Skip to main content
Log in

Electrophysiological control of ciliary motor responses in the ctenophorePleurobrachia

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

Summary

  1. 1.

    Prey capture by a tentacle of the ctenophorePleurobrachia elicits a reversal of beat direction and increase in beat frequency of comb plates in rows adjacent to the catching tentacle (Tamm and Moss 1985).

  2. 2.

    These ciliary motor responses were elicited in intact animals by repetitive electrical stimulation of a tentacle or the midsubtentacular body surface with a suction electrode.

  3. 3.

    An isolated split-comb row preparation allowed stable intracellular recording from comb plate cells during electrically stimulated motor responses of the comb plates, which were imaged by high-speed video microscopy.

  4. 4.

    During normal beating in the absence of electrical stimulation, comb plate cells showed no changes in the resting membrane potential, which was typically about − 60 mV.

  5. 5.

    Trains of electrical impulses (5/s, 5 ms duration, at 5–15 V) delivered by an extracellular suction electrode elicited summing facilitating synaptic potentials which gave rise to graded regenerative responses.

  6. 6.

    High K+ artificial seawater caused progressive depolarization of the polster cells which led to volleys of action potentials.

  7. 7.

    Current injection (depolarizing or release from hyperpolarizing current) also elicited regenerative responses; the rate of rise and the peak amplitude were graded with intensity of stimulus current beyond a threshold value of about −40 mV.

  8. 8.

    Increasing levels of subthreshold depolarization were correlated with increasing rates of beating in the normal direction.

  9. 9.

    Action potentials were accompanied by laydown (upward curvature of nonbeating plates), reversed beating at high frequency, and intermediate beat patterns.

  10. 10.

    TEA increased the summed depolarization elicited by pulse train stimulation, as well as the size and duration of the action potentials. TEA-enhanced single action potentials evoked a sudden arrest, laydown and brief bout of reversed beating.

  11. 11.

    Dual electrode impalements showed that cells in the same comb plate ridge experienced similar but not identical electrical activity, even though all of their cilia beat synchronously.

  12. 12.

    The large number of cells making up a comb plate, their highly asymmetric shape, and their complex innervation and electrical characteristics present interesting features of bioelectric control not found in other cilia.

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

Abbreviations

ss :

subsagittal

st :

subtentacular

ASW :

artificial seawater

TEA :

tetraethylammonium chloride

References

  • Afzelius BA (1961) The fine structure of the cilia from ctenophore swimming plates. J Biophys Biochem Cytol 9:383–394

    Google Scholar 

  • Bessen M, Fay RB, Witman GB (1980) Calcium control of waveform in isolated axonemes ofChlamydomonas. J Cell Biol 86:446–455

    Google Scholar 

  • Bone QA, Mackie GO (1982) Urochordata. In: Shelton GAB (ed) Electrical conduction and behavior in ‘simple’ invertebrates. Oxford, London New York, pp 473–535

    Google Scholar 

  • Brokaw CJ, Josslin R, Bobrow L (1974) Calcium ion regulation of flagellar beat symmetry in reactivated sea urchin spermatozoa. Biochem Biophys Res Commun 58(3):795–800

    Google Scholar 

  • Cavenaugh GM (1956) Formulae and methods VI of the Marine Biological Laboratory Chemical Room. Marine Biological Laboratory

  • Charleton MP, Smith SJ, Zucker RJ (1982) Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse. J Physiol 323:173–193

    Google Scholar 

  • DePeyer J, Machemer H (1977) Membrane excitability inStylonychia: properties of the two-peak regenerative Ca-response. J Comp Physiol 121:15–32

    Google Scholar 

  • DePeyer J, Machemer H (1978) Hyperpolarizing and depolarizing mechanoreceptor potentials inStylonychia. J Comp Physiol 127:255–266

    Google Scholar 

  • DePeyer J, Machemer H (1982a) Electromechanical coupling in cilia: I. Effects of depolarizing voltage steps. Cell Motility 2:483–496

    Google Scholar 

  • DePeyer J, Machemer H (1982b) Electromechanical coupling in cilia: II. Effects of hyperpolarizing voltage steps. Cell Motility 2:497–508

    Google Scholar 

  • DePeyer J, Machemer H (1983) Threshold activation and dynamic response range of cilia following low rates of membrane polarization under voltage-clamp. J Comp Physiol 150:223–232

    Google Scholar 

  • Deitmer J (1984) Evidence for two voltage-dependent calcium currents in the membrane of the ciliateStylonychia. J Physiol 355:137–159

    Google Scholar 

  • Dunlap K (1977) Localization of calcium channels inParamecium caudatum. J Physiol 271:119–133

    Google Scholar 

  • Eckert R (1972) Bioelectric control of ciliary activity. Science 176:473–481

    Google Scholar 

  • Eckert R, Machemer H (1975) Regulation of ciliary beating frequency by the surface membrane. In: Inoué S, Stephens R (eds) Molecules and cell movement. Raven, New York, pp 151–164

    Google Scholar 

  • Eckert R, Murakami A (1972) Calcium dependence of ciliary activity in the oviduct of the salamanderNecturus. J Physiol 226:699–711

    Google Scholar 

  • Gibbons BH, Gibbons IR (1980) Calcium-induced quiescence in reactivated sea urchin sperm. J Cell Biol 84:13–27

    Google Scholar 

  • Hernandez-Nicaise M-L (1973) Les système nerveux des Cténaires. I. Structure et ultrastructure des réseaux épitheliaux. Z Zellforsch 137:223–250

    Google Scholar 

  • Horridge GA (1965a) Relations between nerves and cilia in ctenophores. Am Zool 5:357–375

    Google Scholar 

  • Horridge GA (1965b) Intracellular action potentials associated with the beating of the cilia in ctenophore comb plate cells. Nature 205:602

    Google Scholar 

  • Horridge GA, Mackay B (1964) Neurociliary synapses inPleurobrachia (Ctenophora). Q J Microsc Sci 105:163–174

    Google Scholar 

  • Hyams JS, Borisy GG (1978) Isolated flagellar apparatus ofChlamydomonas: Characterization of forward swimming and alterations of waveform and reversal of motion by calcium ionsin vitro. J Cell Sci 33:235–253

    Google Scholar 

  • Kamiya R, Witman G (1984) Submicromolar levels of calcium control the balance of beating between the two flagella in demembranated models ofChlamydomonas. J Cell Biol 98:97–107

    Google Scholar 

  • Katz B, Miledi R (1968) The role of calcium in neuromuscular facilitation. J Physiol 195:481–492

    Google Scholar 

  • Machemer H (1974) Frequency and directional responses of cilia to membrane potential changes inParamecium. J Comp Physiol 92:293–316

    Google Scholar 

  • Machemer H (1975) Modification of ciliary activity by the rate of membrane potential changes inParamecium. J Comp Physiol 101:343–356

    Google Scholar 

  • Machemer H (1977) Motor activity and bioelectric control of cilia. Fortschr Zool 24:195–210

    Google Scholar 

  • Machemer H, Eckert R (1973) Electrophysiological control of reversed ciliary beating inParamecium. J Gen Physiol 61:572–587

    Google Scholar 

  • Machemer H, Eckert R (1975) Ciliary frequency and orientational responses to clamped voltage steps inParamecium. J Comp Physiol 104:247–260

    Google Scholar 

  • Machemer H, Machemer-Röhnisch S (1984) Mechanical and electric correlates of mechanoreceptor activation of the ciliated tail inParamecium. J Comp Physiol A 154:273–278

    Google Scholar 

  • Machemer H, Ogura A (1979) Ionic conductances of membranes in ciliated and deciliatedParamecium. J Physiol 296:49–60

    Google Scholar 

  • Machemer-Röhnisch S, Machemer H (1984) Receptor current following controlled stimulation of immobile tail cilia inParamecium caudatum. J Comp Physiol A 154:263–271

    Google Scholar 

  • Mackie GO, Paul DH, Singla CM, Sleigh MA, Williams DE (1974) Branchial innervation and ciliary control in the ascidianCorella. Proc R Soc Lond 187B:1–35

    Google Scholar 

  • Mackie GO, Singla CL, Thiriot-Quievreux C (1976) Nervous control of ciliary activity in gastropod larvae. Biol Bull 151:182–199

    Google Scholar 

  • Magleby KL, Zengel JA (1976) Long-term changes in augmentation, potentiation, and depression of transmitter release as a function of repeated synaptic activity at the frog neuromuscular junction. J Physiol 257:471–494

    Google Scholar 

  • Moss AG, Tamm SL (1981) Properties of the unilateral ciliary reversal response during prey capture byPleurobrachia (Ctenophora). Biol Bull 161:308a

    Google Scholar 

  • Moss AG, Tamm SL (1985) Action potential propagation along cilia of ctenophore comb plates. J Cell Biol 101:270a

    Google Scholar 

  • Murakami A (1983) Control of ciliary beat frequency inMytilus. J Submicrosc Cytol 15:313–316

    Google Scholar 

  • Murakami A, Eckert R (1972) Cilia: Activation coupled to mechanical stimulation by calcium influx. Science 175:1375–1377

    Google Scholar 

  • Murakami A, Machemer H (1982) Mechanoreception and signal transmission in the lateral ciliated cells on the gill ofMytilus. J Comp Physiol 145:351–362

    Google Scholar 

  • Murakami A, Takahashi K (1975) Correlation of electrical and mechanical responses in nervous control of cilia. Nature 257:48–49

    Google Scholar 

  • Naitoh Y (1982) Protozoa. In: Shelton GAB (ed) Electrical conduction and behavior in ‘simple’ invertebrates. Oxford London New York, pp 1–48

    Google Scholar 

  • Naitoh Y, Eckert R (1969) Ionic mechanisms controlling behavioral responses ofParamecium to mechanical stimulation. Science 164:963–965

    Google Scholar 

  • Naitoh Y, Eckert R, Friedman K (1972) A regenerative calcium response inParamecium. J Exp Biol 56:667–681

    Google Scholar 

  • Naitoh Y, Kaneko H (1972) Reactivated Triton-extracted models ofParamecium: Modification of ciliary movement by calcium ions. Science 176:523–524

    Google Scholar 

  • Naitoh Y, Kaneko H (1973) Control of ciliary activities by adenosine triphosphate and divalent cation in Triton-extracted models ofParamecium caudatum. J Exp Biol 58:657–676

    Google Scholar 

  • Nakamura S, Tamm SL (1985) Calcium control of ciliary reversal in ionophore-treated and ATP-reactivated comb plates of ctenophores. J Cell Biol 100:1447–1454

    Google Scholar 

  • Nakaoka Y, Tanaka H, Oosawa F (1984) Ca2+-dependent regulation of beat frequency of cilia inParamecium. J Cell Sci 65:223–231

    Google Scholar 

  • Ogura A, Takahashi K (1976) Artificial deciliation causes loss of calcium-dependent responses inParamecium. Nature 264:170–172

    Google Scholar 

  • Parker GH (1905) The movements of the swimming-plates in ctenophores, with reference to the theories of ciliary metachronism. J Exp Zool 2:407–423

    Google Scholar 

  • Saimi Y, Murakami A, Takahashi K (1983a) Electrophysiological correlates of nervous control of ciliary arrest response in the gill epithelial cells ofMytilus. Comp Biochem Physiol 74A:499–506

    Google Scholar 

  • Saimi Y, Murakami A, Takahashi K (1983b) Ciliary and electrical responses to intracellular current injection in the ciliated epithelium of the gill ofMytilus. Comp Biochem Physiol 74A:507–511

    Google Scholar 

  • Satterlie RA, Case JF (1978) Gap junctions suggest epithelial conduction within the comb plates of the ctenophorePleurobrachia bachei. Cell Tissue Res 193:87–91

    Google Scholar 

  • Sleigh MA, Barlow DI (1982) How are different ciliary beat patterns produced? In: Amos WB, Duckett JG (eds) Prokaryotic and eukaryotic flagella, Soc Exp Biol Symp 35, pp 139–157

  • Spray DC, Bennett MVL (1985) Physiology and pharmacology of gap junctions. Annu Rev Physiol 47:281–303

    Google Scholar 

  • Stommel EW (1984a) Calcium regenerative potentials inMytilus edulis gill abfrontal ciliated epithelial cells. J Comp Physiol A 155:445–456

    Google Scholar 

  • Stommel EW (1984b) Calcium activation of mussel gill abfrontal cilia. J Comp Physiol A 155:457–469

    Google Scholar 

  • Takahashi T, Baba SA, Murakami A (1973) The ‘excitable’ cilia of the tunicate,Ciona intestinalis. J Fac Sci Tokyo Univ IV 13:123–137

    Google Scholar 

  • Tamm SL (1973) Mechanisms of ciliary coordination in ctenophores. J Exp Biol 59:231–245

    Google Scholar 

  • Tamm SL (1982) Ctenophores. In: Shelton GAB (ed) Electrical conduction and behavior in ‘simple’ invertebrates, Oxford London New York, pp 266–358

  • Tamm SL (1983) Motility and mechanosensitivity of macrocilia in the ctenophoreBeroë. Nature 305:430–433

    Google Scholar 

  • Tamm SL (1984) Mechanical synchronization of ciliary beating within comb plates of ctenophores. J Exp Biol 113:401–408

    Google Scholar 

  • Tamm SL, Moss AG (1985) Unilateral ciliary reversal and motor responses during prey capture by the ctenophorePleurobrachia. J Exp Biol 114:443–461

    Google Scholar 

  • Tamm SL, Tamm S (1981) Ciliary reversal without rotation of axonemal structures in ctenophore comb plates. J Cell Biol 89:495–509

    Google Scholar 

  • Tsuchiya T (1977) Effects of calcium ion on Triton-extracted lamellibranch gill cilia: ciliary arrest response in a model system. Comp Biochem Physiol 56A:353–361

    Google Scholar 

  • Walter M, Satir P (1978) Calcium control of ciliary arrest in mussel gill cells. J Cell Biol 79:110–120

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Moss, A.G., Tamm, S.L. Electrophysiological control of ciliary motor responses in the ctenophorePleurobrachia . J. Comp. Physiol. 158, 311–330 (1986). https://doi.org/10.1007/BF00603615

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00603615

Keywords

Navigation