Skip to main content
Log in

Microvilli in electroreceptor organs in Ictalurus nebulosus play a part in signal filtering

  • Original Papers
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Ampullary electroreceptor organs of catfish show a band-pass-filter characteristic on sinusoidal electric stimulation. The structures and processes which are responsible for the frequency characteristics are not fully understood. To investigate the role of the apical membrane and its microvilli in signal filtering, the ampullary organs were apically exposed to the actin filament disrupting agent cytochalasin B. Electrophysiological data showed that cytochalasin B treatment reduced the absolute sensitivity to about 20% over the whole frequency range. The decrease in sensitivity at 20 Hz, however, was less than at other frequencies. The phase lags at 14 and 20 Hz became less negative, indicating a relatively better transduction at high frequencies. Calculations with an electric equivalent circuit of an electroreceptor cell indicated that a reduction in apical surface area in combination with a reduction of the number or the conductivity of apical ion channels can explain such effects. We conclude that, although only the basal membrane is thought to be involved in stimulus transduction, the apical membrane contributes considerably to the frequency characteristics of ampullary electroreceptor organs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bennett MVL (1971) Electroreception. In: Hoar WS, Randall DS (eds) Fish physiology. Academic Press, New York, pp 493–574

    Google Scholar 

  • Bennett MVL, Clusin WT (1979) Transduction at electroreceptors: origins of sensitivity. In: Cone RA, Dowling EJ (eds) Membrane transduction mechanisms. Raven Press, New York, pp 91–116

    Google Scholar 

  • Bretschneider F, Peters RC (1992) Transduction and transmission in ampullary electroreceptors of catfish. Comp Biochem Physiol 103A(2):245–252

    Google Scholar 

  • Bretschneider F, Kroesbergen G, Beijnink FB (1979) Functioning of catfish electroreceptors: relation between skin potential and receptor activity. J Physiol (Paris) 75:343–347

    Google Scholar 

  • Bretschneider F, de Weille JR, Klis JFL (1985) Functioning of catfish electroreceptors: Fractional-order filtering and non-linearity. Comp Biochem Physiol 80A(2):191–198

    Google Scholar 

  • Bretschneider F, Verwey J, Heuts P (1991) Functioning of catfish electroreceptors: input impedance and stimulus efficiency. Comp Biochem Physiol 99A(3):295–299

    Google Scholar 

  • Cantiello HF, Stow JL, Prat AG, Ausiello A (1991) Actin filaments regulate epithelial Na+ channel activity. Am J Physiol 261:C882-C888

    Google Scholar 

  • Cooper JA (1987) Effects of cytochalasin and phalloidin on actin. J Cell Biol 105:1473–1478

    Google Scholar 

  • Els WJ, Chou K (1993) Sodium-dependent regulation of epithelial sodium channel densities in frog skin; a role for the cytskeleton. J Physiol (Lond) 462:447–464

    Google Scholar 

  • Heijmen PS, Peters RC (1994) Apically administered cytochalasin B and D decreases sensitivity of electroreceptor organs in the North-American catfish, Ictalurus nebulosus. J Comp Physiol A 175:279–287

    Google Scholar 

  • Johnson BD, Byerly L (1993) A cytoskeletal mechanism for Ca2+ channel dependence and inactivation by intracellular Ca2+. Neuron 10:797–804

    Google Scholar 

  • MacLean-Fletcher S, Pollard TD (1980) Mechanism of action of cytochalasin B on actin. Cell 20:329–341

    Google Scholar 

  • Mullinger AM (1964) The fine structure of ampullary electric receptors in Amiurus. Proc R Soc Lond B 160:345–359

    Google Scholar 

  • Nilsson M, Moine J, Ericson LE (1991) Integrity of the occluding barrier in high-resistant thyroid follicular epithelium in culture. II. Immediate protective effect of TSH on paracellular leakage induced by CA2+ removal and cytochalasin B. Eur J Cell Biol 56:308–318

    Google Scholar 

  • Peters RC, Teunis PFM, Bretschneider F, Weerden R van (1988) Ampullary electroreceptors in neurophysiological instruction. J Biol Educ 22(1):61–66

    Google Scholar 

  • Schäfer K, Braun HA, Bretschneider F, Teunis PFM, Peters RC (1990) Ampullary electroreceptors in catfish (Teleostei): temperature dependence of stimulus transduction. Pflügers Arch 417:100–105

    Google Scholar 

  • Roth A (1978) Further indications of a chemical synapse in the electroreceptors of the catfish. J Comp Physiol 126:147–150

    Google Scholar 

  • Sugawara Y, Obara S (1989) Receptor Ca current and Ca-gated K current in tonic electroreceptors of the marine catfish Plotosus. J Gen Physiol 93:343–364

    Google Scholar 

  • Suzuki M, Miyazaki K, Ikeda M, Kawaguchi Y, Sakai O (1993) Factin network may regulate a Cl channel in renal proximal tubule cells. J Membrane Biol 134:31–39

    Google Scholar 

  • Teeter JH, Bennett MVL (1981) Synaptic transmission in the ampullary electroreceptor of the transparent catfish, Kryptopterus. J Comp Physiol 142:371–377

    Google Scholar 

  • Teunis PMF, Bretschneider F, Peters RC (1990) Synaptic latency in denervated electroreceptor organs. Comp Biochem Physiol 97A(3):399–403

    Google Scholar 

  • Urbanik E, Ware BR (1989) Actin filament capping and cleaving activity of cytochalasins B, D, E, and H. Arch Biochem Biophys 269(1):181–187

    Google Scholar 

  • Watson GM, Hessinger DA (1991) Chemoreceptor-mediated elongation of stereocilium bundles tunes vibration-sensitive mechanoreceptors on cnidocyte-supporting cell complexes to lower frequencies. J Cell Sci 99:307–316

    Google Scholar 

  • Zakon HH (1986) The electroreceptive periphery. In: Bullock TH, Heiligenberg W (eds) Electroreception. John Wiley and Sons, New York, pp 103–156

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heijmen, P.S., Braks, M.A.H., Bretschneider, F. et al. Microvilli in electroreceptor organs in Ictalurus nebulosus play a part in signal filtering. J Comp Physiol A 176, 103–109 (1995). https://doi.org/10.1007/BF00197756

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00197756

Key words

Navigation