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The responses of primary and secondary sensory hair cells in the squid statocyst to mechanical stimulation

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Summary

Intracellular recordings were obtained from primary and secondary sensory hair cells in the anterior transverse crista segment of the squid (Alloteuthis subulata) statocyst during imposed displacements of the overlying cupula. The secondary sensory hair cells were depolarized by ventral movements of the cupula and hyperpolarized by dorsal cupula movements. The displacement/response curve was asymmetric around the zero position and sigmoidal in shape, similar to that already described for vertebrate hair cells. The cells are estimated to have a sensitivity of at least 0.5 mV per degree angle of cilia displacement. The responses showed pronounced adaptation and could be blocked by bath applied alcohols, such as heptanol or octanol, or by high concentrations of aminoglycosides.

The primary sensory hair cells were depolarized by dorsal movements of the cupula, usually responding with a burst of action potentials. The displacement/response curve was also sigmoidal in shape and the firing pattern showed strong adaptation to maintained displacements of the cupula.

The cupula itself appeared to be irregular in shape, extending much further into the statocyst cavity in its central part than at its edges. This is likely to result in differences in the responses of the underlying hair cells along the length of the crista ridge.

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References

  • Alkon DL (1975) Responses of hair cells to statocyst rotation. J Gen Physiol 66:507–530

    Google Scholar 

  • Alkon DL, Bak A (1973) Hair cell generator potentials. J Gen Physiol 61:619–637

    Google Scholar 

  • Armstrong CM, Binstock L (1964) The effects of several alcohols on the properties of the squid giant axon. J Gen Physiol 48:265–278

    Google Scholar 

  • Blaxter JHS, Fuiman LA (1989) Function of the free neuromasts of marine teleost larvae. In: Coombs S, Görner P, Münz H (eds) The mechanosensory lateral line. Springer, Berlin Heidelberg New York, pp 481–500

    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 (1979) Hair cell polarization in the gravity receptor systems of the statocysts of the cephalopods Sepia officinalis and Loligo vulgaris. Brain Res 160:261–270

    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, Berlin Heidelberg New York, pp 757–782

    Google Scholar 

  • Budelmann BU, Thies G (1977) Secondary receptor cells in the gravity receptor system of the statocyst of Octopus vulgaris. Cell Tissue Res 182:93–98

    Google Scholar 

  • Budelmann BU, Wolff HG (1973) Gravity response from angular acceleration receptors in Octopus vulgaris. J Comp Physiol 85:283–290

    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 

  • Corey DP, Hudspeth AJ (1980) Mechanical stimulation and micro-manipulation with piezoelectric bimorph elements. J Neurosci Meths 3:183–202

    Google Scholar 

  • Crawford AC, Fettiplace R (1985) The mechanical properties of ciliary bundles of turtle cochlear hair cells. J Physiol Lond 364:359–380

    Google Scholar 

  • Dickman JD, Correia MJ (1989) Response of pigeon horizontal semicircular canal afferent fibres I. Step, trapezoid, and low-frequency sinusoid mechanical and rotational stimulation. J Neurophysiol 62:1090–1101

    Google Scholar 

  • Eatock RA, Corey DP, Hudspeth AJ (1987) Adaptation of mechanoelectric transduction in hair cells of the bullfrog's sacculus. J Neurosci 7:2821–2836

    Google Scholar 

  • Flock Å (1971) Sensory transduction in hair cells. In: Loewenstein WR (ed) Principles of receptor physiology (Handbook of sensory physiology, vol. 1). Springer, Berlin Heidelberg New York, pp 396–441

    Google Scholar 

  • Flock Å, Wersäll J (1962) A study of the orientation of the sensory hairs of the receptor cells in the lateral line organ of fish, with special reference to the function of the receptors. J Cell Biol 15:19–27

    Google Scholar 

  • French AS (1989) Two components of rapid sensory adaptation in a cockroach mechanoreceptor neuron. J Neurophysiol 62:768–777

    Google Scholar 

  • Harris GG (1968) Brownian motion in the cochlear partition. J Acoust Soc Am 44:176–186

    Google Scholar 

  • Haydon DA, Urban BW (1983) The action of alcohols and other non-ionic surface active substances on the sodium current of the squid giant axon. J Physiol Lond 341:411–427

    Google Scholar 

  • Hodgkin AL, Katz B (1949) The effect of sodium ions on the electrical activity of the giant axon of the squid. J Physiol Lond 108:37–77

    Google Scholar 

  • Holton T, Hudspeth AJ (1986) The transduction channel of hair cells from the bull-frog characterized by noise analysis. J Physiol Lond 375:195–227

    Google Scholar 

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

    Google Scholar 

  • Howard J, Hudspeth AJ (1988) Compliance of the hair bundle associated with gating of mechanoelectric transduction channels in the bullfrog's saccular hair cells. Neuron 1:189–199

    Google Scholar 

  • Hudspeth AJ (1989) How the ear's ear works. Science 341:397–404

    Google Scholar 

  • Hudspeth AJ, Corey DP (1977) Sensitivity, polarity and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. Proc Natl Acad Sci USA 74:2407–2411

    Google Scholar 

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

    Google Scholar 

  • Janse C (1983) The function of the statocyst sensory cells in Aplysia limacina. J Comp Physiol 150:359–370

    Google Scholar 

  • Kroese ABA, Bercken van den (1982) Effects of ototoxic antibiotics on sensory hair cell functioning. Hearing Res 6:183–197

    Google Scholar 

  • Kroese ABA, Netten van SM (1989) Sensory transduction in lateral line hair cells. In: Coombs S, Görner P, Münz H (eds) The mechanosensory lateral line. Springer, Berlin Heidelberg New York, pp 265–284

    Google Scholar 

  • Kroese ABA, Das A, Hudspeth AJ (1989) Blockage of the transduction channels of hair cells in the bullfrog's sacculus by aminoglycoside antibiotics. Hearing Res 37:203–218

    Google Scholar 

  • Mechmann S, Pott L (1989) Inhibition of a large-conductance ion channel in guinea-pig cardiac myocytes by octanol. J Physiol Lond 417:157P

    Google Scholar 

  • Mellon D Jr (1968) The physiology of sense organs. Oliver and Boyde, London

    Google Scholar 

  • Moore JW, Ulbricht W, Takata M (1964) Effects of ethanol on the sodium and potassium conductances of the squid axon membrane. J Gen Physiol 48:279–295

    Google Scholar 

  • Münz H (1985) Single unit activity in the peripheral lateral line of the cichlid fish Sarotherodon niloticus. J Comp Physiol A 157:555–568

    Google Scholar 

  • Narins PM, Lewis ER (1984) The vertebrate ear as an exquisite seismic sensor. J Acoust Soc Am 76:1384–1387

    Google Scholar 

  • Ohmori H (1989) Mechano-electric transduction of the hair cell. Jpn J Physiol 39:643–657

    Google Scholar 

  • Ottoson D, Shepherd GM (1965) Receptor potentials and impulse generation in the isolated spindle during controlled extension. Cold Spring Harbor Symp Quant Biol 30:105–114

    Google Scholar 

  • Pocock G, Shepherd RM (1986) The effects of ethanol on intracellular calcium binding in isolated electro-permeabilized rat hepatocytes. J Physiol Lond 376:39P

    Google Scholar 

  • Russell IJ, Cody AR, Richardson GP (1986) The response of inner and outer hair cells in the basal turn of the guinea-pig cochlea and in the mouse cochlea grown in vitro. Hearing Res 22:199–216

    Google Scholar 

  • Sand O (1975) Effects of different ionic environments on mechanosensitivity of lateral line organs in the mudpuppy. J Comp Physiol 102:27–42

    Google Scholar 

  • Stephens PR, Young JZ (1982) The statocyst of the squid Loligo. J Zool Lond 197:241–266

    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 

  • Williamson R (1988a) Hair cell morphology in the statocyst of the squid Alloteuthis subulata. Soc Neurosci Abstr 14:377

    Google Scholar 

  • Williamson R (1988b) Vibration sensitivity in the statocyst of the northern octopus, Eledone cirrhosa. J Exp Biol 134:451–454

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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 

  • Wilson VJ, Jones GM (1979) Mammalian vestibular physiology. Plenum Press, New York

    Google Scholar 

  • Wubbels RJ, Kroese ABA, Duifhuis H (1990) Afferent bursting activity of ruff lateral line induced by background noise stimulation. J Comp Physiol A 166:585–588

    Google Scholar 

  • Young JZ (1989) The angular acceleration receptor system of diverse cephalopods. Phil Trans R Soc Lond B 325:189–238

    Google Scholar 

Download references

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  1. The Marine Biological Association of the U.K., PL1 2PB, Citadel Hill, Plymouth, England

    R. Williamson

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Williamson, R. The responses of primary and secondary sensory hair cells in the squid statocyst to mechanical stimulation. J Comp Physiol A 167, 655–664 (1990). https://doi.org/10.1007/BF00192659

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  • DOI: https://doi.org/10.1007/BF00192659

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