Advertisement

Journal of Comparative Physiology A

, Volume 192, Issue 6, pp 613–624 | Cite as

Regulation and modulation of electric waveforms in gymnotiform electric fish

  • Philip K. StoddardEmail author
  • Harold H. Zakon
  • Michael R. Markham
  • Lynne McAnelly
Review

Abstract

Weakly electric gymnotiform fish specialize in the regulation and modulation of the action potentials that make up their multi-purpose electric signals. To produce communication signals, gymnotiform fish modulate the waveforms of their electric organ discharges (EODs) over timescales spanning ten orders of magnitude within the animal’s life cycle: developmental, reproductive, circadian, and behavioral. Rapid changes lasting milliseconds to seconds are the result of direct neural control of action potential firing in the electric organ. Intermediate-term changes taking minutes to hours result from the action of melanocortin peptides, the pituitary hormones that induce skin darkening and cortisol release in many vertebrates. Long-term changes in the EOD waveform taking days to weeks result from the action of sex steroids on the electrocytes in the electric organ as well as changes in the neural control structures in the brain. These long-term changes in the electric organ seem to be associated with changes in the expression of voltage-gated ion channels in two gene families. Electric organs express multiple voltage-gated sodium channel genes, at least one of which seems to be regulated by androgens. Electric organs also express multiple subunits of the shaker (Kv1) family of voltage-gated potassium channels. Expression of the Kv1 subtype has been found to vary with the duration of the waveform in the electric signal. Our increasing understanding of the mechanisms underlying precise control of electric communication signals may yield significant insights into the diversity of natural mechanisms available for modifying the performance of ion channels in excitable membranes. These mechanisms may lead to better understanding of normal function in a wide range of physiological systems and future application in treatment of disease states involving pathology of excitable membranes.

Keywords

Androgens Electrogenesis Phenotypic plasticity 

Notes

Acknowledgements

The research was supported by NIH grants MBRS GM08205 to PKS, NS025513 to HHZ, and MH064550 to MRM.

References

  1. Allada R, Emery P, Takahashi JS, Rosbash M (2001) Stopping time: the genetics of fly and mouse circadian clocks. Annu Rev Neurosci 24:1091–1119PubMedCrossRefGoogle Scholar
  2. Andreotti F, Redfern PH, Lemmer B (1997) Physiology and pharmacology of biological rhythms. Springer, Berlin Heidelberg New YorkGoogle Scholar
  3. Ashcroft FC (2000) Ion channels and disease. Academic, San DiegoGoogle Scholar
  4. Bass AH (1986) Electric organs revisited. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 13–70Google Scholar
  5. Bell CC, Bradbury J, Russell CJ (1976) The electric organ of a mormyrid as a current and voltage source. J Comp Physiol 110A:65–88Google Scholar
  6. Bennett MLV (1961) Modes of operation of electric organs. Ann NY Acad Sci 94:458–509CrossRefGoogle Scholar
  7. Bennett MV (1970) Comparative physiology: electric organs. Annu Rev Physiol 32:471–528PubMedCrossRefGoogle Scholar
  8. Bennett MVL, Grundfest H (1959) Electrophysiology of electric organ in Gymnotus carapo. J Gen Physiol 42:1067–1104PubMedCrossRefGoogle Scholar
  9. Bennett MV, Pappas GD, Gimenez M, Nakajima Y (1967) Physiology and ultrastructure of electrotonic junctions. IV. Medullary electromotor nuclei in gymnotid fish. J Neurophysiol 30:236–300PubMedGoogle Scholar
  10. Bruguerolle B, Giaufre E, Prat M (1991) Temporal variations in transcutaneous passage of drugs: the example of lidocaine in children and in rats. Chronobiol Int 8:277–282PubMedCrossRefGoogle Scholar
  11. Burioka N, Suyama H, Sako T, Shimizu E (2000) Circadian rhythm in peak expiratory flow: alteration with nocturnal asthma and theophylline chronotherapy. Chronobiol Int 17:513–519PubMedCrossRefGoogle Scholar
  12. Calabrese RL (1998) Cellular, synaptic, network, and modulatory mechanisms involved in rhythm generation. Curr Opin Neurobiol 8:710–717PubMedCrossRefGoogle Scholar
  13. 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
  14. Dong Y, Nasif FJ, Tsui JJ, Ju WY, Cooper DC, Hu XT, Malenka RC, White FJ (2005) Cocaine-induced plasticity of intrinsic membrane properties in prefrontal cortex pyramidal neurons: adaptations in potassium currents. J Neurosci 25:936–940PubMedCrossRefGoogle Scholar
  15. Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96:271–290PubMedCrossRefGoogle Scholar
  16. 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 168:521–532PubMedCrossRefGoogle Scholar
  17. Elekes K, Szabo T (1981) Synaptology of the command (pacemaker) nucleus in the brain of the weakly electric fish, Sternarchus (Apteronotus) albifrons. Neuroscience 6:443–460PubMedCrossRefGoogle Scholar
  18. Fathi Z, Iben LG, Parker EM (1995) Cloning, expression, and tissue distribution of a fifth melanocortin receptor subtype. Neurochem Res 20:107–113PubMedCrossRefGoogle Scholar
  19. Ferrari MB, Zakon HH (1993) Conductances contributing to the action potential of Sternopygus electrocytes. J Comp Physiol A 173:281–292PubMedCrossRefGoogle Scholar
  20. Ferrari MB, McAnelly ML, Zakon HH (1995) Individual variation in and androgen-modulation of the sodium current in electric organ. J Neurosci 15:4023–4032PubMedGoogle Scholar
  21. Few WP, Zakon HH (2001) Androgens alter electric organ discharge pulse duration despite stability in electric organ discharge frequency. Horm Behav 40:434–442PubMedCrossRefGoogle Scholar
  22. Filipski E, King VM, Li X, Granda TG, Mormont MC, Liu X, Claustrat B, Hastings MH, Levi F (2002) Host circadian clock as a control point in tumor progression. J Natl Cancer Inst 94:690–697PubMedGoogle Scholar
  23. 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 183:759–768PubMedCrossRefGoogle Scholar
  24. 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 187:45–52PubMedCrossRefGoogle Scholar
  25. Fu L, Pelicano H, Liu J, Huang P, Lee C (2002) The circadian gene Period2 plays an important role in tumor suppression and DNA damage response in vivo. Cell 111:41–50PubMedCrossRefGoogle Scholar
  26. Gelfant S, Ozawa A, Chalker DK, Smith JG Jr (1982) Circadian rhythms and differences in epidermal and in dermal cell proliferation in uninvolved and involved psoriatic skin in vivo. J Invest Dermatol 78:58–62PubMedCrossRefGoogle Scholar
  27. Hadley ME, Haskell-Luevano C (1999) The proopiomelanocortin system. Ann NY Acad Sci 885:1–21PubMedGoogle Scholar
  28. Hagedorn M (1995) The electric fish Hypopomus occidentalis can rapidly modulate the amplitude and duration of its electric organ discharges. Anim Behav 49:1409–1413CrossRefGoogle Scholar
  29. Hagedorn M, Zelick R (1989) Relative dominance among males is expressed in the electric organ discharge characteristics of a weakly electric fish. Anim Behav 38:520–525CrossRefGoogle Scholar
  30. Hardin PE (2000) From biological clock to biological rhythms. Genome Biol 1(Reviews):1023Google Scholar
  31. Haus E, Smolensky MH (1999) Biologic rhythms in the immune system. Chronobiol Int 16:581–622PubMedCrossRefGoogle Scholar
  32. Hobson AJ, Isom LL (2003) Cloning and expression of novel voltage gated Na+ channel subunits in the genome of Danio rerio. Soc Neurosci Abstr 29(8.3)Google Scholar
  33. Hoglund E, Balm PH, Winberg S (2002a) Behavioural and neuroendocrine effects of environmental background colour and social interaction in Arctic charr (Salvelinus alpinus). J Exp Biol 205:2535–2543Google Scholar
  34. Hoglund E, Balm PH, Winberg S (2002b) Stimulatory and inhibitory effects of 5-HT(1A) receptors on adrenocorticotropic hormone and cortisol secretion in a teleost fish, the Arctic charr (Salvelinus alpinus). Neurosci Lett 324:193–196CrossRefGoogle Scholar
  35. Hopkins CD (1974) Electric communication in the reproductive behavior of Sternopygus macrurus (Gymnotoidei). Z Tierpsych 35:518–535Google Scholar
  36. Hopkins CD (1991) Hypopomus pinnicaudatus (Hypopomidae) a new species of gymnotiform fish from French Guiana. Copeia 1991:151–161CrossRefGoogle Scholar
  37. Hopkins CD (1999) Design features for electric communication. J Exp Biol 202:1217–1228PubMedGoogle Scholar
  38. 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 35:350–367PubMedCrossRefGoogle Scholar
  39. Hruby VJ, Lu D, Sharma SD, Castrucci AL, Kesterson RA, al-Obeidi FA, Hadley ME, Cone RD (1995) Cyclic lactam alpha-melanotropin analogues of Ac-Nle4-cyclo[Asp5, d-Phe7,Lys10] alpha-melanocyte-stimulating hormone-(4–10)-NH2 with bulky aromatic amino acids at position 7 show high antagonist potency and selectivity at specific melanocortin receptors. J Med Chem 38:3454–3461PubMedCrossRefGoogle Scholar
  40. Isom LL (2001) Sodium channel beta subunits: anything but auxiliary. Neuroscientist 7:42–54PubMedGoogle Scholar
  41. Keith LG, Oleszczuk JJ, Laguens M (2001) Circadian rhythm chaos: a new breast cancer marker. Int J Fertil Womens Med 46:238–247PubMedGoogle Scholar
  42. Keynes RD, Martins-Ferreira H (1953) Membrane potentials in the electroplates of the electric eel. J Physiol 119:315–351PubMedGoogle Scholar
  43. Kramer B, Zupanc GKH (1986) Conditioned discrimination of electric waves differing only in form and harmonic content in the electric fish, Eigenmannia. Naturwissenschaften 73:S679–S681CrossRefGoogle Scholar
  44. Levi F (2001) Circadian chronotherapy for human cancers. Lancet Oncol 2:307–315PubMedCrossRefGoogle Scholar
  45. Liu H, Zakon H (2004) Expression and alternative mRNA splicing of sodium channel subunits correlate with cellular excitability of electrocytes in a weakly electric fish. Soc Neurosci Abstr 30(634.15)Google Scholar
  46. Liu H, Wu M, Zakon HH (2005) Coexpression of an electric fish Nav1.4 homolog and two alternatively spliced Na channel beta 1 subunits in Xenopus oocytes. Soc Neurosci Abstr 31(151.17)Google Scholar
  47. Lopreato GF, Lu Y, Southwell A, Atkinson NS, Hillis DM, Wilcox TP, Zakon HH (2001) Evolution and divergence of sodium channel genes in vertebrates. Proc Natl Acad Sci USA 98:7588–7592PubMedCrossRefGoogle Scholar
  48. Lossin C, Wang DW, Rhodes TH, Vanoye CG, George AL Jr (2002) Molecular basis of an inherited epilepsy. Neuron 34:877–884PubMedCrossRefGoogle Scholar
  49. Lossin C, Rhodes TH, Desai RR, Vanoye CG, Wang D, Carniciu S, Devinsky O, George AL Jr (2003) Epilepsy-associated dysfunction in the voltage-gated neuronal sodium channel SCN1A. J Neurosci 23:11289–11295PubMedGoogle Scholar
  50. Markham MR, Stoddard PK (2003) A melanocortin receptor modulates the amplitude and repolarization time of electrocyte action potentials in male electric fish, Brachyhypopomus pinnicaudatus. Soc Neurosci Abstr 29(828.16)Google Scholar
  51. 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 25:8746–8754PubMedCrossRefGoogle Scholar
  52. McAnelly L, Zakon HH (1996) Protein kinase A activation increases sodium current magnitude in the electric organ of Sternopygus. J Neurosci 16:4383–4388PubMedGoogle Scholar
  53. McAnelly ML, Zakon HH (2000) Coregulation of voltage-dependent kinetics of Na(+) and K(+) currents in electric organ. J Neurosci 20:3408–3414PubMedGoogle Scholar
  54. McAnelly L, Silva A, Zakon HH (2003) Cyclic AMP modulates electrical signaling in a weakly electric fish. J Comp Physiol A 189:273–282Google Scholar
  55. Meerlo P, van den Hoofdakker RH, Koolhaas JM, Daan S (1997) Stress-induced changes in circadian rhythms of body temperature and activity in rats are not caused by pacemaker changes. J Biol Rhythms 12:80–92PubMedCrossRefGoogle Scholar
  56. Meerlo P, Sgoifo A, Turek FW (2002) The effects of social defeat and other stressors on the expression of circadian rhythms. Stress 5:15–22PubMedCrossRefGoogle Scholar
  57. Meyer JH (1983) Steroid influences upon the discharge frequency of a weakly electric fish. J Comp Physiol 153A:29–37CrossRefGoogle Scholar
  58. Mills A, Zakon HH (1987) Coordination of EOD frequency and pulse duration in a weakly electric wave fish: the influence of androgens. J Comp Physiol 161:417–430CrossRefGoogle Scholar
  59. Mills A, Zakon HH (1991) Chronic androgen treatment increases action potential duration in the electric organ of Sternopygus. J Neurosci 11:2349–2361PubMedGoogle Scholar
  60. Monk TH, Kupfer DJ (2000) Circadian rhythms in healthy aging—effects downstream from the pacemaker. Chronobiol Int 17:355–368PubMedCrossRefGoogle Scholar
  61. Olman M (2001) Electrolocation abilities of males and females of the gymnotiform electric fish Brachyhypopomus pinnicaudatus. Honors Thesis, Florida International University, Miami, FLGoogle Scholar
  62. Panzer SE, Dodge AM, Kelly EA, Jarjour NN (2003) Circadian variation of sputum inflammatory cells in mild asthma. J Allergy Clin Immunol 111:308–312PubMedCrossRefGoogle Scholar
  63. Pigatto PD, Radaelli A, Tadini G, Polenghi MM, Brambilla L, Altomare G, Carandente F (1985) Circadian rhythm of the in vivo migration of neutrophils in psoriatic patients. Arch Dermatol Res 277:185–189PubMedCrossRefGoogle Scholar
  64. Reppert SM, Weaver DR (2001) Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 63:647–676PubMedCrossRefGoogle Scholar
  65. Richter CP (1967) Sleep and activity: their relation to the 24-hour clock. Res Publ Assoc Res Nerv Ment Dis 45:8–29PubMedGoogle Scholar
  66. Roberts JE (2000) Light and immunomodulation. Ann NY Acad Sci 917:435–445PubMedCrossRefGoogle Scholar
  67. 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 163:465–478PubMedCrossRefGoogle Scholar
  68. Silva A, Quintana L, Galeano M, Errandonea P, Macadar O (1999) Water temperature sensitivity of EOD waveform in Brachyhypopomus pinnicaudatus. J Comp Physiol A 185:187–197CrossRefGoogle Scholar
  69. Smith GT, Zakon HH (2000) Pharmacological characterization of ionic currents that regulate the pacemaker rhythm in a weakly electric fish. J Neurobiol 42:270–286PubMedCrossRefGoogle Scholar
  70. Smolensky MH, Reinberg AE, Martin RJ, Haus E (1999) Clinical chronobiology and chronotherapeutics with applications to asthma. Chronobiol Int 16:539–563PubMedCrossRefGoogle Scholar
  71. 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
  72. Stoddard PK (2002) Electric signals: predation, sex, and environmental constraints. Adv Stud Behav 31:201–242CrossRefGoogle Scholar
  73. Stoddard PK (2006) Plasticity of the electric organ discharge waveform: contexts, mechanisms, and implications for electrocommunication. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Fish communication. Science Publisher, Enfield, N.H. (in press)Google Scholar
  74. Stoddard PK, Rasnow B, Assad C (1999) Electric organ discharges of the gymnotiform fishes. III. Brachyhypopomus. J Comp Physiol A 184:609–630PubMedCrossRefGoogle Scholar
  75. Stoddard PK, Markham MR, Salazar VL (2003) Serotonin modulates the electric waveform of the gymnotiform electric fish Brachyhypopomus pinnicaudatus. J Exp Biol 206:1353–1362PubMedCrossRefGoogle Scholar
  76. Szabo T (1974) Anatomy of the specialized lateral line organs of electroreception. In: Fessard A (ed) Handbook of sensory physiology, vol III. Springer, Berlin Heidelberg New York, pp 13–58Google Scholar
  77. Yager DD, Hopkins CD (1993) Directional characteristics of tuberous electroreceptors in the weakly electric fish, Hypopomus (Gymnotiformes). J Comp Physiol A 173:401–414PubMedCrossRefGoogle Scholar
  78. Zhang W, Linden DJ (2003) The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4:885–900PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Philip K. Stoddard
    • 1
    Email author
  • Harold H. Zakon
    • 2
  • Michael R. Markham
    • 1
  • Lynne McAnelly
    • 2
  1. 1.Department of Biological Sciences Florida International UniversityMiamiUSA
  2. 2.Section of Neurobiology, Patterson LabsUniversity of Texas AustinAustinUSA

Personalised recommendations