Skip to main content
Log in

Ionic currents in secondary sensory hair cells isolated from the statocysts of squid and cuttlefish

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

Abstract

Mechanosensitive hair cells in the statocysts of cephalopods underlie a sophisticated detection system for linear and angular accelerations. To investigate the operation of this system, secondary sensory hair cells were dissociated from the sensory epithelia of these statocysts and their voltage sensitive ionic conductances identified and characterized under whole cell voltage clamp.

All secondary hair cells showed two outward potassium conductances; first, a current similar to the previously described delayed rectifier, IK and second, a current similar to the molluscan A current, IA. A small number of hair cells (15%) also showed an inward sodium current; the presence of this current was correlated with the presence of small membrane extensions at the base of the cell. The sodium current could be blocked by TTX and was abolished by substituting choline for sodium in the external medium. An inward L-type, calcium current was also identified. This current showed rapid activation, with little inactivation, could be carried by barium ions, and was blocked by Nifedipine in the external solution.

These data provide the first information on the ionic conductances in the basolateral membranes of invertebrate secondary sensory hair cells and form a basis for comparison with analogous vertebrate hair cells.

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

  • Armstrong CM, Gilly WF (1992) Access resistance and space clamp problems associated with whole-cell patch clamping. Meths Enzymol 207: 100–122

    Google Scholar 

  • Art JJ, Fettiplace R (1987) Variation of membrane properties in hair cells isolated from the turtle cochlea. J Physiol (Lond) 385: 207–242

    Google Scholar 

  • Barber VC (1968) The structure of molluscan statocysts, with particular reference to cephalopods. Symp Zool Soc Lond 23: 37–62

    Google Scholar 

  • Budelmann BU (1977) Structure and function of the angular acceleration receptor systems in the statocysts of cephalopods. Symp Zool Soc Lond 38: 309–324

    Google Scholar 

  • Budelmann BU (1987) Morphological diversity of equilibrium receptor systems in aquatic invertebrates. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 757–782

    Google Scholar 

  • Budelmann BU (1990) The statocysts of squid. In: Gilbert DL, Adelman WJ, Arnold JM (eds) Squid as experimental animals. Plenum, New York, pp 421–439

    Google Scholar 

  • Budelmann BU, Williamson R (1994) Directional sensitivity of hair cell afferents in the Octopus statocyst. J Exp Biol 187: 245–259

    Google Scholar 

  • Budelmann BU, Barber VC, West S (1973) Scanning electron microscopical studies of the arrangements and numbers of hair cells in the statocysts of Octopus vulgaris, Sepia officinalis and Loligo vulgaris. Brain Res 56: 25–41

    Google Scholar 

  • Budelmann BU, Sachse M, Staudigl M (1987) The angular acceleration receptor system of the statocyst of Octopus vulgaris: morphometry, ultrastructure, and neuronal and synaptic organization. Phil Trans R Soc Lond B 315: 305–343

    Google Scholar 

  • Cole KS, Moore JW (1960) Ionic current measurements in the squid giant axon membrane. J Gen Physiol 44: 123–167

    Google Scholar 

  • Colmers WF (1981) Afferent synaptic connections between hair cells and the somata of intramacular neurons in the gravity receptor system of the statocyst of Octopus vulgaris. J Comp Neurol 197: 385–394

    Google Scholar 

  • Connor JA, Stevens CF (1971) Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol 213: 21–30

    Google Scholar 

  • Evans MG, Fuchs PA (1987) Tetrodotoxin-sensitive, voltage dependent sodium currents in hair cells from the alligator cochlea. Biophys J 52: 649–652

    Google Scholar 

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

    Google Scholar 

  • Fuchs PA (1992) Ionic currents in cochlear hair cells. Prog Neurobiol 39: 493–505

    Google Scholar 

  • Fuchs PA, Evans MG, Murrow BW (1990) Calcium currents in hair cells isolated from the cochlea of the chick. J Physiol (Lond) 429: 553–568

    Google Scholar 

  • Griguer C, Kros CJ, Sans A, Lehoueller J (1993) Potassium currents in type II vestibular hair cells isolated from the guinea-pig's crista ampullaris. Pflügers Arch 425: 344–352

    Google Scholar 

  • Hagiwari AS, Byerly L (1981) Calcium channel. An Rev Neurosci 4: 69–125

    Google Scholar 

  • Hille B (1992) Ionic channels of excitable membranes. Sinauer Sunderland

  • Housley GD, Norris CH, Guth PS (1989) Electrophysiological properties and morphology of hair cells isolated from the semicircular canal of the frog. Hearing Res. 38: 259–276

    Google Scholar 

  • Hudspeth AJ, Jacobs R (1979) Stereocilia mediate transduction in vertebrate hair cells. Proc Natl Acad Sci USA 76: 1506–1509

    Google Scholar 

  • Hudspeth AJ, Lewis RS (1988) Kinetic analysis of voltage and ion dependent conductances in saccular hair cells of the bull-frog Rana catesbeiana. J Physiol (Lond) 400: 237–274

    Google Scholar 

  • Klein K (1932) Die Nervenendigungen in der Statocyste von Sepia. Z Zellforsch Mikrosk Anat 14: 418–516

    Google Scholar 

  • Kostyuk PG, Krishtal OA (1977) Separation of sodium and calcium currents in the somatic membrane of molluscan neurones. J Physiol (Lond) 270: 545–568

    Google Scholar 

  • Lang DG, Correia MJ (1989) Studies of solitary semicircular canal hair cells in the adult pigeon. II Voltage-dependent ionic conductances. J Neurophysiol 62: 935–945

    Google Scholar 

  • Llano I, Bookman RJ (1986) Ionic conductances of squid giant fibre lobe neurons. J Gen Physiol 88: 543–569

    Google Scholar 

  • Lucero MT, Korrigan FT, Gilly Wm F (1992) Electrical responses to chemical stimulation of squid olfactory receptor cells. J Exp Biol 162: 231–249

    Google Scholar 

  • Masetto S, Russo G, Prigioni A (1994) Differential expression of potassium currents by hair cells in thin slices of frog crista ampullaris. J Neurophysiol 72: 443–455

    Google Scholar 

  • Murrow BW, Fuchs PA (1990) Preferential expression of transient potassium current IA by “short” hair cells of the chick's cochlea. Proc R Soc Lond B 242: 189–195

    Google Scholar 

  • Norris CH, Ricci AJ, Housley GD, Guth PS (1992) The inactivating potassium currents of hair cells isolated from the crista ampullaris of the frog. J Neurophysiol 68: 1642–1653

    Google Scholar 

  • Ohmori H (1984) Studies of ionic currents in the isolated vestibular hair cell of the chick. J Physiol (Lond) 350: 561–581

    Google Scholar 

  • Pickles JO, Corey DP (1992) Mechanoelectric transduction by hair cells. Trends Neurosci 15: 254–259

    Google Scholar 

  • Rennie KJ, Ashmore JF (1991) Ionic currents in isolated vestibular hair cells from the guinea-pig crista ampullaris. Hearing Res 51: 279–292

    Google Scholar 

  • Rudy B (1988) Diversity and ubiquity of K channels. Neuroscience 25: 729–749

    Google Scholar 

  • Steinacker A, Romero A (1991) Characterization of voltage-gated and calcium-activated potassium currents in toadfish saccular hair cells. Brain Res 556: 22–32

    Google Scholar 

  • Stockbridge LL, French AS, Sanders EJ (1990) Dissociation and culture of mechanosensory neurons for patch clamp analysis. Brain Res 523: 161–166

    Google Scholar 

  • Stommel EW, Stephens RE, Alkon DL (1980) Motile statocyst cilia transmit rather than directly transduce mechanical stimuli. J Cell Biol 87: 652–662

    Google Scholar 

  • Sugihara I, Furukawa T (1989) Morphological and functional aspects of two different types of hair cells in the goldfish sacculus. J Neurophysiol 62: 1330–1343

    Google Scholar 

  • Williamson R (1989a) Electrical coupling between secondary hair cells in the statocyst of the squid Alloteuthis subulata. Brain Res 486: 67–72

    Google Scholar 

  • Williamson R (1989b) Secondary hair cells and afferent neurones of the squid statocyst receive both inhibitory and excitatory efferent inputs. J Comp Physion A 165: 847–860

    Google Scholar 

  • Williamson R (1989c) Electrophysiological evidence for cholinergic and catecholaminergic efferent transmitters in the statocyst of Octopus. Comp Biochem Physiol 93C: 23–27

    Google Scholar 

  • Williamson R (1990) The responses of primary and secondary sensory hair cells in the squid statocyst to mechanical stimulation. J Comp Physiol A 167: 655–664

    Google Scholar 

  • Williamson R (1991) The responses of the sensory hair cells in the statocyst of Sepia In: Boucaud-Camou E (ed) The cuttlefish Univ Caen Publ, pp 211–221

  • Williamson R, Budelmann BU (1985) The response of the Octopus angular acceleration receptor system to sinusoidal stimulation. J Comp Physiol A 156: 403–412

    Google Scholar 

  • Williamson R, Chrachri A (1994) The efferent system in cephalopod statocysts. Biomed Res 15: 51–56, Suppl 1

    Google Scholar 

  • Young JZ (1960) The statocysts of Octopus vulgaris. Proc R Soc Lond B 162: 3–29

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Williamson, R. Ionic currents in secondary sensory hair cells isolated from the statocysts of squid and cuttlefish. J Comp Physiol A 177, 261–271 (1995). https://doi.org/10.1007/BF00192416

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00192416

Key words

Navigation