Input–Output Functions of Vestibular Afferent Responses to Air-Conducted Clicks in Rats

  • Hong Zhu
  • Xuehui Tang
  • Wei Wei
  • Adel Maklad
  • William Mustain
  • Richard Rabbitt
  • Steve Highstein
  • Jerome Allison
  • Wu Zhou
Research Article


Sound-evoked vestibular myogenic potentials recorded from the sternocleidomastoid muscles (the cervical vestibular-evoked myogenic potential or cVEMP) and the extraocular muscles (the ocular VEMP or oVEMP) have proven useful in clinical assessment of vestibular function. VEMPs are commonly interpreted as a test of saccular function, based on neurophysiological evidence showing activation of saccular afferents by intense acoustic click stimuli. However, recent neurophysiological studies suggest that the clicks used in clinical VEMP tests activate vestibular end organs other than the saccule. To provide the neural basis for interpreting clinical VEMP testing results, the present study examined the extent to which air-conducted clicks differentially activate the various vestibular end organs at several intensities and durations in Sprague–Dawley rats. Single unit recordings were made from 562 vestibular afferents that innervated the otoliths [inferior branch otolith (IO) and superior branch otolith (SO)], the anterior canal (AC), the horizontal canal (HC), and the posterior canal (PC). Clicks higher than 60 dB SL (re-auditory brainstem response threshold) activated both semicircular canal and otolith organ afferents. Clicks at or below 60 dB SL, however, activated only otolith organ afferents. Longer duration clicks evoked larger responses in AC, HC, and SO afferents, but not in IO afferents. Intra-axonal recording and labeling confirmed that sound sensitive vestibular afferents innervated the horizontal and anterior canal cristae as well as the saccular and utricular maculae. Interestingly, all sound sensitive afferents are calyx-bearing fibers. These results demonstrate stimulus-dependent acoustic activation of both semicircular canals and otolith organs, and suggest that sound activation of vestibular end organs other than the saccule should not be ruled out when designing and interpreting clinical VEMP tests.


vestibular sound VEMP single unit recording rat saccule semicircular canal 



This study is supported by NIH R01DC012060 (HZ), NIH R01DC008585 (WZ), and R01DC006685 (RDR).


None of the authors have any conflicts of interests.


  1. Akin FW, Murnane OD, Proffitt TM (2003) The effects of click and tone-burst stimulus parameters on the vestibular evoked myogenic potential (VEMP). J Am Acad Audiol Nov 14(9):500–509CrossRefGoogle Scholar
  2. Baird RA, Desmadryl GL, Femandez 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
  3. Bickford RG, Jacobson JL, Cody DTR (1964) Nature of averaged evoked potentials to sound and other stimuli in man. Ann NY Acad Sci 112:204–218PubMedCrossRefGoogle Scholar
  4. Blanks RH, Torigoe Y (1989) Orientation of the semicircular canals in rat. Brain Res 487(2):278–287PubMedCrossRefGoogle Scholar
  5. Boyle R, Carey JP, Highstein SM (1991) Morphological correlates of response dynamics and efferent stimulation in horizontal semicircular canal afferents of the toadfish Opsanus tau. J Neurophysiol 66(5):1504–1521PubMedGoogle Scholar
  6. Broussard DM, Lisberger SG (1992) Vestibular input to brain stem neurons that participate in motor learning in the primate vestibuloocular reflex. J Neurophysiol 68:1906–1909PubMedGoogle Scholar
  7. Broussard DM, DeCharms RC, Lisberger SG (1995) Inputs from the ipsilateral and contralateral vestibular apparatus to behaviorally characterized abducens neurons in rhesus monkeys. J Neurophysiol 74:2445–2459PubMedGoogle Scholar
  8. 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
  9. Colebatch JG (2001) Vestibular evoked potentials. Curr Opin Neurol 14:21–26PubMedCrossRefGoogle Scholar
  10. Colebatch JG (2010) Sound conclusion? Clin Neurophysiol 121:124–126PubMedCrossRefGoogle Scholar
  11. Colebatch JG, Halmagyi GM (1992) Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentation. Neurology 42(8):1635–1636PubMedCrossRefGoogle Scholar
  12. Colebatch JG, Rothwell JC (2004) Motor unit excitability changes mediating vestibulocollic reflexes in the sternocleidomastoid muscle. Clin Neurophysiol 115(11):2567–2573PubMedCrossRefGoogle Scholar
  13. Colebatch JG, Halmagyi GM, Skuse NF (1994) Myogenic potentials generated by a click-evoked vestibulocollic reflex. J Neurol Neurosurg Psychiatry 57:190–197PubMedCrossRefGoogle Scholar
  14. Curthoys IS (2010) A critical review of the neurophysiological evidence underlying clinical vestibular testing using sound, vibration and galvanic stimuli. Clin Neurophysiol 121:132–144PubMedCrossRefGoogle Scholar
  15. Curthoys IS, Vulovic V (2011) Vestibular primary afferent responses to sound and vibration in the guinea pig. Exp Brain Res 210:347–352PubMedCrossRefGoogle Scholar
  16. Curthoys IS, Kim J, McPhedran SK, Camp AJ (2006) Bone conducted vibration selectively activates irregular primary otolithic vestibular neurons in the guinea pig. Exp Brain Res 175(2):256–267PubMedCrossRefGoogle Scholar
  17. Curthoys IS, Vulovic V, Sokolic L, Pogson J, Burgess AM (2012) Irregular primary otolith afferents from the guinea pig utricular and saccular maculae respond to both bone conducted vibration and to air conducted sound. Brain Res Bull 89(1–2):16–21PubMedCrossRefGoogle Scholar
  18. Daunicht WJ, Pellionisz AJ (1987) Spatial arrangement of the vestibular and the oculomotor system in the rat. Brain Res 435:48–56PubMedCrossRefGoogle Scholar
  19. Eatock RA, Songer JE (2011) Vestibular hair cells and afferents: two channels for head motion signals. Ann Rev Neurosci 34:501–534PubMedCrossRefGoogle Scholar
  20. Estes MS, Blanks RHI, Markham CH (1975) Physiological characteristics of vestibular first-order canal neurons in the cat. I. Response plane determination and resting discharge characteristics. J Neurophysiol 38:1232–1249PubMedGoogle Scholar
  21. Fernandez C, Goldberg JM (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J Neurophysiol 34:661–675PubMedGoogle Scholar
  22. Goldberg JM, Fernandez C (1975) Responses of peripheral vestibular neurons to angular and linear accelerations in the squirrel monkey. Acta Oto-laryngologica 80(1–6):101–110PubMedCrossRefGoogle Scholar
  23. Goldberg JM, Fernandez C (1980) Efferent vestibular system in the squirrel monkey: anatomical location and influence on afferent activity. J Neurophysiol 43:986–1025PubMedGoogle Scholar
  24. 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(6):1236–1256PubMedGoogle Scholar
  25. Goldberg JM, Wilson VJ, Cullen KE, Angelaki DE, Broussard DM, Buttnwe-Ennever JA, Fukushima K, Minor LB (2012) Clinical manifestation of peripheral vestibular dysfunction. In the vestibular system: a sixth sense. Oxford University Press, Oxford, pp 495–524Google Scholar
  26. Halmagyi GM, Curthoys IS, Colebatch JG, Aw ST (2005) Vestibular responses to sound. Ann NY Acad Sci 1039:54–67PubMedCrossRefGoogle Scholar
  27. Holstein GR, Rabbitt RD, Martinelli GP, Friedrich VL Jr, Boyle RD, Highstein SM (2004) Convergence of excitatory and inhibitory hair cell transmitters shapes vestibular afferent responses. PNAS 101:15766–15771PubMedCrossRefGoogle Scholar
  28. Huang TW, Su HC, Cheng PW (2005) Effect of click duration on vestibular-evoked myogenic potentials. Acta Otolaryngol 125:141–144PubMedCrossRefGoogle Scholar
  29. Hullar TE, Minor LB (1999) High-frequency dynamics of regularly discharging canal afferents provide a linear signal for angular vestibuloocular reflexes. J Neurophysiol 82:2000–2005PubMedGoogle Scholar
  30. Keller EL (1976) Behavior of horizontal semicircular canal afferents in alert monkey during vestibular and optokinetic stimulation. Exp Brain Res 24:459–471PubMedCrossRefGoogle Scholar
  31. Klinke R, Galley N (1974) Efferent innervation of vestibular and auditory receptors. Physiol Rev 54:316–357PubMedGoogle Scholar
  32. Lasker DM, Han GC, Park HJ, Minor LB (2008) Rotational responses of vestibular–nerve afferents innervating the semicircular canals in the C57BL/6 mouse. J Assoc Res Otolaryngol 9(3):334–348PubMedCentralPubMedCrossRefGoogle Scholar
  33. Lindeman HH (1969) Studies of the morphology of the sensory regions of the vestibular apparatus. Erg Anat 42:1–113PubMedGoogle Scholar
  34. Lisberger SG, Pavelko TA (1986) Vestibular signals carried by pathways subserving plasticity of the vestibulo-ocular reflex in monkeys. J Neurosci 6:346–354PubMedGoogle Scholar
  35. Luis L, Costa J, Vaz Garcia F, Valls-Solé J, Brandt T, Schneider E (2013a) Spontaneous plugging of the horizontal semicircular canal with reversible canal dysfunction and recovery of vestibular evoked myogenic potentials. Otol. Neurotol 34:743–747Google Scholar
  36. Luis L, Zhu H, Costa J, Valls-Solé J, Brandt T, Zhou W, Schneider E (2013b) Reply to the commentary on Luis et al. “Spontaneous plugging of the horizontal semicircular canal with reversible canal dysfunction and recovery of vestibular evoked myogenic potentials”. Otol Neurotol (in press)Google Scholar
  37. McCue MP, Guinan JJ (1994a) Acoustically responsive fibers in the vestibular nerve of the cat. J Neurosci 14:6058–6070PubMedGoogle Scholar
  38. McCue MP, Guinan JJ (1994b) Influence of efferent stimulation on acoustically responsive vestibular afferents in the cat. J Neurosci 14:6071–6083PubMedGoogle Scholar
  39. McCue MP, Guinan JJ (1995) Spontaneous activity and frequency selectivity of acoustically responsive vestibular afferents in the cat. J Neurophysiol 74:1563–1572PubMedGoogle Scholar
  40. McCue MP, Guinan JJ (1997) Sound-evoked activity in primary afferent neurons of a mammalian vestibular system. Am J Otol 18:355–360PubMedGoogle Scholar
  41. Minor LB, Solomon D, Zinreich J, Zee DS (1998) Sound- and/or pressure-induced vertigo due to bone dehiscence of the superior semicircular canal. Arch Otolaryngol Head Neck Surg 124:249–258PubMedCrossRefGoogle Scholar
  42. Minor LB, Cremer PD, Carey JP, Della Santina CC, Streubel SO, Weg N (2001) Symptoms and signs in superior canal dehiscence syndrome. Ann NY Acad Sci 942:259–273PubMedCrossRefGoogle Scholar
  43. 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
  44. 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
  45. Ochi K, Ohashi T, Nishino H (2001) Variance of vestibular-evoked myogenic potentials. Laryngoscope 111(3):522–527PubMedCrossRefGoogle Scholar
  46. Parker DE, Tubbs RL, Littlefield VM (1978) Visual‐field displacements in human beings evoked by acoustical transients. J Acoust Soc Am 63(6):1912–1918PubMedCrossRefGoogle Scholar
  47. Rauch SD (2006) Vestibular evoked myogenic potentials. Curr Opin Otolaryngol Head Neck Surg 14:299–304PubMedCrossRefGoogle Scholar
  48. Rosengren SM, Welgampola MS, Colebatch JG (2010) Vestibular evoked myogenic potentials: past, present and future. Clin Neurophysiol 121:636–651PubMedCrossRefGoogle Scholar
  49. Sans A, Highstein SM (1984) New ultrastructural features in the vestibular labyrinth of the toadfish. Opsanus tau Brain Res 308:191–195CrossRefGoogle Scholar
  50. Simpson GV, Knight RT, Brailowsky S, Prospero-Garcia O, Scabini D (1985) Altered peripheral and brainstem auditory function in aged rats. Brain Res 348:28–35PubMedCrossRefGoogle Scholar
  51. Songer JE, Eatock RA (2013) Tuning and timing in Mammalian type I hair cells and calyceal synapses. J Neurosci 33(8):3706–3724PubMedCrossRefGoogle Scholar
  52. Streubel SO, Cremer PD, Carey JP, Weg N, Minor LB (2001) Vestibular-evoked myogenic potentials in the diagnosis of superior canal dehiscence syndrome. Acta Otolaryngol Suppl 545:41–49PubMedCrossRefGoogle Scholar
  53. Todd NPM, Rosengren SM, Colebatch JG (2009) A utricular origin of frequency tuning to low-frequency vibration in the human vestibular system? Neurosci Lett 45:175–180CrossRefGoogle Scholar
  54. Tullio P (1929) Das Ohr und die Entstehung der Sprache und Schrift. Urban & Schwarzenberg, BerlinGoogle Scholar
  55. Uchino Y, Kushiro K (2011) Differences between otolith- and semicircular canal-activated neural circuitry in the vestibular system. Neurosci Res 71(4):315–327PubMedCrossRefGoogle Scholar
  56. Uchino Y, Sasaki M, Sato H, Bai R, Kawamoto E (2005) Otolith and canal integration on single vestibular neurons in cats. Exp Brain Res 164:271–285PubMedCrossRefGoogle Scholar
  57. Wei W, Jeffcoat B, Mustain W, Xu Y, Eby T, Zhu H, Tang X, Zhou W (2013) Vestibular-evoked myogenic potentials (VEMP) recorded from different sites of the sternocleidomastoid muscles in normal human subjects. J Assoc Res Otolaryngol 14(1):37–47PubMedCrossRefGoogle Scholar
  58. Welgampola MS, Carey JP (2010) Waiting for the evidence: VEMP testing and the ability to differentiate utricular vs saccular function. Otolaryngol Head Neck Surg 143:281–283PubMedCentralPubMedCrossRefGoogle Scholar
  59. Welgampola MS, Colebatch JG (2001) Vestibulocollic reflexes: normal values and the effect of age. Clin Neurophysiol 112:1971–1979PubMedCrossRefGoogle Scholar
  60. Welgampola MS, Colebatch JG (2005) Characteristics and clinical applications of vestibular-evoked myogenic potentials. Neurology 64:1682–1688PubMedCrossRefGoogle Scholar
  61. Wilson VJ, Schor RH (1999) The neural substrate of the vestibulocollic reflex: what needs to be learned. Exp Brain Res 129:483–493PubMedCrossRefGoogle Scholar
  62. Wit HP, Bleeker JD, Mulder HH (1984) Responses of pigeon vestibular nerve fibers to sound and vibration with audiofrequencies. J Acoust Soc Am 75(1):202–208PubMedCrossRefGoogle Scholar
  63. Xu Y, Simpson I, Tang X, Zhou W (2009) Acoustic clicks activate both the canal and otolith vestibulo-ocular reflex pathways in behaving monkeys. J Assoc Res Otolaryngol 10(4):569–577PubMedCentralPubMedCrossRefGoogle Scholar
  64. 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
  65. Zhou G, Cox LC (2004) Vestibular evoked myogenic potentials: history and overview. Am J Audiol 13:135–143PubMedCrossRefGoogle Scholar
  66. Zhou W, Mustain W, Simpson I (2004) Sound-evoked vestibulo-ocular reflexes (VOR) in trained monkeys. Exp Brain Res 156:129–134PubMedCrossRefGoogle Scholar
  67. Zhou W, Simpson I, Xu Y, Fong A (2005) Activity-dependent modulation: a non-linearity in the unilateral vestibulo-ocular reflex (VOR) pathways. Exp Brain Res 163:267–272PubMedCrossRefGoogle Scholar
  68. Zhou W, Xu Y, Simpson I, Cai YD (2007) Multiplicative computation in the vestibulo-ocular reflex (VOR). J Neurophysiol 97:2780–2789PubMedCrossRefGoogle Scholar
  69. Zhu H, Tang X, Wei W, Xu Y, Mustain W, Zhou W (2011a) Click-evoked responses in vestibular afferents in rats. J Neurophysiol 106(2):754–763PubMedCrossRefGoogle Scholar
  70. Zhu H, Tang X, Wei W, Mustain M, Zhou W (2011b) Air-conducted short tone bursts-evoked vestibular responses in rats. Society for Neuroscience, Program No. 579.05/FF12 Neuroscience Meeting Planner, WashingtonGoogle Scholar
  71. Zhu H, Tang X, Mustain M, Zhou W (2012) Air-conducted click-evoked responses in the vestibular nuclei of rats. Program No. 574.10/II2 Neuroscience Meeting Planner. New Orleans, Society for NeuroscienceGoogle Scholar

Copyright information

© Association for Research in Otolaryngology 2013

Authors and Affiliations

  • Hong Zhu
    • 1
    • 2
  • Xuehui Tang
    • 1
  • Wei Wei
    • 1
  • Adel Maklad
    • 2
  • William Mustain
    • 1
  • Richard Rabbitt
    • 4
    • 5
  • Steve Highstein
    • 5
  • Jerome Allison
    • 1
    • 2
  • Wu Zhou
    • 1
    • 2
    • 3
  1. 1.Department of Otolaryngology and Communicative SciencesUniversity of Mississippi Medical CenterJacksonUSA
  2. 2.Department of Neurobiology and Anatomical SciencesUniversity of Mississippi Medical CenterJacksonUSA
  3. 3.Department of NeurologyUniversity of Mississippi Medical CenterJacksonUSA
  4. 4.Department of BioengineeringUniversity of UtahSalt Lake CityUSA
  5. 5.Marine Biological LaboratoryWoods HoleUSA

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