Journal of Comparative Physiology A

, Volume 158, Issue 3, pp 311–330 | Cite as

Electrophysiological control of ciliary motor responses in the ctenophorePleurobrachia

  • Anthony G. Moss
  • Sidney L. Tamm


  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.



Rest Membrane Potential Prey Capture Train Stimulation Beat Pattern Single Action Potential 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.







artificial seawater


tetraethylammonium chloride


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Afzelius BA (1961) The fine structure of the cilia from ctenophore swimming plates. J Biophys Biochem Cytol 9:383–394Google Scholar
  2. Bessen M, Fay RB, Witman GB (1980) Calcium control of waveform in isolated axonemes ofChlamydomonas. J Cell Biol 86:446–455Google Scholar
  3. Bone QA, Mackie GO (1982) Urochordata. In: Shelton GAB (ed) Electrical conduction and behavior in ‘simple’ invertebrates. Oxford, London New York, pp 473–535Google Scholar
  4. 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):795–800Google Scholar
  5. Cavenaugh GM (1956) Formulae and methods VI of the Marine Biological Laboratory Chemical Room. Marine Biological LaboratoryGoogle Scholar
  6. 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 323:173–193Google Scholar
  7. DePeyer J, Machemer H (1977) Membrane excitability inStylonychia: properties of the two-peak regenerative Ca-response. J Comp Physiol 121:15–32Google Scholar
  8. DePeyer J, Machemer H (1978) Hyperpolarizing and depolarizing mechanoreceptor potentials inStylonychia. J Comp Physiol 127:255–266Google Scholar
  9. DePeyer J, Machemer H (1982a) Electromechanical coupling in cilia: I. Effects of depolarizing voltage steps. Cell Motility 2:483–496Google Scholar
  10. DePeyer J, Machemer H (1982b) Electromechanical coupling in cilia: II. Effects of hyperpolarizing voltage steps. Cell Motility 2:497–508Google Scholar
  11. 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 150:223–232Google Scholar
  12. Deitmer J (1984) Evidence for two voltage-dependent calcium currents in the membrane of the ciliateStylonychia. J Physiol 355:137–159Google Scholar
  13. Dunlap K (1977) Localization of calcium channels inParamecium caudatum. J Physiol 271:119–133Google Scholar
  14. Eckert R (1972) Bioelectric control of ciliary activity. Science 176:473–481Google Scholar
  15. 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 151–164Google Scholar
  16. Eckert R, Murakami A (1972) Calcium dependence of ciliary activity in the oviduct of the salamanderNecturus. J Physiol 226:699–711Google Scholar
  17. Gibbons BH, Gibbons IR (1980) Calcium-induced quiescence in reactivated sea urchin sperm. J Cell Biol 84:13–27Google Scholar
  18. Hernandez-Nicaise M-L (1973) Les système nerveux des Cténaires. I. Structure et ultrastructure des réseaux épitheliaux. Z Zellforsch 137:223–250Google Scholar
  19. Horridge GA (1965a) Relations between nerves and cilia in ctenophores. Am Zool 5:357–375Google Scholar
  20. Horridge GA (1965b) Intracellular action potentials associated with the beating of the cilia in ctenophore comb plate cells. Nature 205:602Google Scholar
  21. Horridge GA, Mackay B (1964) Neurociliary synapses inPleurobrachia (Ctenophora). Q J Microsc Sci 105:163–174Google Scholar
  22. 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 33:235–253Google Scholar
  23. 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 98:97–107Google Scholar
  24. Katz B, Miledi R (1968) The role of calcium in neuromuscular facilitation. J Physiol 195:481–492Google Scholar
  25. Machemer H (1974) Frequency and directional responses of cilia to membrane potential changes inParamecium. J Comp Physiol 92:293–316Google Scholar
  26. Machemer H (1975) Modification of ciliary activity by the rate of membrane potential changes inParamecium. J Comp Physiol 101:343–356Google Scholar
  27. Machemer H (1977) Motor activity and bioelectric control of cilia. Fortschr Zool 24:195–210Google Scholar
  28. Machemer H, Eckert R (1973) Electrophysiological control of reversed ciliary beating inParamecium. J Gen Physiol 61:572–587Google Scholar
  29. Machemer H, Eckert R (1975) Ciliary frequency and orientational responses to clamped voltage steps inParamecium. J Comp Physiol 104:247–260Google Scholar
  30. Machemer H, Machemer-Röhnisch S (1984) Mechanical and electric correlates of mechanoreceptor activation of the ciliated tail inParamecium. J Comp Physiol A 154:273–278Google Scholar
  31. Machemer H, Ogura A (1979) Ionic conductances of membranes in ciliated and deciliatedParamecium. J Physiol 296:49–60Google Scholar
  32. Machemer-Röhnisch S, Machemer H (1984) Receptor current following controlled stimulation of immobile tail cilia inParamecium caudatum. J Comp Physiol A 154:263–271Google Scholar
  33. Mackie GO, Paul DH, Singla CM, Sleigh MA, Williams DE (1974) Branchial innervation and ciliary control in the ascidianCorella. Proc R Soc Lond 187B:1–35Google Scholar
  34. Mackie GO, Singla CL, Thiriot-Quievreux C (1976) Nervous control of ciliary activity in gastropod larvae. Biol Bull 151:182–199Google Scholar
  35. 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 257:471–494Google Scholar
  36. Moss AG, Tamm SL (1981) Properties of the unilateral ciliary reversal response during prey capture byPleurobrachia (Ctenophora). Biol Bull 161:308aGoogle Scholar
  37. Moss AG, Tamm SL (1985) Action potential propagation along cilia of ctenophore comb plates. J Cell Biol 101:270aGoogle Scholar
  38. Murakami A (1983) Control of ciliary beat frequency inMytilus. J Submicrosc Cytol 15:313–316Google Scholar
  39. Murakami A, Eckert R (1972) Cilia: Activation coupled to mechanical stimulation by calcium influx. Science 175:1375–1377Google Scholar
  40. Murakami A, Machemer H (1982) Mechanoreception and signal transmission in the lateral ciliated cells on the gill ofMytilus. J Comp Physiol 145:351–362Google Scholar
  41. Murakami A, Takahashi K (1975) Correlation of electrical and mechanical responses in nervous control of cilia. Nature 257:48–49Google Scholar
  42. Naitoh Y (1982) Protozoa. In: Shelton GAB (ed) Electrical conduction and behavior in ‘simple’ invertebrates. Oxford London New York, pp 1–48Google Scholar
  43. Naitoh Y, Eckert R (1969) Ionic mechanisms controlling behavioral responses ofParamecium to mechanical stimulation. Science 164:963–965Google Scholar
  44. Naitoh Y, Eckert R, Friedman K (1972) A regenerative calcium response inParamecium. J Exp Biol 56:667–681Google Scholar
  45. Naitoh Y, Kaneko H (1972) Reactivated Triton-extracted models ofParamecium: Modification of ciliary movement by calcium ions. Science 176:523–524Google Scholar
  46. Naitoh Y, Kaneko H (1973) Control of ciliary activities by adenosine triphosphate and divalent cation in Triton-extracted models ofParamecium caudatum. J Exp Biol 58:657–676Google Scholar
  47. Nakamura S, Tamm SL (1985) Calcium control of ciliary reversal in ionophore-treated and ATP-reactivated comb plates of ctenophores. J Cell Biol 100:1447–1454Google Scholar
  48. Nakaoka Y, Tanaka H, Oosawa F (1984) Ca2+-dependent regulation of beat frequency of cilia inParamecium. J Cell Sci 65:223–231Google Scholar
  49. Ogura A, Takahashi K (1976) Artificial deciliation causes loss of calcium-dependent responses inParamecium. Nature 264:170–172Google Scholar
  50. Parker GH (1905) The movements of the swimming-plates in ctenophores, with reference to the theories of ciliary metachronism. J Exp Zool 2:407–423Google Scholar
  51. 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:499–506Google Scholar
  52. 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:507–511Google Scholar
  53. Satterlie RA, Case JF (1978) Gap junctions suggest epithelial conduction within the comb plates of the ctenophorePleurobrachia bachei. Cell Tissue Res 193:87–91Google Scholar
  54. 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 139–157Google Scholar
  55. Spray DC, Bennett MVL (1985) Physiology and pharmacology of gap junctions. Annu Rev Physiol 47:281–303Google Scholar
  56. Stommel EW (1984a) Calcium regenerative potentials inMytilus edulis gill abfrontal ciliated epithelial cells. J Comp Physiol A 155:445–456Google Scholar
  57. Stommel EW (1984b) Calcium activation of mussel gill abfrontal cilia. J Comp Physiol A 155:457–469Google Scholar
  58. Takahashi T, Baba SA, Murakami A (1973) The ‘excitable’ cilia of the tunicate,Ciona intestinalis. J Fac Sci Tokyo Univ IV 13:123–137Google Scholar
  59. Tamm SL (1973) Mechanisms of ciliary coordination in ctenophores. J Exp Biol 59:231–245Google Scholar
  60. Tamm SL (1982) Ctenophores. In: Shelton GAB (ed) Electrical conduction and behavior in ‘simple’ invertebrates, Oxford London New York, pp 266–358Google Scholar
  61. Tamm SL (1983) Motility and mechanosensitivity of macrocilia in the ctenophoreBeroë. Nature 305:430–433Google Scholar
  62. Tamm SL (1984) Mechanical synchronization of ciliary beating within comb plates of ctenophores. J Exp Biol 113:401–408Google Scholar
  63. Tamm SL, Moss AG (1985) Unilateral ciliary reversal and motor responses during prey capture by the ctenophorePleurobrachia. J Exp Biol 114:443–461Google Scholar
  64. Tamm SL, Tamm S (1981) Ciliary reversal without rotation of axonemal structures in ctenophore comb plates. J Cell Biol 89:495–509Google Scholar
  65. Tsuchiya T (1977) Effects of calcium ion on Triton-extracted lamellibranch gill cilia: ciliary arrest response in a model system. Comp Biochem Physiol 56A:353–361Google Scholar
  66. Walter M, Satir P (1978) Calcium control of ciliary arrest in mussel gill cells. J Cell Biol 79:110–120Google Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • Anthony G. Moss
    • 1
  • Sidney L. Tamm
    • 1
  1. 1.Marine Biological LaboratoryBoston University Marine ProgramWoods HoleUSA

Personalised recommendations