Skip to main content
SpringerLink
Log in

Sensory transduction and neuronal transmission as related to ultrastructure and encoding of information in different labyrinthine receptor systems of vertebrates

  • Published:
Archives of oto-rhino-laryngology Aims and scope Submit manuscript

Summary

Mechano-electric transduction and neuronal transmission were studied in sensory systems ascending from and descending to single receptor cells of the labyrinth organs in submammalian vertebrates. The animals were young crocodiles (Caiman crocodilus), geckos (Gekko gecko, Tarentola mauritanica), and turtles (Pseudemys scripta elegans, Chinemys reevesii). Intracellular receptor potentials from the apical region of the hair cell (or from the ciliary surface) were recorded in the ampullar, macular, and papillar sensory cells. These single-cell responses are, within limits, proportional to stimulus amplitude, frequency, or phase and are bidirectional in that they show depolarization by kinociliopetal stereociliar displacement and hyperpolarization by kinociliofugal displacement. Synaptic potentials (presynaptic from the basal region of the hair cell, postsynaptic from the contacting nerve endings) were recorded in the utricular, saccular, and lagenar neuroepithelia with electron-optic localization of the in situ fixed microelectrode tip. As local excitatory or inhibitory processes, respectively, they follow the stimulus and receptor potential with latency and with nonlinear distortion. Action potentials (spikes), as synchronized by the excitatory synaptic potentials, were recorded from single nerve fibers or bipolar cells, related to ampullar, macular, or papular receptor units. Unit responses and synaptic potentials were recorded from the first, second, and following centripetal and central neurons of the ascending systems, or from neurons of the descending systems in the brain stem or from centrifugal neurons. Such records were achieved during adequate mechanical or acoustical stimulation of the different receptor systems, with additional electrical stimulation, uni- or bilaterally. Thus, the influence of centripetal-centrifugal bilateral interaction on the receptor functions was measured, as inhibition or disinhibition, respectively. The input-output relations of these sequential stages of information transfer were plotted as histograms of different types, as characteristic curves, power spectra, or by correlation operations, with or without feedback, from the different systemic levels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Andres KH, Düring M v, Khan NS, Trincker DEW (1977) Comparative studies on ultrastructure and functions of labyrinth receptors and brain stem neurons in submammalian vertebrates. In: Portmann M, Aran J-M (eds) Inner ear biology, Bordeaux 1977. INSERM (Paris) 68: 77–90

    Google Scholar 

  2. Baird IL (1970/78) The anatomy of the reptilian ear. In: Gans C (ed) Biology of the reptilia, vol 2. Academic Press, London, New York, pp 193–275

    Google Scholar 

  3. Blanks RHI, Precht W (1976) Functional characterization of primary vestibular afferents in the frog. Exp Brain Res 25: 369–390

    Google Scholar 

  4. Budelmann B-U (1978) The function of the equilibrium receptor systems of cephalopods. Verh Ges Neurootol Aequ (Proc Neurootol Equ Soc) 6 (1): 15–63

    Google Scholar 

  5. Dallos P, Cheatham MA (1976) Production of cochlear potentials by inner and outer hair cells. J Acoust Soc Am 60: 510–512

    Google Scholar 

  6. Düring M v, Trincker DEW, Röskenbleck H (1977) Ultrastructure and function of the labyrinthine sensory systems in Caiman crocodilus. Pfluegers Arch [Suppl R 43] 368: 172

    Google Scholar 

  7. Fettiplace R, Crawford AC (1978) The coding of sound pressure and frequency in cochlear hair cells of the terrapin. Proc R Soc B 203: 209–218

    Google Scholar 

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

    Google Scholar 

  9. Flock Å, Flock B, Murray E (1977) Studies on the sensory hairs of receptor cells in the inner ear. Acta Otolaryngol 83: 85–91

    Google Scholar 

  10. Flohr H, Bienhold H, Abeln W, Macskovics I (1981) Concepts of vestibular compensation. In: Flohr H, Precht W (eds) Lesion-induced neuronal plasticity in sensorimotor systems, Bremen 1980. Springer, Berlin Heidelberg New York, pp 153–172

    Google Scholar 

  11. Furukawa T, Matsuura S (1978) Adaptive rundown of excitatory post-synaptic potentials at synapses between hair cells and eight nerve fibres in the goldfish. J Physiol (Lond) 276: 193–209

    Google Scholar 

  12. Gawlik P, Khan NS, Küpper R, Müller-Arnecke H, Trincker DEW (1978) Studies on receptor functions of lagena and papilla basilaris in the tokay and caiman. Pfluegers Arch [Suppl R 86] 373: 315

    Google Scholar 

  13. Grundig P, Khan NS, Müller-Arnecke H, Trincker DEW (1980) Bilateral interaction in the sensory systems, ascending from and descending to labyrinthine receptor cells. Pfluegers Arch [Suppl R 25] 384: 97

    Google Scholar 

  14. Grundig P, Khan NS, Rennings U, Trincker DEW (1981) Electro-optical transmission of signals as a method for bio-electrical recording from mechanoreceptor systems. Pfluegers Arch [Suppl R 32] 389: 127

    Google Scholar 

  15. Hartmann R, Klinke R (1980) Efferent activity in the goldfish vestibular nerve and its influence on afferent activity. Pfluegers Arch 388: 123–128

    Google Scholar 

  16. Hepp-Reymond M-C, Palin J (1968) Patterns in the cochlear potentials of the tokay gecko (Gekko gecko). Acta Otolaryngol 65: 270–292

    Google Scholar 

  17. Honrubia V, Ward PH (1969) Mechanism of production of cochlear microphonics. J Acoust Soc Am 47: 498–503

    Google Scholar 

  18. 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 

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

    Google Scholar 

  20. Iurato S (ed) (1967) Submicroscopic structure of the inner ear. Pergamon Press, London

    Google Scholar 

  21. Khan NS, Müller-Arnecke H, Trincker DEW (1978) Hair cell functions and related neuronal activities in the different receptor systems of the geckonid and crocodilian labyrinth. J Physiol (Lond) 284:78–79P

    Google Scholar 

  22. Khan NS, Müller-Arnecke H, Röskenbleck H, Trincker DEW (1979) Functions of different receptor systems in the reptilian labyrinth. Arch Otorhinolaryngol 224: 31–35

    Google Scholar 

  23. Kim DO, Molnar CE (1979) A population study of cochlear nerve fibers: comparison of the spatial distributions of average-rate and phase-locking measures of responses to single tones. J Neurophysiol 42: 16–30

    Google Scholar 

  24. Klinke R, Pause M (1980) Discharge properties of primary auditory fibres in Caiman crocodilus: comparisons and contrasts to the mammalian auditory nerve. Exp Brain Res 38: 137–150

    Google Scholar 

  25. Lowenstein O (1970) Electro-physiological experiments on the isolated surviving labyrinth of elasmobranch fish to analyse the responses to linear accelerations. In: Stahle J (ed) Vestibular function on earth and in space. Pergamon Press, London New York, pp 35–41

    Google Scholar 

  26. Manley GA (1974) Activity patterns of neurons in the peripheral auditory system of some reptiles. Brain Behav Evol 10: 244–256

    Google Scholar 

  27. Miller MR (1980) The reptilian cochlear duct. In: Popper AN, Fay RR (eds) Comparative studies of hearing in vertebrates. Springer, Berlin Heidelberg New York, pp 169–204

    Google Scholar 

  28. Mulroy MJ, Altmann DW, Weiss TF, Peake WT (1974) Intracellular electric responses to sound in a vertebrate cochlea. Nature 249: 482–485

    Google Scholar 

  29. Nadol JB, Mulroy MJ, Goodenough DA, Weiss TF (1976) Tight and gap junctions in a vertebrate inner ear. Am J Anat 147: 281–302

    Google Scholar 

  30. O'Leary DP, Dunn RF, Honrubia V (1976) Analysis of afferent responses from isolated semicircular canal of the guitarfish using rotational acceleration white-noise inputs. J Neurophysiol 39: 631–644 (I.), 645–659 (II.)

    Google Scholar 

  31. Peake WT, Ling A (1978) Absence of tonotopic organization in the motion of the basilar membrane of the alligator lizard. J Acoust Soc Am 63: P 66

    Google Scholar 

  32. Precht W, Llinás R (1969) Functional organization of the vestibular afferents to the cerebellar cortex of frog and cat. Exp Brain Res 9: 30–52

    Google Scholar 

  33. Pritz MB (1974) Ascending connections of a midbrain auditory area in a crocodile, Caiman crocodilus. J Comp Neurol 153: 179–198

    Google Scholar 

  34. Pritz MB (1974) Ascending connections of a thalamic auditory area in a crocodile, Caiman crocodilus. J Comp Neurol 153: 199–214

    Google Scholar 

  35. Retzius G (1881/84) Das Gehörorgan der Wirbelthiere, I und II. Samson & Wallin, Stockholm

    Google Scholar 

  36. Russell IJ, Sellick PM (1978) Intracellular studies of hair cells in the mammalian cochlea. J Physiol (Lond) 284: 261–290

    Google Scholar 

  37. Sellick PM, Russel IJ (1980) The responses of inner hair cells to basilar membrane velocity during low frequency auditory stimulation in the guinea pig cochlea. Hearing Res 2: 439–445

    Google Scholar 

  38. Spoendlin H (1973) The innervation of the cochlear receptor. In: Møller AR (ed) Basic mechanisms in hearing. Academic Press, London New York, pp 185–234

    Google Scholar 

  39. Strutz J (1981) The origin of centrifugal fibers to the inner ear in Caiman crocodilus. A horseradish peroxidase study. Neurosci Lett 27: 95–100

    Google Scholar 

  40. Tanaka Y, Asanuma A, Yanagisawa K (1980) Potentials of outer hair cells and their membrane properties in cationic environments. Hearing Res 2: 431–438

    Google Scholar 

  41. Thalmann I, Marcus NY, Thalmann R (1979) Adenine nucleotides of the stria vascularis. Arch Otorhinolaryngol 224: 89–95

    Google Scholar 

  42. Trincker DEW (1974) Fidelity of mechano-electric transduction by the labyrinthine receptor systems. J Dyn Syst Meas Control 96: 440–444

    Google Scholar 

  43. Trincker DEW, Khan NS (1977) Labyrinthine receptor potentials, peripheral and central neuronal responses, under afferent-efferent bilateral interaction conditions in the vestibular systems of frog and caiman. IRCS Med Sci (Nerv Syst Physiol) 5: 29

    Google Scholar 

  44. Trincker DEW, Khan NS, Müller-Arnecke H (1978) Comparative studies on DC resting potentials of the mammalian and reptilian labyrinth organs. IRCS Med Sci (Nerv Syst Physiol) 6: 211

    Google Scholar 

  45. Trincker DEW, et al. (1982) Die labyrinthäre Haarzelle als mechano-elektrischer Wandler. Funct Biol Med 1: 11

    Google Scholar 

  46. Turner RG (1980) Physiology and bioacoustics in reptiles. In: Popper AN, Fay RR (eds) Comparative studies of hearing in vertebrates. Springer, Berlin Heidelberg New York, pp 205–237

    Google Scholar 

  47. Weiss TF, Altmann DW, Mulroy MJ (1978) Endolymphatic and intracellular resting potential in the alligator lizard cochlea. Pfluegers Arch 373: 77–84

    Google Scholar 

  48. Weiss TF, Mulroy MJ, Altmann DW (1974) Intracellular responses to acoustic clicks in the inner ear of the alligator lizard. J Acoust Soc Am 55: 606–619

    Google Scholar 

  49. Weiss TF, Peake WT, Ling A, Holton T (1978) Which structures determine the frequency selectivity and tonotopic organization of vertebrate cochlear nerve fibers? Evidence from the alligator lizard. In: Naunton RF, Fernández C (eds) Evoked electrical activity in the auditory nervous system. Academic Press, London New York, pp 91–112

    Google Scholar 

  50. Wersäll J, Bagger-Sjöbäck D (1974) Morphology of the vestibular sense organ. In: Kornhuber HH (ed) Handbook of sensory physiology, vol VI/1. Springer, Berlin Heidelberg New York, pp 123–170

    Google Scholar 

  51. Weston JK (1936) The reptilian vestibular and cerebellar gray with fiber connections. J Comp Neurol 65: 93–199

    Google Scholar 

  52. Wever EG (1978) The reptile ear: Its structure and function. Princeton University Press, Princeton

    Google Scholar 

  53. Wilson VJ, Gacek RR, Uchino Y, Susswein A (1978) Properties of central vestibular neurons fired by stimulation of the saccular nerve. Brain Res 143: 251–261

    Google Scholar 

  54. Wylie RM (1973) Evidence of electrotonic transmission in the vestibular nuclei of the rat. Brain Res 50: 179–183

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology II, MA 4/149, Ruhr University, Hattinger Str. 374, D-4630, Bochum 1, Federal Republic of Germany

    N. S. Khan, U. Schwabl & D. E. W. Trincker

Authors
  1. N. S. Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. U. Schwabl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. E. W. Trincker
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported by the VW-Stiftung, Hannover

This work, as a shorter paper, was read at the 18th Workshop on Inner Ear Biology, Montpellier/La Grande Motte, September 15, 1981

Rights and permissions

Reprints and permissions

About this article

Cite this article

Khan, N.S., Schwabl, U. & Trincker, D.E.W. Sensory transduction and neuronal transmission as related to ultrastructure and encoding of information in different labyrinthine receptor systems of vertebrates. Arch Otorhinolaryngol 236, 27–39 (1982). https://doi.org/10.1007/BF00464055

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00464055

Key words

Search

Navigation