The sequence of ciliary responses inParamecium to shifts in membrane potential is rate-dependent. With depolarizations exceeding the rate of 40mV · sec−1 the cilia switch directly from normal to reversed beating, thereby rapidly increasing their frequency. If the membrane is depolarized at the rate of 40 mV · sec−1 or less, unabbreviated ciliary responses occur with the sequence: reduction in normal beating → inactivation → increase in reversed beating. This “typical”, since potential-correlated, sequence is at least 50 times slower than the preceding electric membrane response. A time-dependent hysteresis of current versus voltage during depolarizing and hyperpolarizing slow voltage ramps suggests membrane accommodation mechanisms. A slow inactivation of inward calcium current during depolarization and a slow decrease in Ca-conductance during hyperpolarization is suggested from a hysteresis of the frequency response versus voltage. Differences in local ciliary responses to slow voltage ramps are interpreted as generated by modified local Ca-conductances. It is concluded that the graded frequency and directional responses of the cilia are correlated with the time-course of calcium accumulation and depletion within the cilium.
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Adrian, R. H., Chandler, W. K., Hodgkin, A. L.: Slow changes in potassium permeability in skeletal muscle. J. Physiol. (Lond.)208, 645–668 (1970)
Eckert, R.: Bioelectric control of ciliary activity. Science176, 473–481 (1972)
Eckert, R., Lux, H. D.: A non-inactivating inward current recorded during small depolarizing voltage steps in snail neurons. Brain Res.83, 486–489 (1975)
Eckert, R., Machemer, H.: Regulation of ciliary beating frequency by the surface membrane. In: Symp. Soc. Gen. Physiol. (R. Stephens, S. Inoué, eds.). New York: Raven Press, 1975a (in press)
Eckert, R., Machemer, H.: Regulation of ciliary frequency and orientation by the cell membrane inParamecium. Analysis with clamped voltage steps. (subm.) (1975b)
Eckert, R., Naitoh, Y.: Graded calcium spikes inParamecium. 3rd Intl. Biophys. Congr. Int. Union Pure and Applied Biophys., Cambridge, Mass., Abstr., p. 257 (1969)
Eckert, R., Naitoh, Y.: Passive electric properties ofParamecium and problems of ciliary coordination. J. gen. Physiol.55, 467–483 (1970)
Epstein, M., Eckert, R.: Membrane control of ciliary activity in the protozoanEuplotes. J. exp. Biol.58, 437–462 (1973)
Grabowski, W., Lobsiger, E. A., Lüttgau, H. C.: The effect of repetitive stimulation at low frequencies upon the electrical and mechanical activity of single muscle fibres. Pflügers Arch.334, 222–239 (1972)
Katz, B., Miledi, R.: Tetrodotoxin-resistant electric activity in presynaptic terminals. J. Physiol. (Lond.)203, 459–487 (1969)
Kinosita, H., Dryl, S., Naitoh, Y.: Changes in the membrane potential and the response to stimuli inParamecium. J. Fac. Sci. Tokyo Univ. IV,10, 291–301 (1964a)
Kinosita, H., Dryl, S., Naitoh, Y.: Relation between the magnitude of membrane potential and ciliary activity inParamecium. J. Fac. Sci. Tokyo Univ. IV,10, 303–309 (1964b)
Krnjević, K., Lisiewicz, A.: Injections of calcium ions into spinal motoneurones. J. Physiol. (Lond.)225, 363–390 (1972)
Lew, V. L.: Effect of intracellular calcium on the potassium permeability of human red cells. J. Physiol. (Lond.)206, 35–36P (1970)
Machemer, H.: Korrelation zwischen Membranpotential und Fortbewegung beiStylonychia. Naturwissenschaften57, 398–399 (1970)
Machemer, H.: Ciliary activity and the origin of metachrony inParamecium: Effects of increased viscosity. J. exp. Biol.57, 239–259 (1972a)
Machemer, H.: Temperature influences on ciliary beat and metachronal coordination inParamecium. J. Mechanochem. Cell Motility1, 57–66 (1972b)
Machemer, H.: Frequency and directional responses of cilia to membrane potential changes inParamecium. J. comp. Physiol.92, 293–316 (1974)
Machemer, H.: Interactions of membrane potential and cations in regulation of ciliary activity inParamecium. (subm.) (1975)
Machemer, H., Eckert, R.: Electrophysiological control of reversed ciliary beating inParamecium. J. gen. Physiol.61, 572–587 (1973)
Meech, R. W., Strumwasser, F.: Intracellular calcium injection activates potassium conductance inAplysia nerve cells. Fed. Proc.29, 834 (1970)
Naitoh, Y.: Direct current stimulation ofOpalina with intracellular microelectrode. Annot. Zool. Japon.31, 59–73 (1958)
Naitoh, Y.: Reversal response elicited in nonbeating cilia ofParamecium by membrane depolarization. Science154, 660–662 (1966)
Naitoh, Y., Eckert, R.: Ionic mechanisms controlling behavioral responses ofParamecium to mechanical stimulation. Science164, 963–965 (1969)
Naitoh, Y., Eckert, R.: Electrophysiology of the ciliate protozoa. In: Experiments in physiology and biochemistry, vol. V, p. 17–31 (G. A. Kerkut, ed.). New York-London: Academic Press 1972
Naitoh, Y., Eckert, R., Friedman, K.: A regenerative calcium response inParamecium. J. exp. Biol.56, 667–681 (1972)
Naitoh, Y., Kaneko, H.: ATP-Mg-reactivated Triton-extracted models ofParamecium: Modification of ciliary movement by calcium ions. Science176, 523–524 (1972)
Romero, P. J., Whittam, R.: The control by internal calcium of membrane permeability to sodium and potassium. J. Physiol. (Lond.)214, 481–507 (1971)
Trautwein, W.: Membrane currents in cardiac muscle fibres. Physiol. Rev.53, 793–825 (1973)
Whittam, R.: Control of membrane permeability to potassium in red blood cells. Nature (Lond.)219, 610–611 (1968)
Dedicated to Professor Bernhard Rensch on the occasion of his seventyfifth birthday.
The experiments were done in the laboratory of Dr. Roger Eckert, Department of Biology, University of California at Los Angeles. I am grateful to Dr. Eckert and to his collaborator, Dr. Yutaka Naitoh, for practical help and many inspiring discussions. I would like to thank Dr. Naitoh for permission to cite an unpublished result, and Dr. Eckert and Dr. Ulrich Thurm, Münster, for their critical reading of the manuscript.
The experiments were supported by the NSF grant GB-30499, USPHS grant NS-05670 and a grant from the Deutsche Forschungsgemeinschaft.
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Machemer, H. Modification of ciliary activity by the rate of membrane potential changes inParamecium . J. Comp. Physiol. 101, 343–356 (1975). https://doi.org/10.1007/BF00657050
- Membrane Potential
- Frequency Response
- Potential Change
- Directional Response