, J. Comp. Physiol. A 165 (1989) 731-742.
48. M. Kawasaki, W. Heiligenberg, 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 (1990) 3896-3904.
49. C.H. Keller, M. Kawasaki, W. Heiligenberg, The control of pacemaker modulations for social communication in the weakly electric fish Sternopygus, J. Comp. Physiol. A 169 (1991) 441-450.
50. G. Kennedy, W. Heiligenberg, Ultrastructural evidence of GABA-ergic inhibition and glutamatergic excitation in the pacemaker nucleus of the gymnotiform electric fish, Hypopomus, J. Comp. Physiol. A 174 (1994) 267-280.
51. M. Konishi, T.T. Takahashi, H. Wagner, W.E. Sullivan, C.E. Carr, Neurophysiological and anatomical substrates of sound localization in the owl, in: G.M. Edelman, W.E. Gan, W.M. Cowan (Eds.), Auditory Function: Neurobiological Bases of Hearing, Wiley, New York, 1988, pp. 721-745.
52. B. Kramer, Electric organ discharge interaction during inter-specific agonistic behavior in freely swimming mormyrid fish: A method to evaluate two or more simultaneous time series of events with a digital analyzer, J. Comp. Physiol. A 93 (1974) 203-235.
53. B. Kramer, Flight-associated discharge pattern in a weakly electric fish, Gnathonemus petersii (Mormyridae, Teleostei), Behav. 59 (1976) 88-95.
54. B. Kramer, The attack frequency of Gnathonemus petersii towards electrically silent, denervated and intact conspecifics and towards another mormyrid (Brienomyrus niger), Behav. Ecol. Sociobiol. 1 (1976) 425-446.
55. B. Kramer, Electric and motor responses of the weakly electric fish, Gnathonemus petersii (Mormyridae), to play-back of social signals, Behav. Ecol. Sociobiol. 6 (1979) 67-79.
56. B. Kramer, Electric organ discharges and their relation to sex in mormyrid fishes, Naturwissenschaften 84 (1997) 119-121.
57. B. Kramer, Electric organ discharges and sex in mormyrid fishes: a field study, Adv. Ethol. 32 (1997) 106.
58. B. Kramer, R. Bauer, Agonistic behavior and electric signaling in a mormyrid fish (Gnathonemus petersii), Behav. Ecol. Sociobiol 1 (1976) 45-61.
59. B. Kramer, B. Kuhn, Species recognition by the sequence of discharge intervals in weakly electric fishes of the genus Campylomormyrus (Mormyridae, Teleostei), Anim. Behav 48 (1994) 435-445.
60. R.E. Landsman, Sex differences in external morphology and electric organ discharges in imported Gnathonemus petersii (Mormyritormes), Anim. Behav 46 (1993) 417-429.
61. R.E. Landsman, P. Moller, Testosterone changes the electric organ discharge and external morphology of the mormyrid fish Gnathonemus petersii (Mormyriformes), Experientia 44 (1988) 900-903.
62. H. Lücker, B. Kramer, Development of a sex difference in the preferred latency response in the weakly electric fish, Pollimyrus isidori (Cuvier et Valenciennes)(Mormyridae, Teleostei), Behav. Ecol. Sociobiol. 9 (1981) 103-109.
63. J. Meek, H.W.J. Joosten, Distribution of serotonin in the brain of the mormyrid teleost Gnathonemus petersii, J. Comp. Neurol. 281 (1989) 206-224.
64. W. Metzner, Neural circuitry for communication, jamming avoidance in gymnotiform electric fish, J. Exp. Biol. 202 (1999) 1365-1375.
65. P. Moller, Communication in weakly electric fish (Gnathonemus niger, Mormyridae) Part 1. Variation of electric organ discharge frequency elicited by controlled electric stimuli, Anim. Behav. 18 (1970) 768-786.
66. P. Moller, Electric signals and schooling behavior in a weakly electric fish (Marcusenius cyprinoides, Mormyriformes), Science (1976) 697-699.
67. P. Moller, R. Bauer, Communication in weakly electric fish (Gnathonemus petersii, Mormyridae) Part 2. Interaction of electric organ discharge activities of two fish, Anim. Behav. 21 (1973) 501-512.
68. P. Moller, J. Serrier, Species recognition in mormyrid weakly electric fish, Anim. Behav. 34 (1986) 333-339.
69. P. Moller, J. Serrier, A. Squire, Spacing and aggregation in mormyrid fish, Neurosci. Lett. 3 (1979) S60.
70. P. Moller, J. Serrier, D. Bowling, Electric organ discharge displays during social encounter in the weakly electric fish Brienomyrus niger L. (Mormyridae), Ethol. 82 (1989) 177-191.
71. R. Niso, J. Serrier, K. Grant, Mesencephalic control of the bulbar electromotor network in the mormyrid Gnathonemus petersii, Eur. J. Neurosci. 2 (1989) 176.
72. C.J. Russell, J.P. Myers, C.C. Bell, The echo response in Gnathonemus petersii (Mormyridae), J. Comp. Physiol. 92 (1974) 181-200.
73. A. Scheffel, B. Kramer, Electric signals in the social behavior of sympatric elphantfish (Mormyridae, Teleostei) from the upper Zambezi river, Naturwissenschaften 87 (2000) 142-147.
74. J. Serrier, P. Moller, Social behavior in mormyrid fish (Mormyriformes: Pisces): Short and long-term changes associated with repeated interactions, in: T. Szabo, G. Czeh (Eds.), Advances in Physiological Science, Pergamon Press, Budapest, 1981, pp. 221-233.
75. J. Serrier, P. Moller, Patterns of electric organ discharge activity in the weakly electric fish Brienomyrus niger L. (Mormyridae), J. Exp. Biol. 48 (1989) 235-244.
76. T. Szabo, Anatomophysiologie de centres nerveux specifiques de quelques organes électriques, in: C. Chagas, X. Paes del Carvahlo (Eds.), Bioelectrogenesis, Elsevier, Amsterdam, 1961, pp. 185-201.
77. C. Teyssedre, J. Serrier, Temporal spacing of signals in communication studied in weakly electric mormyrid fish (Teleostei, Pisces), Behav. Proc. 12 (1986) 77-98.
78. G. von der Emde, Electrolocation of capacitive objects in four species of pulse-type weakly electric fish: II. Electric signalling behaviour, Ethol. 92 (1992) 177-192.
79. G. von der Emde, Active electrolocation of objects in weakly electric fish, J. Exp. Biol. 202 (1999) 1205-1215.
80. G. von der Emde, L. Gomez-Sena, R. Niso, K. Grant, The midbrain precommand nucleus of the mormyrid electromotor network, J. Neurosci. 20 (2000) 5483-5495.
81. M.F. Wullimann, R.G. Northcutt, Visual and electrosensory circuits of the diencephalon in mormyrids: An evolutionary perspective, J. Comp. Neurol. 297 (1990) 537-552.
82. M.A. Xu-Friedman, Central mechanisms of temporal analysis in the knollenorgan pathway of mormyrid electric fish, J. Exp. Biol. 202 (1999) 1311-1318.
83. B.A Carlson, Neuroanatomy of the mormyrid electromotor control system, J. Comp. Neurol. 454 (2002) 440-455.