Why do oVEMPs become larger when you look up? Explaining the effect of gaze elevation on the ocular vestibular evoked myogenic potential
Highlights
► Gaze elevation significantly increases oVEMP amplitude, while gaze depression decreases amplitude and prolongs latency. ► This gaze effect is primarily due to changes in tonic eye muscle activity, while the contribution of changes in muscle-electrode distance is significant but small. ► oVEMPs recorded from below the eyes originate mainly in the inferior oblique muscle during up-gaze and in the inferior rectus muscle during down-gaze.
Introduction
The ocular vestibular evoked myogenic potential (oVEMP) is a recently-described, vestibular-dependent reflex recorded from the extraocular muscles in humans (see Rosengren et al., 2010 for review). It is elicited by vestibular stimulation with vibration or loud sounds and is recorded from surface electrodes placed near the eyes. The oVEMP is part of the vestibulo-ocular reflex (VOR), as it represents the muscle activity that underlies a vestibular-evoked eye movement: it is, however, independent of the electrical activity generated by the corneoretinal dipole of the eye (i.e. the electro-oculogram, EOG; Todd et al., 2007, Welgampola et al., 2009). The reflex is best measured during up-gaze from electrodes placed below the eyes, as it is largest and most consistent under these conditions (e.g. Iwasaki et al., 2009, Rosengren et al., 2005). When thus measured, the oVEMP consists of a series of waves, beginning with a negativity which peaks at around 10 ms (n10). This potential is a ‘crossed’ reflex, i.e. recorded in the eye contralateral to the stimulated ear (Iwasaki et al., 2007), and is thought to be mediated by otolith fibres, as animal studies have shown that otolith afferents are preferentially activated by vibration and sound (Curthoys et al., 2006, Murofushi and Curthoys, 1997). As the n10 component of the reflex is abolished in patients with vestibular loss, the oVEMP has been introduced as a clinical test of otolith function.
Although many extraocular muscles may be activated by otolith stimulation, when recorded from beneath the eyes, the n10 response appears to originate in the inferior oblique (IO) muscle. We recently investigated the myogenic origin of the oVEMP by recording the motor unit activity of the extraocular muscles located closest to the recording site: the IO and inferior rectus (IR) muscles (Weber et al., 2012). The results showed a series of increases and decreases of IO motor unit discharge, beginning with an excitation of the muscle at approximately 10 ms. The IR was also excited, but the first peak of activity occurred later at about 15 ms. This demonstrated that, although both muscles are activated by the oVEMP stimulus, the n10 potential originates in the IO muscle and is excitatory, as predicted from its surface polarity (Colebatch and Rothwell, 2004).
An important property of the oVEMP is that its amplitude increases with up-gaze and decreases with down-gaze (Govender et al., 2009). Two hypotheses have been proposed to explain this: the first attributes the change in amplitude to movement of the IO muscle belly relative to the recording electrodes, while the second attributes the effect to changes in tonic activation of the IO at different vertical gaze angles (e.g. Chou et al., 2009, Govender et al., 2009, Huang et al., 2012, Iwasaki et al., 2008, Rosengren et al., 2005, Welgampola et al., 2009). The size of any potential can be expected to increase as the distance between the source and the electrodes is decreased. On the other hand, tonic activity of the muscle is an important contributor to the amplitude of the cervical VEMP (cVEMP), a similar (but inhibitory) short-latency vestibular reflex measured from the neck muscles (Colebatch et al., 1994, Lim et al., 1995). As the main actions of the IO are extorsion and elevation, the IO is activated during up-gaze. However, the demands on the VOR are different to those on postural muscles, and it is not clear whether reflexes elicited in the extraocular muscles can be expected to share the same properties.
As Demer et al. (2003) have measured the actual displacement of the IO muscle during changes in vertical gaze, it is possible to use this information to estimate the effect of muscle displacement relative to the recording electrodes. They used magnetic resonance imaging to compare the antero–posterior position of the IO at the point where it crosses the inferior rectus muscle during different levels of vertical gaze. Since the IO is maximally activated in up-gaze with adduction and inhibited in down-gaze with abduction, Demer et al. (2003) recorded the eyes in these positions as well as in neutral position. As the eye rotated from the down-gaze to the up-gaze position, the IO muscle belly moved 4.3 mm anteriorly with little change in vertical position. In the current study, we used the same gaze positions as Demer et al. (2003) to modulate oVEMP amplitude. We then simulated a 4.3 mm muscle displacement by systematically moving the recording electrodes away from the muscle while holding gaze (and therefore muscle position and activity) constant. If muscle displacement principally determined the gaze effect, we would expect to see a similar decrement in oVEMP amplitude with increasing electrode distance as occurs with the corresponding decreased gaze angle. Conversely, if muscle activity were more important, we would expect a greater modulation with vertical gaze change than with electrode displacement.
Section snippets
Subjects
Ten normal volunteers, with no history of vestibular or neurological disease, participated (3 female, 7 males; age range 26–48 years). The participants gave written informed consent according to the Declaration of Helsinki and the study was approved by the local ethics committee (Kantonale Ethik-Kommission Zurich, 2010-0177/3).
Stimulation and recording parameters
The oVEMP stimulus was a 500 Hz, 4 ms burst of vibration delivered with a hand-held minishaker positioned over the hairline near Fz (i.e. an unshaped sinusoid, delivered at
Results
We analysed the responses from the upper recording electrode in the referential montage to maximise the reliability of measurements in individual subjects. The responses recorded using the referential and bipolar electrode montages were very similar, but the referential montage produced responses approximately twice as large (Fig. 2).
Discussion
Our results clearly demonstrate that the effect of vertical gaze on the oVEMP is not primarily due to displacement of the IO muscle. Instead, the majority of the effect is likely due to tonic activity of the IO muscle. The IO has been shown to move anteriorly as the eyes move upwards (Demer et al., 2003), bringing the source of the signal closer to the recording electrodes. However, this movement is small and myogenic potentials are known to spread widely over the scalp (e.g. Thickbroom and
Conclusion
We have shown that the effect of vertical gaze on the oVEMP is likely to be caused mainly by changes in tonic eye muscle activity. While the effect of muscle-electrode distance is also significant, it cannot alone account for the large effect of gaze on the oVEMP. Although surface electrodes will always reflect the summed activity of several extraocular muscles, the oVEMP is therefore likely to be dominated by responses of the closest tonically-active muscle to the recording electrode. Thus
Acknowledgements
We would like to thank Dr Itsaso Olasagasti and Dr Chris Bockisch for helpful discussions about the study design. Dr Sally Rosengren was supported by the National Health and Medical Research Council of Australia. The study was supported by the Neuro-Otology Society of Australia, the Swiss National Science Foundation, the Betty and David Koetser Foundation for Brain Research and the Zurich Center for Integrative Human Physiology (University of Zurich).
References (46)
- et al.
The electrical activity of the muscles of the eye and eyelid in various positions and during movement
Electroencephalogr Clin Neurophysiol
(1953) - et al.
Feasibility of the simultaneous ocular and cervical vestibular-evoked myogenic potentials in unilateral vestibular hypofunction
Clin Neurophysiol
(2009) - et al.
Motor unit excitability changes mediating vestibulocollic reflexes in the sternocleidomastoid muscle
Clin Neurophysiol
(2004) - et al.
The effect of gaze direction on the ocular vestibular evoked myogenic potential produced by air-conducted sound
Clin Neurophysiol
(2009) - et al.
Feasibility of ocular vestibular-evoked myogenic potentials (oVEMPs) recorded with eyes closed
Clin Neurophysiol
(2012) - et al.
The role of the superior vestibular nerve in generating ocular vestibular-evoked myogenic potentials to bone conducted vibration at Fz
Clin Neurophysiol
(2009) - et al.
Dimensions of the human sclera: thickness measurement and regional changes with axial length
Exp Eye Res
(2010) - et al.
Vestibular-evoked extraocular potentials produced by stimulation with bone-conducted sound
Clin Neurophysiol
(2005) - et al.
Vestibular evoked myogenic potentials: past, present and future
Clin Neurophysiol
(2010) - et al.
Presaccadic ‘spike’ potential: investigation of topography and source
Brain Res
(1985)
Ocular vestibular evoked myogenic potentials (oVEMPs) produced by air- and bone-conducted sound
Clin Neurophysiol
The human sound-evoked vestibulo-ocular reflex and its electromyographic correlate
Clin Neurophysiol
Alexander’s law during high-acceleration head rotations in humans
Neuroreport
Eyes on target: what neurons must do for the vestibuloocular reflex during linear motion
J Neurophysiol
Difference in the amplitude of the human soleus H reflex during walking and running
J Physiol
The cornea in young myopic adults
Br J Ophthalmol
Eye movements induced by ampullary nerve stimulation
Am J Physiol
Semicircular canal nerve eye and head movements: the effect of changes in initial eye and head position on the plane of the induced movement
Arch Ophthalmol
Myogenic potentials generated by a click-evoked vestibulocollic reflex
J Neurol Neurosurg Psychiatry
Muscle tension during unrestrained human eye movements
J Physiol
Bone conducted vibration selectively activates irregular primary otolithic vestibular neurons in the guinea pig
Exp Brain Res
Magnetic resonance imaging characterization of orbital changes with age and associated contributions to lower eyelid prominence
Plast Reconstr Surg
Dual encoding of muscle tension and eye position by abducens motoneurons
J Neurosci
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