Skip to main content
Log in

Structural features of the lateral walls in mammalian cochlear outer hair cells

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Freeze-fracture, freeze-etching and thin sections have been used to determine features of the structural organisation of the lateral walls in cochlear outer hair cells. The presence of an organised meshwork of filaments in the lateral cortex of the cell is confirmed in intact unfixed cells. This meshwork showed morphological features similar to the cytoskeletal lattice. The lateral plasma membrane is shown to be protein-rich and to contain cholesterol. The membranes of the subplasmalemmal lateral cisternae contain much less protein, and little cholesterol as judged by their responses to filipin and tomatin. These findings indicate differences in the physical properties of the two membrane systems. On the fracture faces of the plasma membrane there is a high density of intramembrane particles and this particle population is heterogeneous. Some particles show morphological features consistent with those of transmembrane channels. Regularly spaced pillars crossing the space between the plasma and cisternal membranes were identified both in thin sections and in freezeetched preparations, but neither the plasma nor cisternal membrane fracture faces showed any feature corresponding directly to the pillar. This suggests the pillars do not insert directly into either membrane. Freeze-fracture and freeze-etching of unfixed cells indicated that the pillar is indirectly associated with the cytoplasmic surface of the plasma membrane, and, at its inner end, linked to the cortical cytoskeletal lattice on the outer surface of the cisternal membrane.

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

  • Ashmore JF (1987) A fast motile response in guinea pig outer hair cells: the cellular basis of the cochlear amplifier. J Physiol 388:323–347

    Google Scholar 

  • Ashmore JF, Meech RW (1986) Ionic basis of membrane potential in outer hair cells of guinea pig cochlea. Nature 322:368–371

    Google Scholar 

  • Bagger-Sjoback D, Flock A (1977) Freeze-fracture of the auditory basilar papilla in the lizard Calotes versicolor. Cell Tissue Res 177:431–443

    Google Scholar 

  • Bannister LH, Dodson HC, Astbury AR, Douek EE (1988) The cortical lattice: a highly ordered system of subsurface filaments in guinea pig cochlear outer hair cells. Prog Brain Res 74:213–219

    Google Scholar 

  • Bennett V (1985) The membrane skeleton of human erythrocytes and its implication for more complex cells. Ann Rev Biochem 54:273–304

    Google Scholar 

  • Bennett V (1990) Spectrin: a structural mediator between diverse plasma membrane proteins and the cytoplasm. Curr Opin Cell Biol 2:51–56

    Google Scholar 

  • Block BA, Imagawa T, Campbell KP, Franzini-Armstrong C (1988) Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J Cell Biol 107:2587–2600

    Google Scholar 

  • Branton D (1971) Freeze-etching studies of membrane structure. Phil Trans Roy Soc B 261:133–138

    Google Scholar 

  • Brownell WE (1990) Outer hair cell electromotility and otoacoustic emissions. Ear Hearing 11:82–92

    Google Scholar 

  • Brownell WE, Bader CR, Bertrand D, de Ribaupierre Y (1984) Evoked mechanical responses of isolated cochlear outer hair cells. Science 227:194–196

    Google Scholar 

  • Dodson HC, Bannister LH, Douek EE (1982) The effects of combined gentamicin and white noise on the spiral organ of young guinea pigs. Acta Otolaryngol 94:193–202

    Google Scholar 

  • Dulon D, Aran J-M, Schacht J (1987) Osmotically induced motility of outer hair cells: implications for Menière's disease. Arch Otorhinolaryngol 244:104–107

    Google Scholar 

  • Dulon D, Zajie G, Schacht J (1988) [K+]-depolarisation induces motility in outer hair cells by an osmotic mechanism. Hearing Res 32:123–130

    Google Scholar 

  • Dulon D, Zajic G, Schacht J (1990) Increasing intracellular free calcium induces circumferential contractions in isolated cochlear outer hair cells. J Neurosci 10:1388–1397

    Google Scholar 

  • Evans BN (1990) Fatal contractions: ultrastructural and electromechanical changes in outer hair cells following transmembraneous electrical stimulation. Hearing Res 45:265–282

    Google Scholar 

  • Flock A, Flock B, Ulfendahl M (1986) Mechanisms of movement in outer hair cells and a possible structural basis. Arch Otobaryngol 243:83–96

    Google Scholar 

  • Forge A (1985) Cholesterol distribution in cells of the stria vascularis of the mammalian cochlea and some effects of ototoxic diuretics. J Cell Sci 79:181–197

    Google Scholar 

  • Forge A (1986) The morphology of the normal and pathological cell membrane and junctional complexes of the cochlea. In: Salvi RJ, Henderson D, Hamernik RP, Colletti V (eds) Basic and applied aspects of noise-induced hearing loss. Plenum Publishing Corporation. New York, pp 55–68

    Google Scholar 

  • Forge A (1987) Specialisations of the lateral membrane of inner hair cells. Hearing Res 31:99–110

    Google Scholar 

  • Forge A (1989) The lateral walls of inner and outer hair cells. In: Wilson JP, Kemp DT (eds) Cochlear mechanisms. Plenum Publishing Corporation, pp 29–35

  • Forge A, Knowles PF, Marsh D (1978) Morphology of egg phosphatidylcholine-cholesterol single bilayer vesicles studied by freeze-etch electron microscopy. J Memb Biol 41:249–263

    Google Scholar 

  • Forge A, Davies S, Zajic G (1991) Assessment of ultrastructure in isolated cochlear hair cells using a procedure for rapid-freezing prior to freeze-fracture and deep-etching. J Neurocytol 20:471–484

    Google Scholar 

  • Gulley RL, Reese TS (1977) Regional specialisations of the hair cell plasmalemma in the organ of Corti. Anat Rec 189:109–124

    Google Scholar 

  • Hanna RB, Ornberg RL, Reese TS (1985) Structural details of rapidly frozen gap junctions. In: Bennett MVL, Spray DC (eds) Gap junctions. Cold Spring Harbour Laboratory, pp 23–32

  • Hirokawa N (1980) A freeze-fracture study on intercellular junctions between various kinds of epithelial cells surrounding common endolymphatic space in the hearing organ of the chick. Anat Rec 196:129–143

    Google Scholar 

  • Holley MC, Ashmore JF (1988) A cytoskeletal spring in cochlear outer hair cells. Nature 335:635–637

    Google Scholar 

  • Holley MC, Ashmore JF (1990a) Spectrin actin and the structure of the cortical lattice in mammalian cochlear outer hair cells. J Cell Sci 96:283–291

    Google Scholar 

  • Holley MC, Ashmore JF (1990b) A cytoskeletal spring for the control of cell shape in outer hair cells isolated from the guinea pig cochlea. Eur Arch Otorhinolaryngol 247:4–7

    Google Scholar 

  • Kemp DT (1978) Stimulated acoustic emission from within the human auditory system. J Acoust Soc Am 64:1386–1391

    Google Scholar 

  • Lim DJ (1986) Functional structure of the organ of Corti. A review. Hearing Res 22:117–146

    Google Scholar 

  • McDowell B, Davies S, Forge A (1989) The effect of gentamicin-induced hair cell loss on the tight junctions of the reticular lamina. Hearing Res 40:221–232

    Google Scholar 

  • Rash JE, Johnson TJA, Hudson SC, Giddings FD, Graham WF, Elderfrawi ME (1982) Labelled-replica techniques: post-shadow labelling of intramembrane particles in freeze-fracture replicas. J Microsc 128:121–138

    Google Scholar 

  • Robards AW, Sleytr UB (1985) Low temperature methods in biological electron microscopy. Elsevier, Amsterdam

    Google Scholar 

  • Saito K (1983) Fine structure of the sensory epithelium of guinea-pig organ of Corti: sub-surface cisternae and lamellar bodies in the outer hair cells. Cell Tissue Res 229:467–481

    Google Scholar 

  • Severs N, Robenek H (1983) Detection of microdomains in biomembranes. An appraisal of recent developments in freeze-fracture cytochemistry. Biochim Biophys Acta 737:373–408

    Google Scholar 

  • Slepecky N, Hamernik R, Henderson D, Coling D (1982) Correlation of audiometric data with changes in cochlear hair cell stereocilia resulting from impulse noise trauma. Acta Otolaryngol 93:329–340

    Google Scholar 

  • Sommer JR, Dolber PC, Taylor I (1982) Filipin-sterol complexes in the membranes of cardiac muscle. J Ultrastruct Res 80:98–103

    Google Scholar 

  • Spoendlin H (1974) Neuroanatomy of the cochlea. In: Zwicker E, Terhardt E (eds) Facts and models in hearing. Springer, Berlin, pp 18–32

    Google Scholar 

  • Zajic G, Schacht J (1987) Comparison of isolated outer hair cells from five mammalian species. Hearing Res 26:249–256

    Google Scholar 

  • Zenner HP, Zimmermann U, Schmitt U (1985) Reversible contraction of isolated mammalian cochlear hair cells. Hearing Res 18:127–133

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Forge, A. Structural features of the lateral walls in mammalian cochlear outer hair cells. Cell Tissue Res 265, 473–483 (1991). https://doi.org/10.1007/BF00340870

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00340870

Key words

Navigation