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Video head impulse testing: Pitfalls in neurological patients

  • Nehzat Koohi
    Affiliations
    Centre for Vestibular and Behavioural Neurosciences, Department of Clinical and Movement Neurosciences, Institute of Neurology, University College London, Queen Square, London, UK

    The Ear Institute, University College London, London, UK
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  • Surangi Mendis
    Affiliations
    Department of Neuro-otology, Royal national ENT and Eastman Dental Hospitals, University College London Hospitals, London, UK
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  • Amy Lennox
    Affiliations
    Hypatia Clinic, Liverpool, UK
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  • Darren Whelan
    Affiliations
    Department of Neuro-otology, Royal national ENT and Eastman Dental Hospitals, University College London Hospitals, London, UK
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  • Diego Kaski
    Correspondence
    Corresponding author at: Centre for Vestibular and Behavioural Neurosciences, Department of Clinical and Movement Neurosciences, Institute of Neurology, University College London, Queen Square, WC1N 3BG, UK.
    Affiliations
    Centre for Vestibular and Behavioural Neurosciences, Department of Clinical and Movement Neurosciences, Institute of Neurology, University College London, Queen Square, London, UK

    The Ear Institute, University College London, London, UK

    Department of Neuro-otology, Royal national ENT and Eastman Dental Hospitals, University College London Hospitals, London, UK
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Open AccessPublished:September 17, 2022DOI:https://doi.org/10.1016/j.jns.2022.120417

      Highlights

      • Certain apparent catch-up saccades visible on the vHIT data may be due to the gaze-evoked nystagmus, induced by the head turn and transient eccentric positioning of the eyes.
      • Saccadic oscillations may affect the vHIT by appearing immediately after the head impulse and may be indistinguishable from an overt saccade if seen without clinical correlation.
      • Our cases highlight that oculomotor abnormalities can interfere with quantitative recording of the head impulse VOR responses and may impact the clinical diagnosis.

      Abstract

      The video head impulse test (vHIT) assesses the vestibulo-ocular reflex (VOR) during a rapid high-velocity low amplitude (10°–20°) head rotation. Patients with peripheral vestibulopathy have a reduced VOR gain with corrective catch-up saccades during the head turn. There are several pitfalls, mainly technical, which may interfere with interpretation of vHIT data. In addition, intrusive eye movement disorders such as spontaneous nystagmus that affect normal eye position and tracking can affect the vHIT results. To date there has been little study of neurological saccadic eye movements that may interfere with the interpretation of vHIT data. Here, in ten patients with a range of central neurological disorders, we describe oculomotor abnormalities on vHIT in the presence of normal range VOR gain values, recorded at a tertiary vestibular neurology service.

      Keywords

      1. Introduction

      The video head impulse test (vHIT), using a lightweight video goggle with an embedded infrared camera to track eye movements and inertial accelerometer in the frame to track head movements, assesses the vestibulo-ocular reflex (VOR) during a rapid high-velocity low amplitude (10–20°) head rotation [
      • Aw S.T.
      • Haslwanter T.
      • Halmagyi G.M.
      • Curthoys I.S.
      • Yavor R.A.
      • Todd M.J.
      Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations: I: responses in normal subjects.
      ,
      • Halmagyi G.
      • Chen Luke M.
      • Macdougall Hamish G.
      • Weber Konrad P.
      • Mcgarvie Leigh A.
      • Curthoys Ian S.
      The video head impulse test.
      ]. It provides a quantitative measurement of VOR gain by calculating the ratio of the area under the eye velocity curve with respect to the area under the head velocity curve during the head impulse [
      • Halmagyi G.
      • Chen Luke M.
      • Macdougall Hamish G.
      • Weber Konrad P.
      • Mcgarvie Leigh A.
      • Curthoys Ian S.
      The video head impulse test.
      ]. Normal VOR gain is close to 1.0 but patients with peripheral vestibulopathy have a reduced VOR gain during the head turn (to their affected ear). The lack of slow phase compensation for head turn results in movement of the eyes with the head, and occurrence of corrective eye movements (corrective catch-up or refixation saccades) for head impulses toward the affected ear [
      • Weber K.P.
      • Aw S.T.
      • Todd M.J.
      • McGarvie L.A.
      • Curthoys I.S.
      • Halmagyi G.M.
      Head impulse test in unilateral vestibular loss – vestibulo-ocular reflex and catch-up saccades.
      ]. Corrective catch-up saccades that occur during (covert saccades) or after the head impulse test (overt saccades) usually indicate peripheral vestibulopathy. This is the basis of the clinical head impulse test and allows clinicians to localise a vestibular deficit and differentiate the peripheral from central causes of vertigo [
      • Halmagyi G.M.
      • Curthoys I.S.
      A clinical sign of canal paresis.
      ].
      The vHIT is now a widely used tool in the work-up for dizziness, vertigo, and balance disorders. Recent studies however suggest a number of pitfalls, mostly technical, which may interfere with interpretation of vHIT data, including a dose-response relationship between the degree of tightness of the goggle strap and the amount of slippage-induced artefacts [
      • Suh M.W.
      • Park J.H.
      • Kang S.I.
      • Lim J.H.
      • Park M.K.
      • Kwon S.K.
      Effect of goggle slippage on the video head impulse test outcome and its mechanisms.
      ], presence of blinks, and neck resistance to passive movements. Critical technical considerations as well as expertise and training are required to correctly execute the vHIT and recognise potential artefacts arising during vHIT testing. In addition, intrusive eye movement disorders such as spontaneous nystagmus that affect normal eye position and tracking can interfere with the vHIT testing [
      • Mantokoudis G.
      • Saber Tehrani A.S.
      • Kattah J.C.
      • Eibenberger K.
      • Guede C.I.
      • Zee D.S.
      • Newman-Toker D.E.
      Quantifying the vestibulo-ocular reflex with video-oculography: nature and frequency of artifacts.
      ].
      Most vHIT results are primarily interpreted on the basis of the VOR gain with the exact normal value being specified by the manufacturer, usually >0.8 for the horizontal canals and > 0.7 for the vertical canals [
      • Halmagyi G.
      • Chen Luke M.
      • Macdougall Hamish G.
      • Weber Konrad P.
      • Mcgarvie Leigh A.
      • Curthoys Ian S.
      The video head impulse test.
      ]. Refixation saccades in the context of a normal gain has been identified but is a seemingly paradoxical finding. Perez-Fernandez and Eza-Nuñez [
      • Perez-Fernandez N.
      • Eza-Nuñez P.
      Normal gain of VOR with Refixation saccades in patients with unilateral vestibulopathy.
      ] assessed 36 patients with unilateral vestibular hypofunction who had normal gain on vHIT but unilateral refixation saccades which localised to the suspected pathological side, based on clinical history and complementary vestibular tests. It was hypothesised this occurred during the recovery period with compensatory saccadic mechanisms lagging behind improvement in gain. However, most patients (29 of 36) had suspected Meniere's disease, primarily affecting low frequency hair cells [
      • McGarvie L.A.
      • Curthoys I.S.
      • MacDougall H.G.
      • Halmagyi G.M.
      What does the dissociation between the results of video head impulse versus caloric testing reveal about the vestibular dysfunction in Ménière’s disease?.
      ], and given the high frequency stimulus used for vHIT, this may have introduced bias, particularly as VOR gain may be enhanced in the interictal phase [
      • Manzari L.
      • Burgess A.M.
      • MacDougall H.G.
      • Bradshaw A.P.
      • Curthoys I.S.
      Rapid fluctuations in dynamic semicircular canal function in early Ménière’s disease.
      ].
      While a pathological vHIT showing reduced VOR gain with refixation saccades is interpreted as a sign of a peripheral vestibulopathy, recent studies using quantitative assessments of VOR have shown that central vestibular disorders demonstrate different patterns of responses including normal, positive, hyperactive, and cross-coupled head impulse signs [
      • Choi J.Y.
      • Kim H.J.
      • Kim J.S.
      Recent advances in head impulse test findings in central vestibular disorders.
      ]. This is perhaps of particular relevance in patients with pre-existing oculomotor disorders (nystagmus, squints, oculomotor palsies). To date there has been little study of neurological saccadic eye movements that may interfere with the interpretation of vHIT data.
      Here, in ten patients with a range of central neurological disorders, we describe oculomotor saccadic abnormalities on vHIT in the presence of normal range VOR gain, recorded at a tertiary vestibular neurology service. After calibration, we performed vHIT on patients by unpredictable brisk horizontal head turns (high frequency, 10–20° head excursion in 100–300 m/s corresponding to 1000–6000°/s2 acceleration) while they were fixating on a visual target (eye level) at 1 m distance as per routine clinical guidelines [
      • Halmagyi G.
      • Chen Luke M.
      • Macdougall Hamish G.
      • Weber Konrad P.
      • Mcgarvie Leigh A.
      • Curthoys Ian S.
      The video head impulse test.
      ]. VOR gain values were derived by calculating the ratio of the area under the eye velocity curve with respect to the area under the head velocity curve. A VOR gain close to 1.0 usually reflects a normal range value, whereas a gain <0.8 or > 1.2 is considered abnormal.

      2. Cases

      2.1 Vestibular migraine

      Patient 1: A 55-year-old woman presented to the Emergency Department following an isolated and transient episode of unprovoked vertigo and severe imbalance that lasted for a few seconds. She had a history of motion sickness, tendency to visual auras and migraine headaches, in addition to type 1 diabetes and hypertension. She had experienced similar (at least 8) previous episodes of rotational vertigo and vomiting over the last 3 years. When reviewed 4 days after her vertigo onset, neuro-otological examination revealed normal ocular alignment with a full range of eye movements. Dix-Hallpike and Roll tests were negative. Her MRI and MRA results were unremarkable. Her cervical evoked myogenic potentials (cVEMPs) and caloric responses were normal. Video head impulse test showed normal range VOR gain values with apparent overt refixation saccades in the lateral canals (Fig. 1). The patient was diagnosed with vestibular migraine according to the Barany Society criteria [
      • Lempert T.
      • Olesen J.
      • Furman J.
      • Waterston J.
      • Seemungal B.
      • Carey J.
      • Bisdorff A.
      • Versino M.
      • Evers S.
      • Newman-Toker D.
      Vestibular migraine: diagnostic criteria. Consensus document of the Bárány Society and the International Headache Society.
      ].
      Fig. 1
      Fig. 1Normal range VOR gain values (lateral canals) in the presence of grouped overt refixation saccades. Note the velocity of the refixation saccades is slower than the expected velocity for a patient with peripheral vestibulopathy where the saccade attempts to correct for VOR dysfunction.

      2.2 Cerebellar disease

      Patient 2: A 57- year-old man with a genetically confirmed spinocerebellar ataxia 6 (SCA 6) diagnosis attended the Neuro-otology clinic for routine assessment. He denied vertigo, dizziness, or oscillopsia. He had very mild gait ataxia but no history of falls. MRI scan revealed a mild prominence of the superior cerebellar fissures. Neuro-otological examination revealed bi-directional and downbeat nystagmus horizontally, with no spontaneous nystagmus on primary gaze. Video head impulse test showed normal range VOR gain values, with apparent overt refixation saccades in the lateral canals, particularly the right (Fig. 2).
      Fig. 2
      Fig. 2The VOR gain values are within normal range (lateral canals) in the presence of grouped overt refixation saccades, most marked on the right, and not reaching the threshold for refixation saccades. Note the velocity of the refixation saccades is slower than would be expected for a patient with peripheral vestibulopathy where the saccade attempts to correct for VOR dysfunction.
      Patient 3: A 69-year-old woman with a genetically confirmed SCA 6 diagnosis had been experiencing episodic vertigo since the age of 35. The frequency of her vertigo attacks had reduced over time and she experienced short-lived vertigo only in certain head positions such as tilting her head backward. Neuro-otological examination revealed bi-directional and downbeat nystagmus on horizontal gaze and downbeat nystagmus on primary gaze. Video head impulse test showed normal range VOR gain values with apparent overt refixation saccades in all semicircular canals (Fig. 3). Vestibular responses to impulse chair rotation were normal bilaterally. Her recent MRI scan revealed cerebellar atrophy, stable since her imaging 5 years prior.
      Fig. 3
      Fig. 3vHIT data showing VOR gain values are within normal limits across all semicircular canals except right anterior canal (the right anterior VOR gain value is 1.31). As shown on the figure, the left anterior VOR gain of 1.19 is likely to be artefactually low due to the presence of downbeat nystagmus that would reduce the area under the eye velocity curve. Prominent saccades throughout the recording are related to underlying gaze-evoked and vertical nystagmus. Note that ‘saccades’ are present even prior to the onset of the head impulse (panels B & C, arrows).
      Patient 4: A 31-year-old man with a genetically confirmed diagnosis of late-onset Friedrich's ataxia had been experiencing imbalance over the past five years, particularly noticeable when using stairs. Neuro-otological examination revealed bi-directional and downbeat nystagmus on horizontal gaze. There were prominent microsaccadic oscillations on primary gaze. vHIT testing revealed normal gain across the lateral semicircular canals, with apparent refixation saccades (Fig. 4). Normal peripheral vestibular function was confirmed on bithermal caloric testing and rotational impulse testing.
      Fig. 4
      Fig. 4vHIT of lateral semicircular canals showing apparent overt refixation saccades despite normal range VOR gain values. Note that the ‘saccades’ are scattered and of low velocity (relative to typical refixation saccades seen in acute peripheral vestibulopathies such as vestibular neuritis). These ocular movements likely reflect the underlying gaze-evoked nystagmus and microsaccadic oscillations, hence the anti-compensatory direction of some of the saccadic eye movements, given otherwise normal peripheral vestibular function (on caloric and rotational testing).

      2.3 Mitochondrial disease

      Patient 5: A 63-year-old woman with a genetically confirmed diagnosis of mitochondrial disease (myoclonic epilepsy with ragged-red fibres, MERF) described a long-standing and progressive history of imbalance, tending to be worse in the dark, exacerbated by busy or rich visual environments, and fast-moving objects. She has visual loss, ataxia, neuropathy, muscle fatigue, and myoclonic jerks in relation to the mitochondrial disorder. Clinical examination from a neuro-otological perspective revealed normal ocular alignment with a full range of eye movements. There was a subtle bi-directional nystagmus on horizontal gaze but no spontaneous nystagmus on primary gaze. Video head impulse test showed normal range VOR gain values with apparent overt refixation saccades in the lateral semicircular canals (Fig. 5). Caloric responses were normal. Her MRI showed cerebellar atrophy and widespread symmetrical T2 hyperintensities predominantly involving the basal ganglia.
      Fig. 5
      Fig. 5vHIT data showing apparent refixation saccades despite normal VOR gain values for the lateral semicircular canals (top panel). Note the right anterior VOR gain is slightly larger than normal range with saccades in an anti-compensatory direction (as for the left anterior canal) that do not reach the velocity threshold to be coded red.
      Patient 6: A 59-year-old man with the genetically confirmed diagnosis of mitochondrial disease (m.3243A mutation), reported a three-year history of occasional non-intrusive dizziness. Clinical examination from a neuro-otological perspective revealed normal ocular alignment with a full range of eye movements. There was a subtle bi-directional nystagmus on horizontal gaze but no spontaneous nystagmus on primary gaze. Video head impulse test showed normal range VOR gain values with apparent overt refixation saccades in the lateral semicircular canals (Fig. 6). Vestibular responses to bi-thermal caloric were normal. His MRI scan revealed a mild cerebellar volume loss.
      Fig. 6
      Fig. 6vHIT data showing apparent refixation saccades (red traces) despite normal VOR gain, most evident on lateral semicircular canal testing (top panel). Note the velocity of these saccades is slow, compared to refixation saccades seen in a patient with peripheral vestibulopathy. The saccades are thought to be due to the gaze-evoked nystagmus, induced by the head turn and transient eccentric positioning of the eyes. Note that the relatively high gain value (compared to all the other canal responses) of 1.12 obtained for the right anterior impulses is likely due to goggle movement, with a break/change of slope in the underlying head velocity traces correlating with an apparent increase in the eye velocity signal.

      2.4 Acute stroke

      Patient 7: A 73-year-old woman presented with an acute episode of rotational vertigo and unsteadiness in the context of a right caudate nucleus, putamen and insular cortex stroke two weeks prior to her follow up appointment. She described that she had been experiencing short-lived episodic vertigo prior to her stroke. Her mobility has worsened since the stroke, although she was already struggling to walk due to sciatic pain. She described oscillopsia and dizziness when going over bumps on the road but did not have any further rotational vertigo. On examination (Day 14 post stroke) there was a right over left skew deviation and right sided esotropia. There was a subtle bi-directional nystagmus on horizontal gaze but no spontaneous nystagmus on primary gaze. The gait was broad-based, unsteady, and cautious. Video head impulse test (performed at day 1, day 2 and day 14 post stroke) showed normal range VOR gain values with apparent overt refixation saccades in the lateral semicircular canals (Fig. 7). Her MRI showed restricted diffusion within the right lentiform nucleus, posterior limb of the right internal capsule and right corona radiata, consistent with a recent infarct. Mature left basal ganglia lacunar infarcts were also noted.
      Fig. 7
      Fig. 7vHIT data showing apparent refixation saccades with normal range VOR gain. The saccades are often scattered, and only reach the pre-determined threshold for ‘refixation’ saccades in a few instances. The saccades are thought to be due to the gaze-evoked nystagmus, induced by the head turn and transient eccentric positioning of the eyes.
      Patient 8: A 57-year-old man attended the Emergency Department after experiencing an acute prolonged (>18 h) episode of vertigo. He had noticed tinnitus and reduction of hearing in his right ear. He reported he had a fall when he tried to stand up while he was experiencing the dizziness. He also reported numbness and weakness in his right arm. Medical history included type 2 diabetes mellitus and depression. At the time of assessment, the vertigo had subsided, but he continued to experience hearing loss and tinnitus, a low-frequency constant ‘whooshing’ sound. He was using a stick to mobilise. Despite normal gain on lateral semicircular canal vHIT testing, there were refixation saccades on the right (Fig. 8). Second degree left beating nystagmus was observed on primary position and on left gaze, without vertical nystagmus. A 48-h delayed MRI scan showed small acute infarcts within the right thalamus and dorsal left hemipons, together with scattered microhaemorrhages.
      Fig. 8
      Fig. 8vHIT lateral semicircular canal data showing apparent refixation saccades on the right (red traces) despite normal range VOR gain values, and a reversal of these saccades on left head impulses, suggestive of spontaneous eye oscillations rather than true refixations, induced by the head turn. Note that reversal of saccades are seen even before any head movements occur, suggesting a resting eye oscillation (e.g., spontaneous nystagmus or microsaccadic oscillations that were observed in primary gaze on oculography).

      2.5 Multiple sclerosis

      Patient 9: A 61-year-old woman with a background of relapsing remitting multiple sclerosis diagnosed 16 years previously was evaluated for persistent dizziness characterised by visual disturbance and a sense that the two eyes were ‘out of sync’. Clinical examination revealed a bilateral internuclear ophthalmoplegia (INO) with gaze-paretic nystagmus bilaterally, but no vertical nystagmus. vHIT recorded from the right eye revealed apparent impaired VOR gain with refixation saccades on the right only (Fig. 9A). Using monocular, left eye recording of the vHIT, there was apparent VOR impairment with refixation saccades on the left only. (Fig. 9B) In this case, the abnormal VOR gain was thought to reflect impaired adducting saccade function due to the INO, rather than vestibular dysfunction. Indeed, bi-thermal caloric function was within normal limits bilaterally. A T2 FLAIR brain MRI scan showed multiple lesions affecting multiple supra and infratentorial lesions in the brain parenchyma with new cortical lesions and evidence of progression, but no new cerebellar or brainstem lesions.
      Fig. 9
      Fig. 9Video head impulse (vHIT) testing. For right-sided impulses, the red lines represent the head movements and the black lines represent the eye movements. For left-sided impulses, the blue lines represent head movements, the black lines represent eye movements. VOR gain values are reduced for the lateral semicircular canals. A. Right-eye recording: the vHIT software picked up what appear to be overt saccades testing the right lateral canal but no ‘refixation saccades’ were observed testing the left lateral canal. B. Left-eye recording: the vHIT software picked up what appear to be overt saccades testing the left lateral canal but no ‘refixation saccades’ were observed testing the right lateral canal. Note that the observed saccades take a longer time than normal to complete and hence produce a lower eye velocity than expected for the measured low level of gain. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

      2.6 Patient with microsaccadic oscillations

      Patient 10: An 80-year-old lady was referred to our centre with suspected saccadic dysmetria. She was asymptomatic with no subjective visual disturbance, imbalance, dizziness or headaches. She was known to have a right frontal convexity meningioma that was stable on regular imaging surveillance. Microsaccadic oscillations were noted in spontaneous gaze, modulated by gaze in all directions and with monocular vision. Clinical HIT showed apparent ‘catch-up saccades’. The rest of the clinical eye movement examination was normal. These findings were correlated during oculomotor testing using videonystagmography (Fig. 10A). vHIT showed normal gain values with apparent overt refixation saccades testing the lateral canals. Video recording demonstrated microsaccadic oscillations during horizontal canal vHIT testing (Fig. 10B). Normal peripheral vestibular function was confirmed using rotational testing. With clinical correlation, it was concluded that these ‘saccades’ were representative of the underlying microsaccadic oscillations.
      Fig. 10
      Fig. 10A. Videonystagmography traces taken from recording of the left eye in centre gaze. Frequent microsaccadic oscillations are demonstrated. In the inset, these oscillations are shown to be 0.3° horizontal saccades with an intersaccadic interval of approximately 250 milliseconds. B. vHIT testing: For right-sided impulses (traces on the right), the orange lines represent the head movements and the green lines represent the eye movements. For left-sided impulses (traces on the left), the blue lines represent head movements, the green lines represent eye movements. VOR gain values were normal in all six semicircular canals tested (vertical canals not shown). The vHIT software picked up what appear to be overt refixation saccades (black arrows) in both lateral canals, more so on the right. We observed frequent microsaccadic oscillations during the video recording of the vHIT that are thought to account for these ‘refixation saccades’. Given a 700 msec presentation epoch for the head impulse traces, one would expect an almost equal number of saccades in both the “compensatory” and “anti-compensatory” directions. However, this pattern was mostly present for left lateral responses, with most saccades in the compensatory direction during right lateral impulses. We speculate that in this patient the gaze modulation of the micro-saccades is more prevalent after the head is rotated to the right (and hence the eye to the left) given the presence of a right hemispheric meningioma. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

      3. Discussion

      While abnormal VOR gain with refixation saccades, quantitatively recorded by vHIT, are features of peripheral vestibular hypofunction, various patterns of saccadic movements have been observed in neurological patients with central vestibular involvement. It is proposed that physiological saccades in the presence of normal VOR gain can also occur in older individuals (>70 yrs) [
      • Matiño-Soler E.
      • Esteller-More E.
      • Martin-Sanchez J.C.
      • Martinez-Sanchez J.M.
      • Perez-Fernandez N.
      Normative data on angular vestibulo-ocular responses in the yaw axis measured using the video head impulse test.
      ], putatively due to presbyvestibulopathy. However, saccades increasing in the absence of reduced gain due to ageing seems unlikely if one considers refixation saccades are a compensatory strategy for a defective VOR and its consequent gaze instability.
      For clinical diagnosis, it is crucial to differentiate a catch-up saccade, that indicates a VOR gain deficiency, from the fast phase of spontaneous or gaze-evoked nystagmus. The presence of gaze-evoked nystagmus, as seen across of neurological disorders including cerebellar pathology, and spontaneous nystagmus, as might occur with brainstem strokes (e.g. anterior inferior cerebellar artery strokes), can interfere with VOR recordings and appear as refixation saccades. Such oculomotor ‘artefacts’ differ from true refixation or catch-up saccades. In patients with spontaneous nystagmus this can be observed by focusing on rhythmic runs of three or more nystagmus beats [
      • Mantokoudis G.
      • Saber Tehrani A.S.
      • Kattah J.C.
      • Eibenberger K.
      • Guede C.I.
      • Zee D.S.
      • Newman-Toker D.E.
      Quantifying the vestibulo-ocular reflex with video-oculography: nature and frequency of artifacts.
      ]. In gaze-evoked nystagmus they may occur throughout a vHIT recording (e.g. patients 4 and 7), rather than within 200 ms of the head impulse, have slower velocities (e.g. patient 2), be in a plane outside of that expected for the canal being tested (e.g. patient 3), and the direction of the fast phase of the gaze-evoked nystagmus may be in the “compensatory” direction (e.g., patient 8).
      Damage to the medial longitudinal fasciculus (MLF) results in internuclear ophthalmplegia (INO), a dysconjugate horizontal eye movement disorder characterised by abducting eye nystagmus and adducting eye slowing during horizontal saccades [
      • Zee D.S.
      Internuclear ophthalmoplegia: pathophysiology and diagnosis.
      ]. In our patint with a bilateral INO (patient 9), the reduced VOR gain with only right-sided refixation saccades were present using right-eye recording but this pattern was reversed when we performed the vHIT using the left-eye recording. The VOR gain was reduced using the right-eye and left-eye recording but ‘refixation saccades’ were present depending on which eye was being recorded. The abnormal VOR gain with ‘refixation saccades’ was thought to reflect impaired adducting saccade function due to the INO (the fast phase of nystagmus appeared as refixation saccades), rather than vestibular dysfunction, as also described by Halmagyi and colleagues [
      • Halmagyi G.
      • Chen Luke M.
      • Macdougall Hamish G.
      • Weber Konrad P.
      • Mcgarvie Leigh A.
      • Curthoys Ian S.
      The video head impulse test.
      ]. In such cases, careful eye movement examination is needed before interpreting the vHIT results.
      Abnormal saccadic oscillations can be indeed induced by a range of saccadic oscillations and intrusions, namely square-wave jerks, saccadic pulses, ocular flutter, opsoclonus and micro-saccadic oscillations [
      • Leigh R.
      • Zee D.
      Pathophysiology of abnormalities of saccades.
      ]. Square-wave jerks are thought to be a continuum of micro-saccadic intrusions. They can be found in otherwise healthy individuals and may increase with age [
      • Lemos João
      Eggenberger, Eric Saccadic intrusions.
      ]. Such oscillations are generally small (0.5°), purely horizontal, involuntary and are followed, with an intersaccadic interval of approximately 250 milliseconds, by a corrective saccade that brings the eye back to the fixation target [
      • Leigh R.
      • Zee D.
      Pathophysiology of abnormalities of saccades.
      ]. As seen in patient 10, microsacadic oscillations may affect the vHIT by appearing immediately after the head impulse and may be indistinguishable from an overt saccade if seen without clinical correlation.

      4. Conclusion

      Our cases highlight that oculomotor abnormalities can interfere with quantitative recording of the head impulse VOR responses and may impact the clinicians' diagnosis. A detailed eye movement examination must therefore always take place to account for potential impact of underlying eye movements that may be seen during vHIT testing.

      References

        • Aw S.T.
        • Haslwanter T.
        • Halmagyi G.M.
        • Curthoys I.S.
        • Yavor R.A.
        • Todd M.J.
        Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations: I: responses in normal subjects.
        J. Neurophysiol. 1996; 76: 4009-4020
        • Halmagyi G.
        • Chen Luke M.
        • Macdougall Hamish G.
        • Weber Konrad P.
        • Mcgarvie Leigh A.
        • Curthoys Ian S.
        The video head impulse test.
        Front. Neurol. 2017; 8https://doi.org/10.3389/fneur.2017.00258
        • Weber K.P.
        • Aw S.T.
        • Todd M.J.
        • McGarvie L.A.
        • Curthoys I.S.
        • Halmagyi G.M.
        Head impulse test in unilateral vestibular loss – vestibulo-ocular reflex and catch-up saccades.
        Neurology. 2008; 70: 454-463https://doi.org/10.1212/01.wnl.0000299117
        • Halmagyi G.M.
        • Curthoys I.S.
        A clinical sign of canal paresis.
        Arch. Neurol. 1988; 45: 737-739
        • Suh M.W.
        • Park J.H.
        • Kang S.I.
        • Lim J.H.
        • Park M.K.
        • Kwon S.K.
        Effect of goggle slippage on the video head impulse test outcome and its mechanisms.
        Otol Neurotol. 2017 Jan; 38: 102-109https://doi.org/10.1097/MAO.0000000000001233
        • Mantokoudis G.
        • Saber Tehrani A.S.
        • Kattah J.C.
        • Eibenberger K.
        • Guede C.I.
        • Zee D.S.
        • Newman-Toker D.E.
        Quantifying the vestibulo-ocular reflex with video-oculography: nature and frequency of artifacts.
        Audiol Neurootol. 2015; 20: 39-50https://doi.org/10.1159/000362780
        • Perez-Fernandez N.
        • Eza-Nuñez P.
        Normal gain of VOR with Refixation saccades in patients with unilateral vestibulopathy.
        J Int Adv Otol. 2015 Aug; 11: 133-137https://doi.org/10.5152/iao.2015.1087
        • McGarvie L.A.
        • Curthoys I.S.
        • MacDougall H.G.
        • Halmagyi G.M.
        What does the dissociation between the results of video head impulse versus caloric testing reveal about the vestibular dysfunction in Ménière’s disease?.
        Acta Otolaryngol. 2015 Sep; 135: 859-865https://doi.org/10.3109/00016489.2015.1015606
        • Manzari L.
        • Burgess A.M.
        • MacDougall H.G.
        • Bradshaw A.P.
        • Curthoys I.S.
        Rapid fluctuations in dynamic semicircular canal function in early Ménière’s disease.
        Eur. Arch. Otorhinolaryngol. 2011 Apr; 268: 637-639https://doi.org/10.1007/s00405-010-1442-5
        • Choi J.Y.
        • Kim H.J.
        • Kim J.S.
        Recent advances in head impulse test findings in central vestibular disorders.
        Neurology. 2018 Mar 27; 90: 602-612https://doi.org/10.1212/WNL.0000000000005206
        • Lempert T.
        • Olesen J.
        • Furman J.
        • Waterston J.
        • Seemungal B.
        • Carey J.
        • Bisdorff A.
        • Versino M.
        • Evers S.
        • Newman-Toker D.
        Vestibular migraine: diagnostic criteria. Consensus document of the Bárány Society and the International Headache Society.
        J. Vestib. Res. 2012; 22: 167-172
        • Matiño-Soler E.
        • Esteller-More E.
        • Martin-Sanchez J.C.
        • Martinez-Sanchez J.M.
        • Perez-Fernandez N.
        Normative data on angular vestibulo-ocular responses in the yaw axis measured using the video head impulse test.
        Otol Neurotol. 2015 Mar; 36 (PMID: 25473958): 466-471https://doi.org/10.1097/MAO.0000000000000661
        • Zee D.S.
        Internuclear ophthalmoplegia: pathophysiology and diagnosis.
        Baillieres Clic Neurol. 1992 Aug; 1 (PMID: 1344079): 455-470
        • Leigh R.
        • Zee D.
        Pathophysiology of abnormalities of saccades.
        in: The Neurology of Eye Movements. Oxford University Press, Oxford, UK2015-06 (Retrieved 2 May. 2021, from)
        • Lemos João
        Eggenberger, Eric Saccadic intrusions.
        Curr. Opin. Neurol. February 2013; 26: 59-66https://doi.org/10.1097/WCO.0b013e32835c5e1d