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Experimental Brain Research

, Volume 175, Issue 2, pp 256–267 | Cite as

Bone conducted vibration selectively activates irregular primary otolithic vestibular neurons in the guinea pig

  • Ian S. Curthoys
  • Juno Kim
  • Samara K. McPhedran
  • Aaron J. Camp
Research Article

Abstract

The main objective of this study was to determine whether bone-conducted vibration (BCV) is equally effective in activating both semicircular canal and otolith afferents in the guinea pig or whether there is preferential activation of one of these classes of vestibular afferents. To answer this question a large number (346) of single primary vestibular neurons were recorded extracellularly in anesthetized guinea pigs and were identified by their location in the vestibular nerve and classed as regular or irregular on the basis of the variability of their spontaneous discharge. If a neuron responded to angular acceleration it was classed as a semicircular canal neuron, if it responded to maintained roll or pitch tilts it was classified as an otolith neuron. Each neuron was then tested by BCV stimuli—either clicks, continuous pure tones (200–1,500 Hz) or short tone bursts (500 Hz lasting 7 ms)—delivered by a B-71 clinical bone-conduction oscillator cemented to the guinea pig's skull. All stimulus intensities were referred to that animal's own auditory brainstem response (ABR) threshold to BCV clicks, and the maximum intensity used was within the animal's physiological range and was usually around 70 dB above BCV threshold. In addition two sensitive single axis linear accelerometers cemented to the skull gave absolute values of the stimulus acceleration in the rostro-caudal direction. The criterion for a neuron being classed as activated was an audible, stimulus-locked increase in firing rate (a 10% change was easily detectable) in response to the BCV stimulus. At the stimulus levels used in this study, semicircular canal neurons, both regular and irregular, were insensitive to BCV stimuli and very few responded: only nine of 189 semicircular canal neurons tested (4.7%) showed a detectable increase in firing in response to BCV stimuli up to the maximum 2 V peak-to-peak level we delivered to the B-71 oscillator (which produced a peak-to-peak skull acceleration of around 6–8 g and was usually around 60–70 dB above the animal's own ABR threshold for BCV clicks). Regular otolithic afferents likewise had a poor response; only 14 of 99 tested (14.1%) showed any increase in firing rate up to the maximum BCV stimulus level. However, most irregular otolithic afferents (82.8%) showed a clear increase in firing rate in response to BCV stimuli: of the 58 irregular otolith neurons tested, 48 were activated, with some being activated at very low intensities (only about 10 dB above the animal's ABR threshold to BCV clicks). Most of the activated otolith afferents were in the superior division of the vestibular nerve and were probably utricular afferents. That was confirmed by evidence using juxtacellular injection of neurobiotin near BCV activated neurons to trace their site of origin to the utricular macula. We conclude there is a very clear preference for irregular otolith afferents to be activated selectively by BCV stimuli at low stimulus levels and that BCV stimuli activate some utricular irregular afferent neurons. The BCV generates compressional and shear waves, which travel through the skull and constitute head accelerations, which are sufficient to stimulate the most sensitive otolithic receptor cells.

Keywords

Vestibular Otolith Labyrinth Semicircular canal Sound Vibration Utricular Saccular 

Abbreviations

AC

Air conducted

BCV

Bone conducted vibration

ABR

Auditory brainstem response

VEMP

Vestibular evoked myogenic potential

CV

Coefficient of variation

Notes

Acknowledgments

We thank Michael Halmagyi, Leigh McGarvie, Mike Todd, Warren Davies, Ann Burgess for their help. Darek Figa and his team for their care of the guinea pigs. This research was supported by a grant from the NH & MRC of Australia (253620).

References

  1. Baird RA, Desmadryl G, Fernandez C, Goldberg JM (1988) The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J Neurophysiol 60:182–203PubMedGoogle Scholar
  2. Blanks RHI, Precht W (1976) Functional characterization of primary vestibular afferents in the frog. Exp Brain Res 25:369–370PubMedCrossRefGoogle Scholar
  3. de Burlet HM (1929) Zur vergleichenden Anatomie der Labyrinthinnervation. J Comp Neurol 47:155–169CrossRefGoogle Scholar
  4. Carey JP, Hirvonen TP, Hullar TE, Minor LB (2004) Acoustic responses of vestibular afferents in a model of superior canal dehiscence. Otol Neurotol 25:345–352PubMedCrossRefGoogle Scholar
  5. Cazals Y, Aran J-M, Erre J-P (1982) Frequency sensitivity and selectivity of acoustically evoked potentials after complete cochlear hair cell destruction. Brain Res 231:197–203PubMedCrossRefGoogle Scholar
  6. Colebatch JG, Halmagyi GM (1992) Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentation. Neurology 42:1635–1636PubMedGoogle Scholar
  7. Curthoys IS (1981a) Scarpa's ganglion in the rat and guinea pig. Acta Otolaryngol 92:107–113CrossRefGoogle Scholar
  8. Curthoys IS (1981b) The organization of the horizontal semicircular duct, ampulla and utricle in the rat and guinea pig. Acta Otolaryngol 92:323–330CrossRefGoogle Scholar
  9. Curthoys IS (1982) The response of primary horizontal semicircular canal neurons in the rat and guinea pig to angular acceleration. Exp Brain Res 47:286–294PubMedGoogle Scholar
  10. Curthoys IS, Markham CH (1971) Convergence of labyrinthine influences on units in the vestibular nuclei of the cat. I. Natural stimulation. Brain Res 35:469–490PubMedCrossRefGoogle Scholar
  11. Curthoys IS, Curthoys EJ, Blanks RHI, Markham CH (1975) The orientation of the semicircular canals in the guinea pig. Acta Otolaryngol 80:197–205PubMedCrossRefGoogle Scholar
  12. Curthoys IS, Markham CH, Blanks RHI (1977) Semicircular canal functional anatomy in cat, guinea pig and man. Acta Otolaryngol 83:258–265PubMedCrossRefGoogle Scholar
  13. Curthoys IS, Betts GA, Burgess AM, MacDougall HG, Cartwright AD, Halmagyi GM (1999) The planes of the utricular and saccular maculae of the guinea pig. Ann NY Acad Sci 871:27–34PubMedCrossRefGoogle Scholar
  14. Doyle H (1995) Seismology. Wiley, ChichesterGoogle Scholar
  15. Fernandez C, Goldberg JM (1976a) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. J Neurophysiol 39:970–984Google Scholar
  16. Fernandez C, Goldberg JM (1976b) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. II. Directional selectivity and force-response relations. J Neurophysiol 39:985–995Google Scholar
  17. Fernandez C, Goldberg JM (1976c) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. J Neurophysiol 39:996–1008Google Scholar
  18. Fernandez C, Goldberg JM, Baird RA (1990) The vestibular nerve of the chinchilla. III. Peripheral innervation patterns in the utricular macula. J Neurophysiol 63:767–804PubMedGoogle Scholar
  19. Goldberg JM (2000) Afferent diversity and the organization of central vestibular pathways. Exp Brain Res 130:277–297PubMedCrossRefGoogle Scholar
  20. Goldberg JM, Smith CE, Fernandez C (1984) Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J Neurophysiol 51:1236–1256PubMedGoogle Scholar
  21. Goldberg JM, Desmadryl G, Baird RA, Fernandez C (1990) The vestibular nerve of the chinchilla. V. Relation between afferent discharge properties and peripheral innervation patterns in the utricular macula. J Neurophysiol 63:791–804PubMedGoogle Scholar
  22. Hardy M (1934) Observations on the innervation of the macula sacculi in man. Anat Rec 59:403–418CrossRefGoogle Scholar
  23. Hullar TE, Della Santina CC, Hirvonen T, Lasker DM, Carey JP, Minor LB (2005) Responses of irregularly discharging chinchilla semicircular canal vestibular-nerve afferents during high-frequency head rotations. J Neurophysiol 93:2777–2786PubMedCrossRefGoogle Scholar
  24. Jombik P, Bahyl V (2005) Short latency responses in the averaged electro-oculogram elicited by vibrational impulse stimuli applied to the skull: could they reflect vestibulo-ocular reflex function. J Neurol Neurosurg Psychiatry 76:222–228PubMedCrossRefGoogle Scholar
  25. Koyama H, Lewis ER, Leverenz EL, Baird RA (1982) Acute seismic sensitivity in the bullfrog ear. Brain Res 250:168–172PubMedCrossRefGoogle Scholar
  26. Lee H-Y, Camp AJ, Callister RJ, Brichta AM (2005) Vestibular primary afferent activity in an in vitro preparation of the mouse inner ear. J Neurosci Methods 145:73–87PubMedCrossRefGoogle Scholar
  27. McCue MP, Guinan JJ (1994a) Acoustically responsive fibers in the vestibular nerve of the cat. J Neurosci 14:6058–6070Google Scholar
  28. McCue MP, Guinan JJ (1994b) Influence of efferent stimulation on acoustically responsive vestibular afferents in the cat. J Neurosci 14:6071–6083Google Scholar
  29. McCue MP, Guinan JJ (1995) Spontaneous activity and frequency selectivity of acoustically responsive vestibular afferents in the cat. J Neurophysiol 74:1563–1572PubMedGoogle Scholar
  30. McCue MP, Guinan JJ (1997) Sound-evoked activity in primary afferent neurons of a mammalian vestibular system. Am J Otol 18:355–360PubMedGoogle Scholar
  31. Mikaelian D (1964) Vestibular response to sound: single unit recording from the vestibular nerve in fenestrated deaf mice (Df/Df). Acta Otolaryngol 58:409–422PubMedCrossRefGoogle Scholar
  32. Murofushi T, Curthoys IS (1997) Physiological and anatomical study of click-sensitive primary vestibular afferents in the guinea pig. Acta Otolaryngol 117:66–72PubMedCrossRefGoogle Scholar
  33. Murofushi T, Curthoys IS, Topple AN, Colebatch JG, Halmagyi GM (1995) Responses of guinea pig primary vestibular neurons to clicks. Exp Brain Res 103:174–178PubMedCrossRefGoogle Scholar
  34. Naito R, Murofushi T, Mizutani M, Kaga K (1999) Auditory brainstem responses, electrocochleograms and cochlear microphonics in the myelin deficient hamster ‘bt’. Hear Res 136:44–48PubMedCrossRefGoogle Scholar
  35. Pinault D (1994) Golgi-like labeling of a single neuron recorded extracellularly. Neurosci Lett 170:255–260PubMedCrossRefGoogle Scholar
  36. Rosengren SM, Todd NPM, Colebatch JG (2005) Vestibular-evoked extra-ocular potentials produced by stimulation with bone-conducted sound. Clin Neurophysiol 116:1938–1948PubMedCrossRefGoogle Scholar
  37. Stein S, Wysession M (2003) An introduction to seismology, earthquakes and earth structure. Blackwell Publishing, OxfordGoogle Scholar
  38. Wada S-I, Starr A (1983) Generation of the auditory brainstem responses (ABRs). I. Effects of injection of a local anesthetic (Procaine HCl) into the trapezoid body of guinea pigs and cat. Electroencephalogr Clin Neurophysiol 56:326–339PubMedCrossRefGoogle Scholar
  39. Welgampola MS, Colebatch JG (2005) Characteristics and clinical applications of vestibular-evoked myogenic potentials. Neurology 64:1682–1688PubMedCrossRefGoogle Scholar
  40. Welgampola MS, Rosengren SM, Halmagyi GM, Colebatch JG (2003) Vestibular activation by bone conducted sound. J Neurol Neurosurg Psychiatry 74:771–778PubMedCrossRefGoogle Scholar
  41. Wit HP, Bleeker JD, Mulder HH (1984) Responses of pigeon vestibular nerve fibers to sound and vibration with audiofrequencies. J Acoust Soc Am 75:202–208PubMedCrossRefGoogle Scholar
  42. Young ED, Fernandez C, Goldberg JM (1977) Responses of squirrel monkey vestibular neurons to audio-frequency sound and head vibration. Acta Otolaryngol 84:352–360PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Ian S. Curthoys
    • 1
  • Juno Kim
    • 1
  • Samara K. McPhedran
    • 1
  • Aaron J. Camp
    • 1
  1. 1.Vestibular Research Laboratory, School of Psychology, A 18University of SydneySydneyAustralia

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