Skip to main content
SpringerLink
Log in

Periodic firing pattern in afferent discharges from electroreceptor organs of catfish

  • Original Article
  • Neurophysiology, Muscle and Sensory Organs
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

Spontaneous afferent activity was recorded from 26 single ampullary electroreceptive organs of freshwater catfish (Ictalurus nebulosus LeS) at various temperatures. Regular grouping of action potentials was apparent in this secondary sensory system at 35°C and occasionally at 30°C. Impulse groups consisted of up to seven impulses. The precise timing of impulse generation and the temporal sequence of impulses indicated that oscillating processes are involved. Expectation density functions were calculated for records of afferent activity obtained at various temperatures below 35°C. In the majority of records the function was periodic. Impulse grouping and expectation density functions became more distinct in units exhibiting extremely high thresholds (i.e. being insensitive) to electrical stimuli. The results suggest that the oscillations originate from the postsynaptic membrane. The temporal pattern of impulse generation within impulse groups of ampullary electroreceptor organs and of specific warm and cold receptors was compared and found to be similar. Application of cadmium and menthol, which both reduce calcium entry, suppressed spontaneous activity in normal and insensitive electroreceptor systems, attenuated the sensitivity of normal receptors and modified the periodic pattern. This indicates that calcium is implicated in sensory transduction and in postsynaptic mechanisms. The data suggest that an oscillating process is one component of signal transmission in ampullary electroreceptor organs of teleost fish.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bennett MVL, Clusin WT (1979) Transduction at electroreceptors: origins of sensitivity. In: Cone RA, Dowling JE (eds) Membrane transduction mechanisms. Raven, New York, pp 91–121

    Google Scholar 

  2. Bennett MVL, Obara S (1986) Ionic mechanisms and pharmacology of electroreceptors. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 157–181

    Google Scholar 

  3. Braun HA, Bade H, Hensel H (1980) Static and dynamic discharge patterns of bursting cold fibres related to hypothetical receptor mechanisms. Pflügers Arch 386:1–9

    Google Scholar 

  4. Braun HA, Schäfer K, Wissing H (1990) Theories and models of temperature transduction. In: Bligh J, Voigt KH (eds) Thermoreception and temperature regulation. Springer, Berlin Heidelberg New York, pp 19–29

    Google Scholar 

  5. Braun HA, Wissing H, Schäfer K, Hirsch MC (1994) Oscillation and noise determine signal transduction in shark multimodal sensory cells. Nature 367:270–273

    Google Scholar 

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

    Google Scholar 

  7. Bretschneider F, Peters RC, Peele PH, Dorresteijn A (1980) Functioning of catfish electroreceptors: statistical distribution of sensitivity and fluctuations of spontaneous activity. J Comp Physiol 137:273–279

    Google Scholar 

  8. Bretschneider F, De Weille JR, Klis JFL (1985) Functioning of catfish electroreceptors: fractional-order filtering and nonlinearity. J Comp Physiol 80:191–198

    Google Scholar 

  9. Carbone E, Lux HD (1987) Kinetics and selectivity of a low-voltage-activated calcium current in chick and rat sensory neurones. J Physiol (Lond) 386:547–570

    Google Scholar 

  10. van Dongen AMJ, Bretschneider F (1984) Functioning of catfish electroreceptors: bursting discharge pattern of Kryptopterus electroreceptors elicited by microelectrode impalement. Comp Biochem Physiol [A] 77:647–650

    Google Scholar 

  11. Fox AP, Nowycky MC, Tsien RW (1987) Kinetic and pharmacological properties distinguishing three types of calcium current in chick sensory neurones. J Physiol (Lond) 394:149–172

    Google Scholar 

  12. Iggo A (1969) Cutaneous thermoreceptors in primates and subprimates. J Physiol (Lond) 200:403–430

    Google Scholar 

  13. Kalmijn AJ, Kolba CA, Kalmijn V (1976) Orientation of catfish (Ictalurus nebulosus) in strictly uniform electric fields: I. Sensitivity of response. Biol Bull (Woods Hole) 151:415

    Google Scholar 

  14. Obara S, Higuchi T (1980) High-gain synapse in the sensory transduction of the ampullary electroreceptors (abstract). J Physiol Soc Jpn 42:250

    Google Scholar 

  15. Peters RC, van Wijland F (1974) Electro-orientation in the passive electric catfish, Ictalurus nebulosus LeS. J Comp Physiol 92:273–281

    Google Scholar 

  16. Peters RC, Zwart R, Loos WJG, Bretschneider F (1989) Transduction at electroreceptor cells manipulated by exposure of apical membranes to ionic channel blockers. Comp Biochem Physiol [C] 94E: 663–669

    Google Scholar 

  17. Poggio GF, Viernstein LJ (1963) Time series analysis of impulse sequences of thalamic somatic sensory neurons. J Neurophysiol 27:517–545

    Google Scholar 

  18. Schäfer K, Braun HA (1990) Modulation of periodic cold receptor activity by ouabain. Pflügers Arch 417:91–99

    Google Scholar 

  19. Schäfer K, Braun HA, Hensel H (1984) Temperature transduction in the skin. In: Hales JRS (ed) Thermal physiology. Raven, New York, pp 1–11

    Google Scholar 

  20. Schäfer K, Braun HA, Isenberg C (1986) Effect of menthol on cold receptor activity. Analysis of receptor processes. J Gen Physiol 88:757–776

    Google Scholar 

  21. Schäfer K, Braun HA, Kürten L (1988) Analysis of cold and warm receptor activity in vampire bats and mice. Pflügers Arch 412:188–194

    Google Scholar 

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

    Google Scholar 

  23. Schäfer K, Braun HA, Rempe L (1991) Discharge pattern analysis suggests existence of a low-threshold calcium channel in cold receptors. Experientia 47:47–50

    Google Scholar 

  24. Sugawara Y (1989) Two Ca current components of the receptor current in the electroreceptors of the marine catfish Plotosus. J Gen Physiol 93:365–380

    Google Scholar 

  25. 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 

  26. Swandulla D, Carbone E, Schäfer K, Lux HD (1987) Effect of menthol on two types of Ca current in cultured sensory neurons of vertebrates. Pflügers Arch 409:52–59

    Google Scholar 

  27. Teunis PFM, Bretschneider F, Bedaux JJM, Peters RC (1991) Synaptic noise in spike trains of normal and denervated electroreceptor organs. Neuroscience 41:809–816

    Google Scholar 

  28. Teunis PFM, Bretschneider F, van Groeningen C, Peters RC, Bedaux JJM (1991) Quantitative aspects of transduction in an electroreceptor organ studied by means of experimental manipulation of the interspike interval. Neuroscience 42: 283–289

    Google Scholar 

  29. Wissing H, Braun HA, Schäfer K (1988) Dynamic response characteristics of the ampullae of Lorenzini to thermal and electrical stimuli. Prog Brain Res 74:99–107

    Google Scholar 

  30. Wissing H, König U, Hirsch M, Braun HA (1991) Quantification of oscillation parameters from neuronal impulse activity (abstract). Pflügers Arch 418:R42

    Google Scholar 

  31. Zakon HH (1986) The electroreceptive periphery. In: Bullock TH (ed) Electroreception. Wiley, New York, pp 103–156

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zentrum der Physiologie, Universität Frankfurt, Theodor-Stern-Kai 7, D-60590, Frankfurt, Germany

    K. Schäfer

  2. Institut für Physiologie, Universität Marburg, D-35037, Marburg, Germany

    H. A. Braun

  3. Laboratorium voor Vergelijkende Fysiologie, Universiteit Utrecht, NL-3584, Utrecht, CH, The Netherlands

    R. C. Peters & F. Bretschneider

Authors
  1. K. Schäfer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. A. Braun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. C. Peters
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Bretschneider
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schäfer, K., Braun, H.A., Peters, R.C. et al. Periodic firing pattern in afferent discharges from electroreceptor organs of catfish. Pflugers Arch. 429, 378–385 (1995). https://doi.org/10.1007/BF00374153

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00374153

Key words

Search

Navigation