By Marcello Cherchi, MD PhD
For clinicians
Georg von Békésy’s observation in 1935 (von Békésy 1935) that applying vibration to various locations on the skull could alter vestibular perception has been replicated (Betts et al. 2000) many times, and is sometimes referred to as the “propriogyral illusion.”(Lackner and Levine 1979) But that actual nystagmus could be induced by applying vibration to the neck was first demonstrated by Lücke in 1973.(Lücke 1973) Subsequent studies have investigated its occurrence, clinical significance, and mechanisms (Choi et al. 2007; Dumas et al. 2007; Hamann and Schuster 1999; Karlberg et al. 2003; Michel et al. 2001; Ohki et al. 2003; Park, Shin, Shim 2007; Perez 2003; Ulmer, Chays, Bremond 2004; Xie et al. 2006). We describe here the technique involving a lateralized application of vibration to the neck or mastoid. Stimulation at the midline (midfrontal, vertex, etc.) has also been studied but is not used in most clinical laboratories.
Vibration-induced nystagmus (VIN) can be elicited by applying low-frequency vibration to the neck or mastoid area. A common technique is as follows: The patient seated upright and instrumented with electronystagmography (ENG), videonystagmography (VNG) or video Frenzel oculography (VFO) so that eye movements can be observed in the dark, avoiding fixation suppression. Direct visualization, or using optical Fresnel lenses, are not sufficient. Spontaneous nystagmus is recorded for at least 10 seconds in complete darkness to obtain a baseline. Next, a source of low-frequency vibration, is firmly applied to the neck over the belly of the sternocleidomastoid muscle. A recent review (Dumas et al. 2017) notes that vibration frequencies from 40 Hz – 150 Hz have been studied; occasional studies use higher frequencies (e.g., 500 Hz (Aw et al. 2011) to 800 Hz (Dumas et al. 2019), though for skull vibration); many laboratories use 100 Hz but this has not been standardized. The location of the vibration is not critical as long as there is a firm connection between the vibrator and the muscle. During the vibration, the eyes are observed for nystagmus. Ten seconds of vibration is adequate. After eye movements are recorded with vibration applied to one side, the source of vibration is moved to the other side.
Vibration-induced nystagmus is commonly observed in patients with vestibular asymmetry (such as a person who has had vestibular neuritis, removal of a vestibular schwannoma, or treatment with intratympanic gentamicin) (Hamann and Schuster 1999). In these contexts, vibration on either side of the neck provokes a modest (about 5 deg/sec) horizontal nystagmus whose fast phase beats towards the intact side. People with symmetrical vestibular function — whether normal subjects (with symmetrical and intact vestibulo-ocular reflexes), or patients with bilateral weakness (in whom the deficiency is symmetrical) — often have no VIN. Some normal subjects have a direction-changing VIN that can be either ipsiversive (fast phase beating towards the side of vibration) or contraversive (fast phase beating away from the side of vibration) (Popov et al. 1999). One study (Perez 2003) found VIN in a surprising 81.6% (31 out of 38) normal subjects, but added that the magnitude of the nystagmus did not exceed 2.8 deg/sec.
In some patients with unilateral vestibular weakness the VIN may additionally have a torsional component, or be exclusively torsional. Presumably this is due to involvement of utricular afferents.
Variations in technique of the vibration test mainly involve the location of the vibration. Vibration may be applied to the bony prominences around the ear with the mastoid process being the most favored (but this is loud and can therefore introduce the confounding effect of additionally eliciting Tullio’s phenomenon in patients with perilymphatic fistulae or third window syndromes), or may be applied to the posterior neck rather than the anterior neck muscles (Dumas et al. 2003).
Hypothetical mechanisms (Cherchi and Hain 2009) for VIN fall into three general categories: (1) direct generation by the neck (“cervical nystagmus”), perhaps through proprioceptors, (2) generation from the inner ear itself, and (3) through an interaction between the neck and central vestibular processing (“neck fixation”).
The first hypothesis, namely that vibration-induced nystagmus is generated from the neck, relies on the observation that vibration stimulates neck proprioceptors (Burke et al. 1976; Karlberg et al. 2003; Roll, Vedel, Ribot 1989). This hypothesis does not account for the reliable directionality of VIN.
The second hypothesis, namely that VIN is generated from the inner ear, is based on the idea that vibration stimulates labyrinthine structures (Karlberg et al. 2003), including the semicircular canals and the otolith organs (Christensen-Dalsgaard and Narins 1993; Hudspeth 1989; Ulmer, Chays, Bremond 2004; Wit, Bleeker, Mulder 1984; Young, Fernandez, Goldberg 1977). Karlberg and colleagues (Karlberg et al. 2003), citing work from Hudspeth (Hudspeth 1989), describes this logic as follows: “Most [vestibular hair] cells show saturation in the negative stimulus direction but no abrupt or complete saturation for positive stimuli. Thus, movements of the hair bundle toward the kinocilium will depolarize the cell more than movements of the same amplitude in the opposite direction will hyperpolarize it. The net effect of an oscillating mechanical stimulus to a hair bundle will be excitatory.” If this hypothesis were true (and if it were the only mechanism at play), then since vibration acts more powerfully on the side on which the vibration is applied, one would expect that this would temporarily induce a vestibular asymmetry in normal subjects and thereby elicit nystagmus beating towards the ear being stimulated, as well as greater nystagmus in patients with unilateral loss for stimulation on the intact side. VIN is usually generated equally well from vibration on either sternocleidomastoid, but the patterns predicted above are seen in some subjects. Accordingly, there is some plausibility to this hypothesis, and it may account for VIN in some patients.
The third hypothesis, namely that VIN results from an interaction between neck and central vestibular processing (specifically from the release of neck fixation), is based on the idea that the vestibular system is merely one of multiple sensory inputs to central circuits that estimate one’s orientation in space and generate compensatory movements. Vision and ankle proprioception are sensory inputs that are most commonly considered as part of the somatosensory integration process, but some suggest that in order for input from the vestibular system (situated in the head) to be properly used to stabilize the body, the position of the neck on the trunk is critical as it defines a coordinate transformation (Nashner and Wolfson 1974). By the same reasoning, neck input may be helpful in the brain’s determination of whether or not the head is moving; if the neck muscles’ inputs are stable, then the head is probably stationary (with respect to the trunk). Thus, the neck fixation hypothesis conjectures that the central vestibular system can conclude that the head is not moving in space when the neck is unstimulated, and therefore can suppress spontaneous nystagmus. Additional evidence in support of this hypothesis comes from data suggesting that cervical afferents influence the velocity storage mechanism(Karlberg and Magnusson 1996) and interposed nuclei of the cerebellum (Luan et al. 2013). Overall we find this hypothesis more plausibly explains the findings observed in VIN.
References
Aw ST, Aw GE, Todd MJ, Bradshaw AP, Halmagyi GM (2011) Three-dimensional vibration-induced vestibulo-ocular reflex identifies vertical semicircular canal dehiscence. J Assoc Res Otolaryngol 12: 549-58. doi: 10.1007/s10162-011-0274-3
Betts GA, Barone M, Karlberg M, MacDougall H, Curthoys IS (2000) Neck muscle vibration alters visually-perceived roll after unilateral vestibular loss. Neuroreport 11: 2659-2662. doi: PMID: 10976939
Burke D, Hagbarth KE, Lofstedt L, Wallin BG (1976) The responses of human muscle spindle endings to vibration of non-contracting muscles. J Physiol 261: 673-93.
Cherchi M, Hain TC (2009) Provocative maneuvers for vestibular disorders. In: Eggers S, Zee D (eds) Vertigo and Imbalance: Clinical Neurophysiology of the Vestibular System. Elsevier, Amsterdam, pp 111-134
Choi KD, Oh SY, Kim HJ, Koo JW, Cho BM, Kim JS (2007) Recovery of vestibular imbalances after vestibular neuritis. Laryngoscope 117: 1307-12. doi: 10.1097/MLG.0b013e31805c08ac
Christensen-Dalsgaard J, Narins PM (1993) Sound and vibration sensitivity of VIIIth nerve fibers in the frogs Leptodactylus albilabris and Rana pipiens pipiens. J Comp Physiol [A] 172: 653-62.
Dumas G, Curthoys IS, Lion A, Perrin P, Schmerber S (2017) The Skull Vibration-Induced Nystagmus Test of Vestibular Function-A Review. Front Neurol 8: 41. doi: 10.3389/fneur.2017.00041
Dumas G, De Waele C, Hamann KF, Cohen B, Negrevergne M, Ulmer E, Schmerber S (2007) [Skull vibration induced nystagmus test.]. Ann Otolaryngol Chir Cervicofac.
Dumas G, Perrin P, Schmerber S, Lavieille JP (2003) [Nystagmus and vibration test research of mechanisms, theoretical methods: on 52 cases of unilateral vestibular lesions]. Rev Laryngol Otol Rhinol (Bord) 124: 75-83.
Dumas G, Tan H, Dumas L, Perrin P, Lion A, Schmerber S (2019) Skull vibration induced nystagmus in patients with superior semicircular canal dehiscence. Eur Ann Otorhinolaryngol Head Neck Dis. doi: 10.1016/j.anorl.2019.04.008
Hamann KF, Schuster EM (1999) Vibration-induced nystagmus – A sign of unilateral vestibular deficit. ORL J Otorhinolaryngol Relat Spec 61: 74-79. doi: PMID: 10095196
Hudspeth AJ (1989) Mechanoelectrical transduction by hair cells of the bullfrog’s sacculus. Prog Brain Res 80: 129-35; discussion 127-8. doi: 10.1016/s0079-6123(08)62206-2
Karlberg M, Aw ST, Black RA, Todd MJ, MacDougall HG, Halmagyi GM (2003) Vibration-induced ocular torsion and nystagmus after unilateral vestibular deafferentation. Brain 126: 956-64. doi: PMID: 12615651
Karlberg M, Magnusson M (1996) Asymmetric optokinetic after-nystagmus induced by active or passive sustained head rotations. Acta Otolaryngol 116: 647-51. doi: 10.3109/00016489609137903
Lackner JR, Levine MS (1979) Changes in apparent body orientation and sensory localization induced by vibration of postural muscles: vibratory myesthetic illusions. Aviat Space Environ Med 50: 346-54.
Luan H, Gdowski MJ, Newlands SD, Gdowski GT (2013) Convergence of vestibular and neck proprioceptive sensory signals in the cerebellar interpositus. J Neurosci 33: 1198-210a. doi: 10.1523/JNEUROSCI.3460-12.2013
Lücke K (1973) [A vibratory stimulus of 100 Hz for provoking pathological nystagmus]. Z Laryngol Rhinol Otol 52: 716-720. doi: PMID: 4766429
Michel J, Dumas G, Lavieille JP, Charachon R (2001) Diagnostic value of vibration-induced nystagmus obtained by combined vibratory stimulation applied to the neck muscles and skull of 300 vertiginous patients. Rev Laryngol Otol Rhinol (Bord) 122: 89-94.
Nashner LM, Wolfson P (1974) Influence of head position and proprioceptive cues on short latency postural reflexes evoked by galvanic stimulation of the human labyrinth. Brain Res 67: 255-268. doi: PMID: 4470421
Ohki M, Murofushi T, Nakahara H, Sugasawa K (2003) Vibration-induced nystagmus in patients with vestibular disorders. Otolaryngol Head Neck Surg 129: 255-258. doi: PMID: 12958576
Park H, Shin J, Shim D (2007) Mechanisms of vibration-induced nystagmus in normal subjects and patients with vestibular neuritis. Audiol Neurootol 12: 189-97.
Perez N (2003) Vibration induced nystagmus in normal subjects and in patients with dizziness. A videonystagmography study. Rev Laryngol Otol Rhinol (Bord) 124: 85-90.
Popov KE, Lekhel H, Faldon M, Bronstein AM, Gresty MA (1999) Visual and oculomotor responses induced by neck vibration in normal subjects and labyrinthine-defective patients. Exp Brain Res 128: 343-52.
Roll JP, Vedel JP, Ribot E (1989) Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study. Exp Brain Res 76: 213-22.
Ulmer E, Chays A, Bremond G (2004) [Vibration-induced nystagmus: mechanism and clinical interest]. Ann Otolaryngol Chir Cervicofac 121: 95-103.
von Békésy G (1935) Über akustische Reizung des Vestibularapparates. Arch Ges Physiol 236: 59-72. doi: https://doi.org/10.1007/BF01752324
Wit HP, Bleeker JD, Mulder HH (1984) Responses of pigeon vestibular nerve fibers to sound and vibration with audiofrequencies. J Acoust Soc Am 75: 202-8.
Xie SJ, Yang WY, Zhang SZ, Wu ZM, Chen YS, Jia HB, Zhou N, Ji F (2006) [Clinical significance of vibration-induced nystagmus in patients with unilateral peripheral vestibular disorders]. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 41: 736-9.
Young ED, Fernandez C, Goldberg JM (1977) Responses of squirrel monkey vestibular neurons to audio-frequency sound and head vibration. Acta Otolaryngol 84: 352-60.
