Recent workers have claimed that bone-conducted tone bursts activate the vestibular system, producing potentials in the extraocular muscles (e.g. Jombic and Bahyl, 2005). There is also literature stating that sound can do the same.
These are called "oVEMP" responses, where the "o" stands for ocular. The term is a little ambiguus as there are many ocular muscles, that might reasonably have input from different vestibular structures. Nevertheless, it is short, and we will just use it as is conventional.
We will use the terminology "oVEMP" to denote vestibular evoked myogenic potentials elicited from the ocular muscles. When we use the terms "cVEMP" or tVEMP or whatever (e.g. gVEMP), the small letter indicates that a muscle other than the eye muscle is being monitored - - such as cervical or triceps or other skeletal muscles.
In general, one needs to consider the input, central processing, and output for physiological responses. Basically, things are very messy.
Stimulation of the otolith organ is transmitted via the vestibular nerve and nuclei and the MLF resulting in activation of the oculomotor nuclei and the extraocular muscles. (Kantner, Gurkov, 2012. )
Input for the oVEMP:
The vibration stimuli as well as sound stimuli that are used to elicit oVEMPs excite many structures -- the cochlea, the otoliths, the semicircular canals, proprioceptive input, so there are many choices for input.
There is some evidence that these are utricular in origin. (Manzari et al, 2012a). Curthoys et al (2016) reported in guinea pigs that both bone and air conducted inputs causes "phase locking" of afferents in both the utricle and saccule, and furthermore that this produces a limit on neural firing. Phase locking occurs up to 1500 for bone and 3000 for air, implying that guinea pig afferents can fire as high as 3000 spikes/second (thats very high !). On the other hand, phase locking at low frequencies (i.e. 100 hz) limits responses, presumably because afferents cannot fire less than about 100 spikes/sec. Fife et al (2017) stated that "it is not known whether oVEMP/cVEMP responses accurately identify vestibular function specifically related to the saccule/utricle". We think this is fair, as of 2017. We have unproven claims.
Sound can excite the semicircular canals as well as the utricle, and does this especially so in SCD (superior canal dehiscence). The corallary is that sound (in disease states), could excite the superior canal, and cause a VOR in the vertical eye muscles -- including the inferior rectus and inferior oblique. This means that the input AND output might be different in disease than in normal subjects.
If oVEMPS are indeed utricular, they should enter the brain through the superior vestibular nerve. If oVEMPS also have some saccule component, there could also be some input through the inferior vestibular nerve. Of course, if one considers the multiple other structures that can be activated by sound (i.e. the cochlea, the semicircular canals), or vibration (i.e. all of the above plus proprioceptors), there are a large number of potential generators for oVEMPS, that might vary according to whether one is working with a normal individual or a patient with pathology.
Chihara et al (2009) reported that oVEMPs do not require either a cochlear or facial nerve. This does not mean that oVEMPs have no input at all from these nerves, but merely that it is not required. In other words, cochlear and facial nerves are not necessary. They may still be sufficient. Similarly, oVEMPs do not require an eyeball.
According to Naranjo, VEMP amplitudes are increased by threat and fear (Naranjo et al, 2016) showing that there are also other inputs to consider. The implication is that cVEMPs are not simple saccule reflexes, but have multiple inputs. This could also be the cases for oVEMPs.
According to Oh et al (2016), the ocular VEMPs (oVEMPs) reflect the function of the vestibular nuclei and the crossed vestibulo-ocular reflex (VOR) pathways, mostly contained in the medial longitudinal fasciculus (MLF). Therefore, lesions involving the vestibular nuclei can present abnormalities of both cVEMPs and oVEMPs. The medullary lesions involving the descending MLF or the spinal accessory nucleus impair cVEMPs. In contrast, the lesions involving the MLF, the crossed ventral tegmental tract, oculomotor nuclei and the interstitial nucleus of Cajal can impair oVEMPs.
The output system for oVEMPs is the surface EMG under the eyes. It is generally assumed that the output is the extraocular muscles. For the central signal to activate the extraocular muscles, it must traverse one or more of the oculomotor nerves (3,4,6), and the neuromuscular junction of the eye muscle (s). Logic would suggest that the inferior oblique muscle is the one that is being picked up by the usual electrode placement.
If sound were exciting other structures than the utricle, such as the superior semicircular canal (which happens), then one would expect that there would be vestibular ocular reflexes in all of the muscles measured by the oVEMP (i.e. inferior oblique, inferior rectus), and laterality would be gone as well. In other words, one could not depend on the left eye reflecting the output of the right utricle.
Other factors. The oVEMP is a tiny response and the person interpreting the test has a strong influence on oVEMP latency and amplitude (Ertl et al, 2016). This is not the case for cVEMPs. This suggests that oVEMP studies could easily be affected by bias, and that ideally they should use blinded interpreters.
Fife et al (2017) published a review of VEMP usage including methodology of oVEMP.
Ovemp methodology from Katner and Gurkov, 2012.
The input signal for an oVEMP is either sound or vibration, and the output is the response triggered average of EMG from the ocular muscles -- generally those just under the eye. While oVEMPs were developed using bone vibration, as of 2017, the most common method of eliciting oVEMPs is with sound, in a way similar to cVEMPs. The best frequency of sound is reportedly similar to cVEMPs, about 500 Hz, but Piker et al (2013) suggested that 750 or 1000 might be attempted in older adults. In Piker et al (2013), 750 was the best frequency overall, and one would wonder why not just use 750.
For the bone stimulus, subjects are positioned lying supine and looking upward, and undergo repeated applications of the stimulus through a source of vibration, commonly a "minishaker". Some studies are done using a B71 bone vibrator. A "minishaker" such as the Bruel and Kjer 4810 is a common method of providing a vibration input. The much cheaper bone oscillator, such as the Radioear B-71, is not sufficiently loud to produce a reliable output (Iwasaki et al, 2008). Obviously, for bone vibration, both ears are being stimulated at the same time, and one must hope that the "wiring" is unilateral and not partially crossed as nearly everything else in the brainstem seems to be. So in other words, for clinical use, the air input seems more logical.
For either method, the electrodes are placed under the eye, with the goal of recording EMG activity from the inferior oblique muscle. Becuse the inferior oblique is located under the eyeball, it is activated by looking upward. The inferior rectus is relaxed. Although the superior rectus is also activated, it is on the other side of the eye-socket. Thus the idea is that one is mainly measuring the inferior oblique. These are small muscles and likely rather sensitive to electrode placement.
oVEMPS are not due to the corneoretinal potential used for ENG testing. This is a DC potential that is filtered out by the oVEMP amplifier settings.
oVEMP obtained in a patient using sound. The latency here is 11-12 msec, and the amplitude is only 2.5-7.5 uV
This produces a rather small (compared to the cervical VEMP) potential, at about 10 msec (i.e. a shorter latency than the cervical or triceps VEMPs).
oVEMPS can be elicited as early as the age of 3 years old, making them potentially a good test to use for vesibular assessment in children (Young, 2015). One does have the problem here of getting the child to look upward.
Venhovens et al (2015) reported that oVEMP amplitudes have fair-good test-retest reliability, but latencies had a poor reliability (when repeated 1 week later). This would suggest that latencies are not a good parameter for diagnosis.
Mattingly et al (2015) reported a single case of bilateral hearing loss immediately after oVEMP and cVEMP testing. They suggested limits for sound exposure for VEMPS. Practically, we do not think that the risk is high in as much as persons who operate loud construction equipment do not generally have significant risk for sudden hearing loss. Noise exposure is very well studied and we see this case as an unfortunate event alone.
Iwasaki et al (2008) reported that oVEMPS are asymmetrical when stimuli are presented in the midline, and simultaneous recordings are made from each eye. From other studies of oVEMPS, one would think that this protocol would be less sensitive than AC oVEMPS.
Other methods of eliciting oVEMPs:
- Huang et al (2011) reported that oVEMPS can be recorded with eyes closed rather than eyes open/looking upward. We find this implausible. We wonder what they are measuring.
- Walther et al (2016) reported that using "CHIRP" stimuli is more effective than click or short tone bursts. This seems reasonable.
- Versino et al (2015) reported using bilateral stimulation to elicit oVEMP. While the idea is a reasonable one, these authors reported extremely low values for their oVEMP amplitudes (about 1 uV), and more study is needed to understand why their data is so different than others in the literature. The most important issue with bilateral stimulation relates to whether or not there is interaction between the ears, and also whether the protocol provides the same results as unilateral stimulation. We would say that this paper doesn't answer either of these questions.
- Manzari et al (2013) reported on using 4000 Hz stimuli, either air or bone. They wrote "Here we report a 1-trial indicator: that the oVEMP n10 in response to a very high frequency stimulus (4000 Hz), either air-conducted sound (ACS) or bone conducted vibration (BCV), is such a fast indicator of probable SCD." This procedure is simply a threshold type VEMP (either potential is present or not), using a frequency threshold rather than an amplitude. We are not sure that this method adds anything to the conventional method of using amplitude criteria for dection of SCD by oVEMP. Furthermore, Noij et al (2018) commented that "intense 4000-Hz tones can be very uncomfortable". We also think that the high frequency method does not address the question as to whether or not utricular function is normal.
Obvious technical pitfalls in oVEMPS.
There are a HUGE number of issues with oVEMP studies -- both technical as well as methodological.
A common logical lapse in procedures used to measure oVEMPs is lack of a method of calibrating the surface EMG. As far as we tell, the present attititude in the literature is just to live with the logical lapse, presumably thinking that it is better to do the test than not test at all. Because the eye muscles are much smaller than the neck muscles, there is less "wiggle-room" to make a mistake with electrode positioning with oVEMPs, compared to cVEMPs.
Another logical issue is that there is generally no method of being sure that the patient is cooperating with the oVEMP and keeping their eyes positioned upward. Again, researchers seem to take the general approach that it is better to do this fairly simple test and see how it works without controlling for obvious technical problems. Patients with nystagmus may not be able to do this, and for this reason, have no oVEMP (Yang et al, 2017).
A third logical problem is that studies are generally not blinded -- allowing for the possibility of bias. This is typical of an "early" adopter research base.
A fourth problem is that in disease (such as SCD or cholesteatoma), the semicircular canals may be sensitive to sound as well, which would make most of the assumptions about this being a contralateral utricular response go out the window.
A fifth problem is that in disease, the central wiring of VEMPs may be different. After all, what is going in is sound, not movement. Why couldn't sound be a sufficient stimulus by itself in persons with clear vestibular loss, and not require utricular stimulation ?
A 6th problem is that oVEMPs are usually done sitting upright, and the brain's weight on the dura may "autoplug" an open superior canal. This issue has not been dealt with in any great detail. It is not a problem with cVEMPs done supine (but some people do them upright -- a bad idea in our opinion).
One can also broadly criticize all studies of VEMPs in that the core dogma driving the enthusiasm in doing VEMP tests is implausible. The core dogma is that things are very simple, allowing one to make diagnostic inferences. While not emphasized much in the enthusiast literature, VEMP tests likely involve input from many senses, and are not confined to saccule or utricle inputs as has been suggested. It is also implausible that the wiring is completely "unilateral", and especially so in the very patients we are attempting to diagnose. Thus we have a substantial clinical database concerning oVEMPs that has not produced very impressive results, perhaps based on oversimplified ideas about how the ear is wired up to the nervous system.
A discussion of normal values for oVEMPs is found here.
The brief answer is that oVEMP amplitude averages about 5uV, and amplitude declines with age. oVEMP amplitudes are skewed with a long tail at higher values. Only 2% of oVEMP amplitudes in most people are > 20uV, but it seems likely that there are a few more in the young.
What data is there concerning particular disorders in the literature ?
The VEMP literature is rapidly increasing and it seems that there are considerable valuable diagnostic information to be obtained.
In the pages below, we review papers claiming a utility for VEMPs, convering both cVEMPs and oVEMPs. This is a difficult task as the literature is growing rapidly. One would think that AC oVEMPS would generally perform better for localization than BC oVEMPS, as the stimulus is confined to one ear. We think it is a very bad idea (for diagnosis) to use a BC stimulus, as one does not know what is being activated.
Probably the main reason to do oVEMPs is to diagnose SCD. These oVEMPs can be amazingly clear.
oVEMP obtained in a patient using sound. The right ear has clear SCD on temporal bone CT scan.
- Superior canal dehiscence
- Vestibular nerve disorders
- Ramsay Hunt
- Vestibular Neuritis
- Acoustic Neuroma
- failed VNS
- Bilateral vestibular loss (such as due to gentamicin)
- Benign paroxysmal positional vertigo (BPPV)
- Central vestibular disorders
- Meniere's disease
- Hearing disorders
- Acoustic trauma
Below is a discussion of entities not covered in the pages above.
Bayram et al (2015) found no difference between amplitude ratio and thresholds in patients with Behcet's. This has little significance given the rarity of Behcet's.
Taylor et al (2012) reported that increased oVEMPs, compared to normal VEMPS, were found in a single patient with bilaterally enlarged vestibular aqueducts. Interesting I suppose, but this obviously needs to be confirmed with, lets say, 10 cases.
Bottcher et al (2016) reported that one third of 25 patients with suspected NPH had impaired otolith function. "Responders to STT only had a significant increase of oVEMP and thereby utricular input, probably due to a decrease of pressure. " We would wonder in this study if the age group being tested might not have VEMPs at all, as VEMPs are reduced with age.
Spinocerebellar degeneration (i.e. a variant of central vestibular disorder).
Riberio et al (2015) reported in 14 Machado-Joseph disease patients that 13/14 had various abnormalities in cVEMP or oVEMP. They included timing, amplitude and asymmetry among their "abnormalities". Given the rather broad nature of this report, somewhat of a fishing expedition, we think more work needs to be done.
One would think that oVEMPs would be the perfect test for unilateral utricular disease, but we have a catch-22 here -- we have no practical way of diagnosing unilateral utricular disease aside from oVEMPs, and because of this, we cannot use one to calibrate the other. In other words, another example of the "circular reasoning" that is abundant in the VEMP literature.
Schaaf et al (2013) attempted to correlate oVEMP tests with several other maneuver ("Turn over" test, and Subjective vertical). They reported about 63% agreement among these three maneuvers.
References: Journals that have links are those with low scores for quality or other issues concerning their reliability
- Bayram, A., et al. (2015). "Cervical and ocular vestibular evoked myogenic potentials in Behcet's disease." Am J Otolaryngol 36(4): 503-508.
- Bottcher, N., et al. (2016). "Normal pressure hydrocephalus: Increase of utricular input in responders to spinal tap test." Clin Neurophysiol 127(5): 2294-2301.
- Chen, Y. J. and Y. H. Young (2016). "Secondary Endolymphatic Hydrops After Acoustic Trauma." Otol Neurotol.
- Chihara, Y., et al. (2007). "Vestibular-evoked extraocular potentials by air-conducted sound: another clinical test for vestibular function." Clin Neurophysiol 118(12): 2745-2751.
- Chihara, Y., et al. (2009). "Ocular vestibular-evoked myogenic potentials (oVEMPs) require extraocular muscles but not facial or cochlear nerve activity." Clinical neurophysiology 120(3): 581-587.
- Curthoys, I. S., et al. (2016). "The response of guinea pig primary utricular and saccular irregular neurons to bone-conducted vibration (BCV) and air-conducted sound (ACS)." Hear Res 331: 131-143.
- Ertl, M., et al. (2016). "On the impact of examiners on latencies and amplitudes in cervical and ocular vestibular-evoked myogenic potentials evaluated over a large sample (N = 1,038)." Eur Arch Otorhinolaryngol 273(2): 317-323.
- Fife, T. D., et al. (2017). "Practice guideline: Cervical and ocular vestibular evoked myogenic potential testing:." Neurology 89(22): 2288-2296.
- Huang, Y. C., et al. (2011). "Feasibility of ocular vestibular-evoked myogenic potentials (oVEMPs) recorded with eyes closed." Clinical neurophysiology :
- Iwasaki, S., et al. (2008). "Ocular vestibular evoked myogenic potentials in response to bone-conducted vibration of the midline forehead at Fz. A new indicator of unilateral otolithic loss." Audiology & neuro-otology 13(6): 396-404.
- Iwasaki, S., et al. (2008). "Ocular vestibular evoked myogenic potentials to bone conducted vibration of the midline forehead at Fz in healthy subjects." 119(9): 2135-2147.
- Iwasaki, S., et al. (2010). "Ocular vestibular evoked myogenic potentials to bone-conducted vibration in vestibular schwannomas." Otology & neurotology : 31(1): 147-152.
- Jombik, P. and V. Bahyl (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(2): 222-228.
- Jombik, P., et al. (2011). "Direction-dependent excitatory and inhibitory ocular vestibular-evoked myogenic potentials (oVEMPs) produced by oppositely directed accelerations along the midsagittal axis of the head." Experimental brain research. Experimentelle Hirnforschung. Experimentation cerebrale 211(2): 251-263.
- Kantner, C. and R. Gurkov (2012). "Characteristics and clinical applications of ocular vestibular evoked myogenic potentials." Hear Res 294(1-2): 55-63.
- Li, C., et al. (2015). "Epidemiology of vestibular evoked myogenic potentials: Data from the Baltimore Longitudinal Study of Aging." Clin Neurophysiol 126(11): 2207-2215.
- Manzari L, Burgess AM, Curthoys IS.Ocular and cervical vestibular evoked myogenic potentials in response to bone-conducted vibration in patients with probable inferior vestibular neuritis. J Laryngol Otol. 2012 Jul;126(7):683-91. doi: 10.1017/S0022215112000692. Epub 2012 May 15.
- Mattingly, J. K., et al. (2015). "Sudden Bilateral Hearing Loss After Cervical and Ocular Vestibular Evoked Myogenic Potentials." Otol Neurotol 36(6): 961-964.
- McNerney KM, Burkard RF. The vestibular evoked myogenic potential (VEMP): air- versus bone-conducted stimuli. Ear Hear. 2011 Nov-Dec;32(6):e6-e15.
- Murofushi, T., et al. (2016). "Is otolithic vertigo accompanied by hearing loss caused by sacculocochlear endolymphatic hydrops?" Acta Otolaryngol 136(1): 38-42.
- Murnane, O. D., et al. (2011). "Effects of stimulus and recording parameters on the air conduction ocular vestibular evoked myogenic potential." J Am Acad Audiol 22(7): 469-480.
- Naranjo, E. N., et al. (2016). "Vestibulo-spinal and vestibulo-ocular reflexes are modulated when standing with increased postural threat." J Neurophysiol 115(2): 833-842.
- Noij, K. S., et al. (2018). "Toward Optimizing cVEMP: 2,000-Hz Tone Bursts Improve the Detection of Superior Canal Dehiscence." Audiol Neurootol 23(6): 335-344.
- Taylor, R. L., A. P. Bradshaw, et al. (2012). "Augmented ocular vestibular evoked myogenic potentials to air-conducted sound in large vestibular aqueduct syndrome." Ear Hear 33(6): 768-771.
- Park, H. J., et al. (2010). "Frequency-tuning characteristics of cervical and ocular vestibular evoked myogenic potentials induced by air-conducted tone bursts." Clin Neurophysiol 121(1): 85-89.
- Piker, E. G., et al. (2011). "Normal characteristics of the ocular vestibular evoked myogenic potential." J Am Acad Audiol 22(4): 222-230.
- Piker, E. G., et al. (2013). "Effects of Age on the Tuning of the cVEMP and oVEMP." Ear Hear.
- Piker, E. G., et al. (2015). "Assessment of the Clinical Utility of Cervical and Ocular Vestibular Evoked Myogenic Potential Testing in Elderly Patients." Otol Neurotol 36(7): 1238-1244.
- Ribeiro, R. S., et al. (2015). "Cervical and ocular vestibular evoked potentials in Machado-Joseph disease: Functional involvement of otolith pathways." J Neurol Sci 358(1-2): 294-298.
- Rosengren, S. M., et al. (2011). "Ocular and cervical vestibular evoked myogenic potentials produced by air- and bone-conducted stimuli: comparative properties and effects of age." Clin Neurophysiol 122(11): 2282-2289.
- Schaaf, H., et al. (2013). "[Utricular function. Correlation of three investigations carried out in routine practice]." HNO 61(8): 692-698. (This is written in German).
- Sung P, Cheng P, Young Y. Effect of gender on ocular vestibular-evoked myogenic potentials via various stimulation modes. Clin Neurophys 122 (2011), 183-187
- Venhovens, J., et al. (2015). "Ocular and Cervical Vestibular Evoked Myogenic Potentials (VEMPs) in healthy volunteers: the intra-, interobserver, and the test re-test reliability." J Vestib Res 25(3-4): 161-167.
- Young, Y. H. (2015). "Assessment of functional development of the otolithic system in growing children: a review." Int J Pediatr Otorhinolaryngol 79(4): 435-442.
- Yang TH, Chen HL, Young YH.Pathological eye movements influence on the recordings of ocular vestibular-evoked myogenic potential. Acta Otolaryngol. 2017 Aug;137(8):807-813. doi: 10.1080/00016489.2017.1286037. Epub 2017 Mar 21
- Versino, M., et al. (2015). "Ocular vestibular evoked myogenic potentials in response to air-conducted 500 Hz short tones: Effect of stimulation procedure (monaural or binaural), age and gender." J Vestib Res 25(3-4): 143-149.
- Walther, L. E. and M. Cebulla (2016). "Band limited chirp stimulation in vestibular evoked myogenic potentials." Eur Arch Otorhinolaryngol.