Display options
Cite
Curthoys IS, MacDougall HG, Vidal PP, et al. Sustained and Transient Vestibular Systems: A Physiological Basis for Interpreting Vestibular Function. Front Neurol. 2017;8:117doi: 10.3389/fneur.2017.00117.
Curthoys, I. S., MacDougall, H. G., Vidal, P. P., & de Waele, C. (2017). Sustained and Transient Vestibular Systems: A Physiological Basis for Interpreting Vestibular Function. Frontiers in neurology, 8117. https://doi.org/10.3389/fneur.2017.00117
Curthoys, Ian S, et al. "Sustained and Transient Vestibular Systems: A Physiological Basis for Interpreting Vestibular Function." Frontiers in neurology vol. 8 (2017): 117. doi: https://doi.org/10.3389/fneur.2017.00117
Curthoys IS, MacDougall HG, Vidal PP, de Waele C. Sustained and Transient Vestibular Systems: A Physiological Basis for Interpreting Vestibular Function. Front Neurol. 2017 Mar 30;8:117. doi: 10.3389/fneur.2017.00117. eCollection 2017. PMID: 28424655; PMCID: PMC5371610.
Copy Download .nbib Format: NLM
Share it on

Front Neurol. 2017 Mar 30;8:117. doi: 10.3389/fneur.2017.00117. eCollection 2017.

Sustained and Transient Vestibular Systems: A Physiological Basis for Interpreting Vestibular Function.

Frontiers in neurology

Ian S Curthoys, Hamish G MacDougall, Pierre-Paul Vidal, Catherine de Waele

Affiliations

  1. Vestibular Research Laboratory, School of Psychology, The University of Sydney, Sydney, NSW, Australia.
  2. Cognition and Action Group, CNRS UMR8257, Centre Universitaire des Saints-Pères, University Paris Descartes, Paris, France.
  3. ENT Department, Salpêtrière Hospital, Paris, France.

PMID: 28424655 PMCID: PMC5371610 DOI: 10.3389/fneur.2017.00117

Abstract

Otolithic afferents with regular resting discharge respond to gravity or low-frequency linear accelerations, and we term these the static or sustained otolithic system. However, in the otolithic sense organs, there is anatomical differentiation across the maculae and corresponding physiological differentiation. A specialized band of receptors called the striola consists of mainly type I receptors whose hair bundles are weakly tethered to the overlying otolithic membrane. The afferent neurons, which form calyx synapses on type I striolar receptors, have irregular resting discharge and have low thresholds to high frequency (e.g., 500 Hz) bone-conducted vibration and air-conducted sound. High-frequency sound and vibration likely causes fluid displacement which deflects the weakly tethered hair bundles of the very fast type I receptors. Irregular vestibular afferents show phase locking, similar to cochlear afferents, up to stimulus frequencies of kilohertz. We term these irregular afferents the transient system signaling dynamic otolithic stimulation. A 500-Hz vibration preferentially activates the otolith irregular afferents, since regular afferents are not activated at intensities used in clinical testing, whereas irregular afferents have low thresholds. We show how this sustained and transient distinction applies at the vestibular nuclei. The two systems have differential responses to vibration and sound, to ototoxic antibiotics, to galvanic stimulation, and to natural linear acceleration, and such differential sensitivity allows probing of the two systems. A 500-Hz vibration that selectively activates irregular otolithic afferents results in stimulus-locked eye movements in animals and humans. The preparatory myogenic potentials for these eye movements are measured in the new clinical test of otolith function-ocular vestibular-evoked myogenic potentials. We suggest 500-Hz vibration may identify the contribution of the transient system to vestibular controlled responses, such as vestibulo-ocular, vestibulo-spinal, and vestibulo-sympathetic responses. The prospect of particular treatments targeting one or the other of the transient or sustained systems is now being realized in the clinic by the use of intratympanic gentamicin which preferentially attacks type I receptors. We suggest that it is valuable to view vestibular responses by this sustained-transient distinction.

Keywords: otolith; sound; utricular; vestibular; vestibular-evoked myogenic potential; vestibular-evoked myogenic potentials; vestibulo-ocular reflex; vibration

References

  1. Exp Brain Res. 2015 Mar;233(3):691-9 - PubMed
  2. J Neurophysiol. 1976 Sep;39(5):985-95 - PubMed
  3. Otolaryngol Head Neck Surg. 2010 Aug;143(2):274-80 - PubMed
  4. J Assoc Res Otolaryngol. 2000 Nov;1(3):232-42 - PubMed
  5. Front Neurosci. 2016 Mar 31;10:96 - PubMed
  6. J Neurophysiol. 2009 Jan;101(1):141-9 - PubMed
  7. Neurology. 1983 Nov;33(11):1460-9 - PubMed
  8. Neurology. 2009 Oct 6;73(14):1134-41 - PubMed
  9. J Neurosci. 2013 Feb 20;33(8):3706-24 - PubMed
  10. J Neurosci. 1994 Oct;14(10):6058-70 - PubMed
  11. J Vestib Res. 2015;25(2):91-6 - PubMed
  12. Otol Neurotol. 2010 Jan;31(1):147-52 - PubMed
  13. Scan Electron Microsc. 1979;(3):929-38 - PubMed
  14. PLoS One. 2014 Aug 19;9(8):e105026 - PubMed
  15. Exp Brain Res. 2016 Oct;234(10):2747-60 - PubMed
  16. J Neurosci. 2016 Aug 31;36(35):9097-110 - PubMed
  17. J Neurophysiol. 1976 Sep;39(5):996-1008 - PubMed
  18. Ergeb Anat Entwicklungsgesch. 1969;42(1):1-113 - PubMed
  19. Laryngoscope. 2012 Jun;122(6):1342-52 - PubMed
  20. Int J Audiol. 2013 Oct;52(10):713-8 - PubMed
  21. Rev Laryngol Otol Rhinol (Bord). 2003;124(2):75-83 - PubMed
  22. J Exp Biol. 2011 Mar 1;214(Pt 5):862-70 - PubMed
  23. Comput Methods Programs Biomed. 1991 Jul;35(3):219-30 - PubMed
  24. Hear Res. 2011 Oct;280(1-2):133-40 - PubMed
  25. J Neurophysiol. 1971 Jul;34(4):676-84 - PubMed
  26. J Neurol Neurosurg Psychiatry. 1994 Feb;57(2):190-7 - PubMed
  27. Neurology. 2007 Apr 10;68(15):1227-9 - PubMed
  28. Acta Otolaryngol. 1977 Nov-Dec;84(5-6):352-60 - PubMed
  29. J Neurophysiol. 2004 Aug;92(2):845-61 - PubMed
  30. Otol Neurotol. 2004 May;25(3):345-52 - PubMed
  31. J Neurophysiol. 2011 Dec;106(6):2950-63 - PubMed
  32. Exp Brain Res. 2013 Sep;230(1):137-42 - PubMed
  33. Aviat Space Environ Med. 1987 Oct;58(10):970-6 - PubMed
  34. Exp Brain Res. 2006 May;171(2):251-61 - PubMed
  35. J Neurophysiol. 1992 Aug;68(2):471-84 - PubMed
  36. Hear Res. 1999 Sep;135(1-2):56-60 - PubMed
  37. Scan Electron Microsc. 1979;(3):967-74, 962 - PubMed
  38. Otol Neurotol. 2013 Aug;34(6):974-9 - PubMed
  39. J Neurophysiol. 1995 Oct;74(4):1563-72 - PubMed
  40. Neuroscience. 2011 Feb 23;175:262-72 - PubMed
  41. Compr Physiol. 2014 Apr;4(2):851-87 - PubMed
  42. Front Neurosci. 2014 Oct 09;8:316 - PubMed
  43. Prog Brain Res. 2003;142:189-201 - PubMed
  44. Brain Res Bull. 2004 Sep 30;64(3):265-71 - PubMed
  45. Front Neurosci. 2009 Aug 20;3:64 - PubMed
  46. Audiol Neurootol. 2009;14(1):59-66 - PubMed
  47. Exp Brain Res. 2017 Apr;235(4):957-972 - PubMed
  48. Acta Otolaryngol. 1983 May-Jun;95(5-6):494-507 - PubMed
  49. Auton Neurosci. 2002 Sep 30;100(1-2):77-83 - PubMed
  50. J Assoc Res Otolaryngol. 2007 Dec;8(4):497-508 - PubMed
  51. J Vestib Res. 2011;21(1):5-19 - PubMed
  52. Brain Res Bull. 2012 Oct 1;89(1-2):16-21 - PubMed
  53. J Neurophysiol. 1971 Jul;34(4):661-75 - PubMed
  54. Curr Opin Neurobiol. 2011 Aug;21(4):587-95 - PubMed
  55. Exp Brain Res. 2011 May;210(3-4):643-9 - PubMed
  56. Exp Brain Res. 2013 Aug;229(2):157-70 - PubMed
  57. J Assoc Res Otolaryngol. 2014 Aug;15(4):511-28 - PubMed
  58. J Neurophysiol. 1984 Jun;51(6):1236-56 - PubMed
  59. J Comp Neurol. 1994 Jun 22;344(4):481-507 - PubMed
  60. J Neurophysiol. 2016 May 1;115(5):2536-55 - PubMed
  61. Nat Commun. 2016 Oct 27;7:13229 - PubMed
  62. Exp Brain Res. 2011 May;210(3-4):423-36 - PubMed
  63. Clin Neurophysiol. 2011 Aug;122(8):1650-9 - PubMed
  64. Exp Brain Res. 2014 Apr;232(4):1379-88 - PubMed
  65. J Neurophysiol. 2006 Jan;95(1):171-86 - PubMed
  66. J Neurophysiol. 2008 Feb;99(2):718-33 - PubMed
  67. Neurosci Res. 2011 Dec;71(4):315-27 - PubMed
  68. Clin Neurophysiol. 2005 Aug;116(8):1938-48 - PubMed
  69. Exp Brain Res. 1997 May;114(3):405-22 - PubMed
  70. J Neurosci. 2008 Oct 8;28(41):10349-62 - PubMed
  71. Neuroscience. 2013 Dec 3;253:283-91 - PubMed
  72. J Neurophysiol. 2000 Nov;84(5):2514-28 - PubMed
  73. J Neurophysiol. 1965 Nov;28(6):1014-28 - PubMed
  74. J Comp Physiol A. 1997 Jun;180(6):631-8 - PubMed
  75. J Physiol. 2014 Apr 1;592(7):1565-80 - PubMed
  76. Hear Res. 2016 Jan;331:131-43 - PubMed
  77. Acta Otolaryngol. 1997 Jan;117(1):66-72 - PubMed
  78. Ann N Y Acad Sci. 1981;374:69-79 - PubMed
  79. Proc Biol Sci. 1997 Apr 22;264(1381):611-21 - PubMed
  80. Neurology. 2008 Nov 25;71(22):1776-82 - PubMed
  81. Acta Otolaryngol. 1979 May-Jun;87(5-6):490-8 - PubMed
  82. J Neurophysiol. 1990 Apr;63(4):767-80 - PubMed
  83. Curr Neurol Neurosci Rep. 2015 May;15(5):22 - PubMed
  84. Clin Neurophysiol. 2009 Mar;120(3):569-80 - PubMed
  85. Laryngoscope. 2014 Sep;124(9):2151-4 - PubMed
  86. J Neurophysiol. 2010 Oct;104(4):2034-51 - PubMed
  87. Laryngoscope. 2015 Aug;125(8):1915-20 - PubMed
  88. J Neurophysiol. 1966 May;29(3):467-92 - PubMed
  89. Otolaryngol Clin North Am. 2004 Oct;37(5):1075-90 - PubMed
  90. Acta Otolaryngol. 1999;119(7):750-7 - PubMed
  91. J Acoust Soc Am. 2006 Jul;120(1):258-69 - PubMed
  92. Clin Neurophysiol. 2010 Feb;121(2):132-44 - PubMed
  93. Ann N Y Acad Sci. 2011 Sep;1233:231-41 - PubMed
  94. J Comp Neurol. 2014 Jun 15;522(9):2053-74 - PubMed
  95. Otol Neurotol. 2013 Sep;34(7):1342-8 - PubMed
  96. Trials. 2014 Aug 18;15:328 - PubMed
  97. Audiol Neurootol. 2008;13(6):396-404 - PubMed
  98. J Neurosci. 1990 May;10(5):1557-69 - PubMed
  99. J Vestib Res. 2009;19(1-2):41-7 - PubMed
  100. Neuroscience. 2016 Nov 19;337:9-16 - PubMed
  101. Exp Brain Res. 2006 Nov;175(2):256-67 - PubMed
  102. J Assoc Res Otolaryngol. 2014 Feb;15(1):73-86 - PubMed
  103. Front Neuroanat. 2016 Feb 08;10:7 - PubMed
  104. J Neurophysiol. 2007 Sep;98(3):1549-65 - PubMed
  105. Tohoku J Exp Med. 1971 May;104(1):55-63 - PubMed
  106. Trends Neurosci. 2012 Mar;35(3):185-96 - PubMed
  107. J Neurophysiol. 1967 Jul;30(4):769-93 - PubMed
  108. Hear Res. 2000 Jul;145(1-2):8-16 - PubMed
  109. J Neurophysiol. 2011 Aug;106(2):754-63 - PubMed
  110. J Neurophysiol. 1971 Jul;34(4):635-60 - PubMed
  111. Exp Brain Res. 1996 Sep;111(1):149-52 - PubMed
  112. Exp Brain Res. 1995;103(1):174-8 - PubMed
  113. Front Neurol. 2017 Mar 09;8:41 - PubMed
  114. J Neurophysiol. 1987 Oct;58(4):719-38 - PubMed
  115. Am J Otol. 1997 May;18(3):355-60 - PubMed
  116. J Neurophysiol. 1965 Nov;28(6):991-1013 - PubMed
  117. J Neurophysiol. 2005 May;93(5):2777-86 - PubMed
  118. Hear Res. 1999 Oct;136(1-2):75-85 - PubMed
  119. J Neurophysiol. 2005 Feb;93(2):643-55 - PubMed
  120. J Neurosci. 2007 Apr 18;27(16):4283-96 - PubMed
  121. Ann N Y Acad Sci. 2009 May;1164:37-44 - PubMed
  122. Exp Brain Res. 2000 Feb;130(3):277-97 - PubMed
  123. J Neurophysiol. 2008 Oct;100(4):2192-204 - PubMed
  124. J Neurophysiol. 1976 Sep;39(5):970-84 - PubMed
  125. Prog Neurobiol. 2005 Aug;76(6):349-92 - PubMed
  126. Brain Res Bull. 2011 Aug 10;86(1-2):74-81 - PubMed
  127. Exp Brain Res. 2002 Apr;143(4):463-9 - PubMed
  128. Hear Res. 2005 Dec;210(1-2):53-62 - PubMed
  129. Exp Brain Res. 2011 May;210(3-4):347-52 - PubMed
  130. Acta Otolaryngol. 1969 Oct;68(4):350-62 - PubMed

Publication Types