Biophysical Basis of Electric Signal Diversity

  • Michael R. MarkhamEmail author
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 70)


The electric sensory and communication signals of electric fish show remarkable diversity in their waveforms, and this diversity is driven by selective pressures related to reproduction, sensory ecology, predation avoidance, and the metabolic costs of signaling. These electric signals are generated by electrocytes, electrically excitable cells that comprise the electric organ. Although the signaling rate is controlled by a brainstem pacemaker or command nucleus that coordinates the discharge of electrocytes within the electric organ, waveform diversity arises primarily from the underlying biophysics of electrocytes, including their passive electrical properties, morphology, voltage-gated ion channels, and regulatory pathways that modify electrocyte function. Electrocyte morphology and innervation patterns are a major source of signal diversity in the African mormyrid electric fishes, whereas diversity of ion-channel expression patterns has a strong influence on waveform diversity in the South American gymnotiforms. Convergent evolution of ion channels in both clades further contributes to signal diversity. Little is known about the ionic mechanisms of signal diversity in mormyrids. Additionally, asynchronous activation of distinct electric organ regions with different electrocyte properties enhances waveform complexity in some gymnotiforms. Signal diversity associated with development and sexual dimorphism arises from the effects of steroid hormones on electrocyte ion channel kinetics, and the rapid changes in signal waveform are mediated by the effects of peptide hormones on electrocyte action potentials and ion channel function. These processes have been investigated primarily in a small number of gymnotiforms, highlighting a great need for broader comparative studies across gymnotiform species and between mormyrids and gymnotiforms.


Action potential Electric organ Electric organ discharge Electrocyte Ion channels Melanocortin hormones Sexual dimorphism Steroid hormones 



Preparation of this chapter was supported by Grants IOS1644965, IOS1350753, and IOS1257580 from the National Science Foundation and by the Case-Hooper endowment, funded through a gift from Dr. and Mrs. Robert Case to The University of Oklahoma, Norman.

Compliance with Ethics Requirements

Michael R. Markham declares that he has no conflict of interest.


  1. Aguilera PA, Castello ME, Caputi AA (2001) Electroreception in Gymnotus carapo: differences between self-generated and conspecific-generated signal carriers. J Exp Biol 204(Pt 2):185–198PubMedGoogle Scholar
  2. Albert JS, Crampton WGR (2005) Diversity and phylogeny of neotropical electric fishes. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, New York, pp 360–409CrossRefGoogle Scholar
  3. Alle H, Roth A, Geiger JRP (2009) Energy-efficient action potentials in hippocampal mossy fibers. Science 325(5946):1405–1408. Scholar
  4. Allee SJ, Markham MR, Stoddard PK (2009) Androgens enhance plasticity of an electric communication signal in female knifefish, Brachyhypopomus pinnicaudatus. Horm Behav 56(2):264–273. Scholar
  5. Alves-Gomes J, Hopkins CD (1997) Molecular insights into the phylogeny of mormyriform fishes and the evolution of their electric organs. Brain Behav Evol 49(6):324–350PubMedCrossRefGoogle Scholar
  6. Ardanaz JL, Silva A, Macadar O (2001) Temperature sensitivity of the electric organ discharge waveform in Gymnotus carapo. J Comp Physiol A 187(11):853–864CrossRefGoogle Scholar
  7. Arnegard ME, McIntyre PB, Harmon LJ, Zelditch ML, Crampton WG, Davis JK, Sullivan JP, Lavoue S, Hopkins CD (2010a) Sexual signal evolution outpaces ecological divergence during electric fish species radiation. Am Nat 176(3):335–356. Scholar
  8. Arnegard ME, Zwickl DJ, Lu Y, Zakon HH (2010b) Old gene duplication facilitates origin and diversification of an innovative communication system--twice. Proc Natl Acad Sci U S A 107(51):22172–22177. Scholar
  9. Assad C, Rasnow B, Stoddard PK (1999) Electric organ discharges and electric images during electrolocation. J Exp Biol 202(Pt 10):1185–1193PubMedGoogle Scholar
  10. Ban Y, Smith BE, Markham MR (2015) A highly polarized excitable cell separates sodium channels from sodium-activated potassium channels by more than a millimeter. J Neurophysiol 114(1):520–530PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bass AH, Hopkins CD (1985) Hormonal control of sex differences in the electric organ discharge (EOD) of mormyrid fishes. J Comp Physiol A 156(5):587–604CrossRefGoogle Scholar
  12. Bass AH, Volman SF (1987) From behavior to membranes: testosterone-induced changes in action potential duration in electric organs. Proc Natl Acad Sci U S A 84(24):9295–9298PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bass AH, Denizot JP, Marchaterre MA (1986) Ultrastructural features and hormone-dependent sex differences of mormyrid electric organs. J Comp Neurol 254(4):511–528. Scholar
  14. Bennett MVL (1961) Modes of operation of electric organs. Ann N Y Acad Sci 94:458–509CrossRefGoogle Scholar
  15. Bennett MVL (1970) Comparative physiology: electric organs. Annu Rev Physiol 32:471–528PubMedCrossRefGoogle Scholar
  16. Bennett MVL, Grundfest H (1961) Studies on the morphology and electrophysiology of electric organs III: electrophysiology of electric organs in mormyrids. In: Chagas C, APd C (eds) Bioelectrogenesis: a comparative survey of its mechanisms with particular emphasis on electric fishes. Elsevier Pub. Co., Amsterdam, New York, pp 113–135Google Scholar
  17. Budelli G, Hage TA, Wei A, Rojas P, Jong YJ, O’Malley K, Salkoff L (2009) Na+−activated K+ channels express a large delayed outward current in neurons during normal physiology. Nat Neurosci 12(6):745–750. Scholar
  18. Caputi AA (1999) The electric organ discharge of pulse gymnotiforms: the transformation of a simple impulse into a complex spatio-temporal electromotor pattern. J Exp Biol 202:1229–1241PubMedGoogle Scholar
  19. Caputi AA, Macadar O, Trujillo-Cenóz O (1994) Waveform generation in Rhamphichthys rostratus (L) (Teleostei, Gymnotiformes). J Comp Physiol A 174(5):633–642CrossRefGoogle Scholar
  20. Caputi AA, Silva AC, Macadar O (1998) The electric organ discharge of Brachyhypopomus pinnicaudatus. The effects of environmental variables on waveform generation. Brain Behav Evol 52(3):148–158PubMedCrossRefGoogle Scholar
  21. Caputi AA, Carlson BA, Macadar O (2005) Electric organs and their control. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, New York, pp 410–451CrossRefGoogle Scholar
  22. Carter BC, Bean BP (2009) Sodium entry during action potentials of mammalian neurons: incomplete inactivation and reduced metabolic efficiency in fast-spiking neurons. Neuron 64(6):898–909. Scholar
  23. Catania KC (2017) Power transfer to a human during an eectric eel’s shocking leap. Curr Biol 27(18):2887–2891. e2882. Scholar
  24. Crampton WG, Albert JS (2006) Evolution of electric signal diversity in gymnotiform fishes. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Communication in fishes. Science Publishers, Enfield, pp 647–731Google Scholar
  25. Crampton WG, Lovejoy NR, Waddell JC (2011) Reproductive character displacement and signal ontogeny in a sympatric assemblage of electric fish. Evolution 65(6):1650–1666. Scholar
  26. Crampton WGR, Rodríguez-Cattáneo A, Lovejoy NR, Caputi AA (2013) Proximate and ultimate causes of signal diversity in the electric fish Gymnotus. J Exp Biol 216(13):2523–2541. Scholar
  27. Dunlap KD, McAnelly ML, Zakon HH (1997) Estrogen modifies an electrocommunication signal by altering the electrocyte sodium current in an electric fish, Sternopygus. J Neurosci 17(8):2869–2875PubMedPubMedCentralCrossRefGoogle Scholar
  28. Ferrari MB, Zakon HH (1993) Conductances contributing to the action potential of Sternopygus electrocytes. J Comp Physiol A 173(3):281–292PubMedCrossRefGoogle Scholar
  29. Ferrari MB, McAnelly ML, Zakon HH (1995) Individual variation in and androgen-modulation of the sodium current in electric organ. J Neurosci 15(5 Pt 2):4023–4032PubMedPubMedCentralCrossRefGoogle Scholar
  30. Few WP, Zakon HH (2007) Sex differences in and hormonal regulation of Kv1 potassium channel gene expression in the electric organ: molecular control of a social signal. Dev Neurobiol 67(5):535–549. Scholar
  31. Franchina CR (1997) Ontogeny of the electric organ discharge and the electric organ in the weakly electric pulse fish Brachyhypopomus pinnicaudatus (Hypopomidae, Gymnotiformes). J Comp Physiol A 181(2):111–119PubMedCrossRefGoogle Scholar
  32. Franchina CR, Stoddard PK (1998) Plasticity of the electric organ discharge waveform of the electric fish Brachyhypopomus pinnicaudatus. I Quantification of day-night changes. J Comp Physiol, A 183(6):759–768CrossRefGoogle Scholar
  33. Franchina CR, Salazar VL, Volmar CH, Stoddard PK (2001) Plasticity of the electric organ discharge waveform of male Brachyhypopomus pinnicaudatus. II. Social effects. J Comp Physiol, A 187(1):45–52CrossRefGoogle Scholar
  34. Gallant JR, Arnegard ME, Sullivan JP, Carlson BA, Hopkins CD (2011) Signal variation and its morphological correlates in Paramormyrops kingsleyae provide insight into the evolution of electrogenic signal diversity in mormyrid electric fish. J Comp Physiol A 197(8):799–817. Scholar
  35. Gallant JR, Traeger LL, Volkening JD, Moffett H, Chen P-H, Novina CD, Phillips GN, Anand R, Wells GB, Pinch M, Güth R, Unguez GA, Albert JS, Zakon HH, Samanta MP, Sussman MR (2014) Genomic basis for the convergent evolution of electric organs. Science 344(6191):1522–1525. Scholar
  36. Gavassa S, Stoddard PK (2012) Food restriction promotes signaling effort in response to social challenge in a short-lived electric fish. Horm Behav 62(4):381–388. Scholar
  37. Goldina A, Gavassa S, Stoddard PK (2011) Testosterone and 11-ketotestosterone have different regulatory effects on electric communication signals of male Brachyhypopomus gauderio. Horm Behav 60(2):139–147. Scholar
  38. Hage TA, Salkoff L (2012) Sodium-activated potassium channels are functionally coupled to persistent sodium currents. J Neurosci 32(8):2714–2721. Scholar
  39. 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 156:511–523CrossRefGoogle Scholar
  40. Hopkins CD (1972) Sex differences in electric signaling in an electric fish. Science 176(4038):1035–1037. Scholar
  41. Hopkins CD (1980) Evolution of electric communication channels of mormyrids. Behav Ecol Sociobiol 7(1):1–13CrossRefGoogle Scholar
  42. Hopkins CD (1981) On the diversity of eectric signals in a community of mormyrid electric fish in West Africa. Am Zool 21(1):211–222CrossRefGoogle Scholar
  43. Hopkins CD (1999) Design features for electric communication. J Exp Biol 202(Pt 10):1217–1228PubMedGoogle Scholar
  44. Hopkins CD, Comfort NC, Bastian J, Bass AH (1990) Functional analysis of sexual dimorphism in an electric fish, Hypopomus pinnicaudatus, order Gymnotiformes. Brain Behav Evol 35(6):350–367PubMedCrossRefGoogle Scholar
  45. Hurley IA, Mueller RL, Dunn KA, Schmidt EJ, Friedman M, Ho RK, Prince VE, Yang Z, Thomas MG, Coates MI (2007) A new time-scale for ray-finned fish evolution. Proc Biol Sci 274(1609):489–498PubMedCrossRefGoogle Scholar
  46. Kirschbaum F (1983) Myogenic electric organ precedes the neurogenic organ in apteronotid fish. Naturwissenschaften 70(4):205–207PubMedCrossRefGoogle Scholar
  47. Kirschbaum F, Schwassmann HO (2008) Ontogeny and evolution of electric organs in gymnotiform fish. J Physiol Paris 102(4–6):347–356. Scholar
  48. Lavoué S, Miya M, Arnegard ME, Sullivan JP, Hopkins CD, Nishida M (2012) Comparable ages for the independent origins of electrogenesis in African and South American weakly electric fishes. PLoS One 7(5):e36287. Scholar
  49. Lewis JE, Gilmour KM, Moorhead MJ, Perry SF, Markham MR (2014) Action potential energetics at the organismal level reveal a trade-off in efficiency at high firing rates. J Neurosci 34(1):197–201. Scholar
  50. Liu H, Wu MM, Zakon HH (2007) Individual variation and hormonal modulation of a sodium channel beta subunit in the electric organ correlate with variation in a social signal. Dev Neurobiol 67(10):1289–1304. Scholar
  51. Liu H, Wu MM, Zakon HH (2008) A novel Na+ channel splice form contributes to the regulation of an androgen-dependent social signal. J Neurosci 28(37):9173–9182. Scholar
  52. Lorenzo D, Velluti JC, Macadar O (1988) Electrophysiological properties of abdominal electrocytes in the weakly electric fish Gymnotus carapo. J Comp Physiol A 162(1):141–144CrossRefGoogle Scholar
  53. Macadar O, Lorenzo D, Velluti JC (1989a) Waveform generation of the electric organ discharge in Gymnotus carapo. J Comp Physiol A 165(3):353–360CrossRefGoogle Scholar
  54. Macadar O, Lorenzo D, Velluti JC (1989b) Waveform generation of the electric organ discharge in Gymnotus carapo 2. Electrophysiological properties of single electrocytes. J Comp Physiol A 165(3):353–360. Scholar
  55. Markham MR (2013) Electrocyte physiology: 50 years later. J Exp Biol 216(13):2451–2458. Scholar
  56. Markham MR, Stoddard PK (2005) Adrenocorticotropic hormone enhances the masculinity of an electric communication signal by modulating the waveform and timing of action potentials within individual cells. J Neurosci 25(38):8746–8754PubMedPubMedCentralCrossRefGoogle Scholar
  57. Markham MR, Stoddard PK (2013) Cellular mechanisms of developmental and sex differences in the rapid hormonal modulation of a social communication signal. Horm Behav 63(4):586–597. Scholar
  58. Markham MR, Zakon HH (2014) Ionic mechanisms of microsecond-scale spike timing in single cells. J Neurosci 34(19):6668–6678. Scholar
  59. Markham MR, Allee SJ, Goldina A, Stoddard PK (2009a) Melanocortins regulate the electric waveforms of gymnotiform electric fish. Horm Behav 55(2):306–313. Scholar
  60. Markham MR, McAnelly ML, Stoddard PK, Zakon HH (2009b) Circadian and social cues regulate ion channel trafficking. PLoS Biol 7(9):e1000203PubMedPubMedCentralCrossRefGoogle Scholar
  61. Markham MR, Kaczmarek LK, Zakon HH (2013) A sodium-activated potassium channel supports high-frequency firing and reduces energetic costs during rapid modulations of action potential amplitude. J Neurophysiol 109(7):1713–1723. Scholar
  62. McAnelly ML, Zakon HH (2000) Coregulation of voltage-dependent kinetics of Na(+) and K(+) currents in electric organ. J Neurosci 20(9):3408–3414PubMedPubMedCentralCrossRefGoogle Scholar
  63. McAnelly ML, Zakon HH (2007) Androgen modulates the kinetics of the delayed rectifying K+ current in the electric organ of a weakly electric fish. Dev Neurobiol 67(12):1589–1597. Scholar
  64. McAnelly L, Silva A, Zakon HH (2003) Cyclic AMP modulates electrical signaling in a weakly electric fish. J Comp Physiol A 189(4):273–282. Scholar
  65. McGregor PK, Westby GWM (1992) Discrimination of individually characteristic electric organ discharges by a weakly electric fish. Anim Behav 43(Part 6):977–986CrossRefGoogle Scholar
  66. Mills A, Zakon HH (1991) Chronic androgen treatment increases action potential duration in the electric organ of Sternopygus. J Neurosci 11(8):2349–2361PubMedPubMedCentralCrossRefGoogle Scholar
  67. Nagel R, Kirschbaum F, Tiedemann R (2017) Electric organ discharge diversification in mormyrid weakly electric fish is associated with differential expression of voltage-gated ion channel genes. J Comp Physiol A 203(3):183–195. Scholar
  68. Pinch M, Guth R, Samanta MP, Chaidez A, Unguez GA (2016) The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome. PeerJ 4:e1828. Scholar
  69. Quintana L, Silva A, Berois N, Macadar O (2004) Temperature induces gonadal maturation and affects electrophysiological sexual maturity indicators in Brachyhypopomus pinnicaudatus from a temperate climate. J Exp Biol 207(11):1843–1853PubMedCrossRefGoogle Scholar
  70. Reardon EE, Parisi A, Krahe R, Chapman LJ (2011) Energetic constraints on electric signalling in wave-type weakly electric fishes. J Exp Biol 214(Pt 24):4141–4150. Scholar
  71. Roberts TR (1975) Geographical distribution of african freshwater fishes. Zool J Linn Soc 57(4):249–319. Scholar
  72. Salazar VL, Stoddard PK (2008) Sex differences in energetic costs explain sexual dimorphism in the circadian rhythm modulation of the electrocommunication signal of the gymnotiform fish Brachyhypopomus pinnicaudatus. J Exp Biol 211(Pt 6):1012–1020. Scholar
  73. Salazar VL, Krahe R, Lewis JE (2013) The energetics of electric organ discharge generation in gymnotiform weakly electric fish. J Exp Biol 216(Pt 13):2459–2468. Scholar
  74. Scheich H (1977) Neural basis of communication in the high frequency electric fish, Eigenmannia virescens (jamming avoidance response). J Comp Physiol A 113(2):181–206CrossRefGoogle Scholar
  75. Shenkel S, Sigworth FJ (1991) Patch recordings from the electrocytes of Electrophorus electricus. Na currents and PNa/PK variability. J Gen Physiol 97(5):1013–1041. Scholar
  76. Sierra F, Comas V, Buno W, Macadar O (2005) Sodium-dependent plateau potentials in electrocytes of the electric fish Gymnotus carapo. J Comp Physiol, A 191(1):1CrossRefGoogle Scholar
  77. Sierra F, Comas V, Buno W, Macadar O (2007) Voltage-gated potassium conductances in Gymnotus electrocytes. Neuroscience 145(2):453–463. Scholar
  78. Silva A, Quintana L, Galeano M, Errandonea P, Macadar O (1999) Water temperature sensitivity of EOD waveform in Brachyhypopomus pinnicaudatus. J Comp Physiol A 185(2):187–197CrossRefGoogle Scholar
  79. Sinnett PM, Markham MR (2015) Food deprivation reduces and leptin increases the amplitude of an active sensory and communication signal in a weakly electric fish. Horm Behav 71:31–40. Scholar
  80. Stoddard PK (1999) Predation enhances complexity in the evolution of electric fish signals. Nature 400(6741):254–256PubMedCrossRefGoogle Scholar
  81. Stoddard PK, Markham MR (2008) Signal cloaking by electric fish. Bioscience 58(5):415–425PubMedPubMedCentralCrossRefGoogle Scholar
  82. Stoddard PK, Markham MR, Salazar VL (2003) Serotonin modulates the electric waveform of the gymnotiform electric fish Brachyhypopomus pinnicaudatus. J Exp Biol 206(Pt 8):1353–1362PubMedPubMedCentralCrossRefGoogle Scholar
  83. Stoddard PK, Markham MR, Salazar VL, Allee S (2007) Circadian rhythms in electric waveform structure and rate in the electric fish Brachyhypopomus pinnicaudatus. Physiol Behav 90(1):11–20PubMedCrossRefGoogle Scholar
  84. Swapna I, Ghezzi A, York JM, Markham MR, Halling DB, Lu Y, Gallant JR, Zakon HH (2018) Electrostatic tuning of a potassium channel in electric fish. Curr Biol 28(13):2094–2102.e2095. Scholar
  85. Thompson A, Infield DT, Smith AR, Smith GT, Ahern CA, Zakon HH (2018) Rapid evolution of a voltage-gated sodium channel gene in a lineage of electric fish leads to a persistent sodium current. PLoS Biol 16(3):e2004892. Scholar
  86. Waddell JC, Rodriguez-Cattaneo A, Caputi AA, Crampton WGR (2016) Electric organ discharges and near-field spatiotemporal patterns of the electromotive force in a sympatric assemblage of Neotropical electric knifefish. J Physiol Paris 110(3 Pt B):164–181. Scholar
  87. Westby GWM, Kirschbaum F (1977) Emergence and development of electric organ discharge in mormyrid fish, Pollimyrus isidori. 1. Larval discharge. J Comp Physiol 122(2):251–271CrossRefGoogle Scholar
  88. Westby GWM, Kirschbaum F (1978) Emergence and development of electric organ discharge in mormyrid fish, Pollimyrus isidori. 2. Replacement of larval by adult discharge. J Comp Physiol 127(1):45–59CrossRefGoogle Scholar
  89. Zakon HH, Lu Y, Zwickl DJ, Hillis DM (2006) Sodium channel genes and the evolution of diversity in communication signals of electric fishes: convergent molecular evolution. Proc Natl Acad Sci U S A 103(10):3675–3680. Scholar

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Authors and Affiliations

  1. 1.Department of BiologyUniversity of OklahomaNormanUSA

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