The Video Head Impulse Test

Abstract

In 1988, we introduced impulsive testing of semicircular canal (SCC) function measured with scleral search coils and showed that it could accurately and reliably detect impaired function even of a single lateral canal. Later we showed that it was also possible to test individual vertical canal function in peripheral and also in central vestibular disorders and proposed a physiological mechanism for why this might be so. For the next 20 years, between 1988 and 2008, impulsive testing of individual SCC function could only be accurately done by a few aficionados with the time and money to support scleral search-coil systems-an expensive, complicated and cumbersome, semi-invasive technique that never made the transition from the research lab to the dizzy clinic. Then, in 2009 and 2013, we introduced a video method of testing function of each of the six canals individually. Since 2009, the method has been taken up by most dizzy clinics around the world, with now close to 100 refereed articles in PubMed. In many dizzy clinics around the world, video Head Impulse Testing has supplanted caloric testing as the initial and in some cases the final test of choice in patients with suspected vestibular disorders. Here, we consider seven current, interesting, and controversial aspects of video Head Impulse Testing: (1) introduction to the test; (2) the progress from the head impulse protocol (HIMPs) to the new variant-suppression head impulse protocol (SHIMPs); (3) the physiological basis for head impulse testing; (4) practical aspects and potential pitfalls of video head impulse testing; (5) problems of vestibulo-ocular reflex gain calculations; (6) head impulse testing in central vestibular disorders; and (7) to stay right up-to-date-new clinical disease patterns emerging from video head impulse testing. With thanks and appreciation we dedicate this article to our friend, colleague, and mentor, Dr Bernard Cohen of Mount Sinai Medical School, New York, who since his first article 55 years ago on compensatory eye movements induced by vertical SCC stimulation has become one of the giants of the vestibular world.

Keywords: SHIMP; VOR; head impulse test; semicircular canal; vestibular; vestibulo-ocular reflex; video head impulse test.

Figure 1

The two test protocols for testing semicircular canal function. (A) In the HIMPs protocol (the classical test protocol), the person is required to maintain fixation on an earth-fixed target during a small, unpredictable, passive, head turn. Healthy subjects will not make any saccades at all or only small saccades. (B) In the SHIMPs protocol, the head turn is identical but the instructions are different—the person must maintain fixation on a head-fixed target (a spot from a head-mounted laser projected onto the wall in front of the subject). Healthy subjects make large saccades (see text for explanation).

Figure 2

Superimposed head and eye velocity records for a healthy subject during HIMPs trials (A) and SHIMPs trials (B). (A) During conventional HIMP trials, a typical healthy control elicits only very small mostly positive (compensatory) catch-up saccades after the end of the head impulse. (B) During SHIMP trials, the same healthy control shows large negative (anticompensatory) saccades after the end of the head impulse reflecting anticompensatory eye movements back to the head-fixed target. Both protocols give similar but slightly lower vestibulo-ocular reflex gain values during SHIMP trials compared to HIMP trials, but the saccade pattern is exactly complementary. Head velocity, orange traces; inverted eye velocity, blue traces; HIMP, conventional head impulse protocol; SHIMP, suppression head impulse protocol.

Figure 3

Superimposed head and eye velocity records for a patient with BVL during HIMPs trials (A) and SHIMPs trials (B). The results for a typical patient with complete BVL showing a reversed saccadic pattern during HIMP and SHIMP compared to a healthy control (Figure 2). (A) During standard HIMP trials, the patient with BVL elicits mostly overt positive (compensatory) catch-up saccades after the head impulse. (B) During SHIMP, the same patient with BVL shows only very few downward (anticompensatory) saccades after the end of the head impulse back to the head-fixed target. Both protocols give similar but slightly lower vestibulo-ocular reflex gain values during SHIMP compared to HIMP, but there is a complementary saccade pattern, which is reversed compared to healthy controls. Head velocity, orange traces; inverted eye velocity, blue traces. BVL, bilateral vestibular loss; HIMP, conventional head impulse protocol; SHIMP, suppression head impulse protocol. Reproduced with permission of Wolters Kluwer from the study by MacDougall et al. (3); http://www.neurology.org.

Figure 4

Superimposed head and eye velocity records for a patient with unilateral vestibular loss (UVL) during HIMPs trials (A) and SHIMPs trials (B). (A) For rotations to their healthy (right) side, the patient shows the usual HIMPs pattern of slow compensatory eye movement with few saccades. During rotations to the affected (left) side, there is a reduced slow-phase eye velocity and covert and overt saccades. (B) For rotations to their affected side, there are few SHIMPs saccades, whereas for rotations to their healthy left side, there are many large SHIMP saccades. Reproduced with permission of Wolters Kluwer from the study by MacDougall et al. (3); http://www.neurology.org.

Figure 5

(A) Schematic view of the brainstem showing the basic projections underlying the horizontal VOR. The synapses are numbered and the papers giving evidence for each synapse are given in Table 1. Reprinted from Ref. (28), © 1995, with permission from IOS Press. (B) A depiction of the neural activity in the VOR network during a head turn to the left, eliciting a compensatory eye movement response to the right (see text for a full description). Increased activation is shown by the darker blue and the thicker orange shows the increased commissural inhibition from the activated vestibular nucleus. (C) With head stationary, a unilateral vestibular loss (left here) elicits an imbalance in neural activity between the two vestibular nuclei. The absence of primary vestibular input means that the left vestibular nucleus has reduced activity (light blue), which in turn generates a reduction in commissural inhibition to the right vestibular nucleus (thin orange line), allowing the cells in the right nucleus to fire at a higher firing rate, resulting in the slow phase of vestibular nystagmus to the left and quick phase to the right (red arrows).

Figure 6

(A) A depiction of activity in the pathway during a contralesional (rightward) head turn after a left unilateral vestibular loss. (B) Activity during an ipsilesional head turn (see text for a full description).

Figure 7

The effect of gaze angle on measurements of the eye movement during vertical head impulses. Because the video camera only measures horizontal and vertical components (not torsional components as yet), it is necessary to arrange the test situation so that that there is minimal contribution of torsion to the eye movement response to vertical canal stimulation (66). This is achieved by gaze being directed along the plane of the canals under test (A). If gaze is straight ahead (B), there is a substantial reduction in vertical eye velocity (and VOR gain) and the reduction is shown in (C)—eye velocity from the same subject with only gaze direction changing. Reproduced with permission from the study by McGarvie et al. (10).

Figure 8

How eyelid obstruction of the pupil during the head impulse generates artifactual eye movement records. (A,B) show the results of an eyelid flick touching the top of the pupil: biphasic for the anterior response (A) and uniphasic for the posterior response (B). The lower panels show stills from a grossly exaggerated version of how this occurs during the anterior impulse: the pupil starts in the centre of the vertical range (C), then is moving upwards as the eyelid “flicks” down to touch the top of the pupil (D,E), producing an apparent deceleration of the motion. As the eyelid then moves back up (F), the center of mass appears to accelerate upward. (G–I) A set of posterior canal impulses (G) in the situation where the pupil slides behind a stationary lower eyelid as it moves downward during the stimulus (H,I).

Figure 9

A model of head impulse gain calculation. The figure shows a slow-phase eye velocity response recorded by search coils (blue trace) and by video—video head impulse test (vHIT) (cyan trace) with compensatory “catch-up” saccades (red). The difference between these two traces is the goggle movement “bump artifact” (black trace) that is practically unavoidable for any video goggle system. Traditional VOR gain measurements over a narrow window that is usually centered on peak head acceleration (vertical green line) are very sensitive to contamination by this artifact (red gain values). For vHIT, we measure gain over a “wide window” from the beginning of the head impulse until the head velocity returns to 0°/s (vertical black dashed lines). This gain calculation method is relatively unaffected by the biphasic “bump artifact” (gray shaded areas) because the positive component (caused by manual acceleration of the head) and the negative component (deceleration) tend to cancel out during the impulse. Gains calculated using this wide window method are very similar for video and coils and quite comparable to the traditional narrow window gain measurement method for search coils.

Figure 10

Issues in how VOR performance should be calculated. The ideal eye movement response is one that is compensatory (i.e., maintains fixation) during head impulses with a fixation point: far (A) and close (B), and for linear “head heaves”: far (C) and close (D). Even in this simple example in one (horizontal) plane, with head rotation around a single point (or for purely linear translations), the calculation of an ideal eye movement response must factor in the geometric consequences of fixation distance, gaze eccentricity, interocular distance, head size (rotation radius), etc. The ideal eye movement rotation responses for a 20° head rotation and a 10 cm head translation are different: for the head rotation for the two eyes, and for the two fixation distances. With more natural head movements, in six degrees-of-freedom, these calculations are more complicated. Although technologies to track head movements and target positions in six degrees-of-freedom are improving rapidly, it is still convenient for video head impulse test to approximate gain calculations with simplified head rotation vs eye-rotation calculations. Such a convenient simplification does however require an understanding of the limitations and some diligence in minimizing departures from the assumptions such as a distant fixation point.

Figure 11

Examples of head impulse test (HIT) results. (1) Posterior circulation stroke (PCS) and vestibular neuritis (VN). Examples of HIT in PCS and VN, displayed as time series of inverted eye (ipsilesional: green, contralesional: blue) to head (red) impulse velocities. (A) In VN, ipsilateral gain deficit (mean 0.16) led to large overt (black arrows) saccades (cumulative amplitude: 9.1°, mean) and frequent covert saccades (73% of trials). Contralesional gain was mildly reduced (0.72), matched by small overt saccades (1.2°). Saccades occurring in the direction of contralesional impulses (#) were quick phases of spontaneous nystagmus. (B) In anterior inferior cerebellar artery-peripheral (AICAp) stroke due to left vestibular nuclear infarction (white arrow), gains were bilaterally deficient (ipsilesional: 0.11, contralesional: 0.21) and overt saccades were present bilaterally, larger after ipsilesional (5.7°) than contralesional (3.3°) trials. Compared to VN, overt saccades were 63% smaller after ipsilesional trials but 2.8 times larger after contralesional trials. Anticompensatory saccades (^∧) were dominant after contralesional trials. (C) In anterior inferior cerebellar artery-central (AICAc) stroke due to isolated right floccular infarction, gains were asymmetrically reduced (ipsilesional: 0.55, contralesional: 0.75) with few small overt saccades (ipsilesional trials: 2.7°, contralesional trials: 2.1°). (D) Upper: in posterior inferior cerebellar artery (PICA) stroke involving the left cerebellar hemisphere and nodulus (white arrowhead), gains were symmetrical (ipsilesional: 0.85, contralesional: 0.82) with frequent overt saccades, larger after contralesional (4.3°) than ipsilesional (2.8°) trials. Lower: in superior cerebellar artery (SCA) stroke involving the superior vermis, gains were mildly reduced bilaterally (ipsilesional: 0.66, contralesional: 0.71) with small overt saccades (ipsilesional trials: 2.2°, contralesional trials: 1.2°). Reproduced from the study by Chen et al. (104), used with permission from Wolters Kluwer Health, Inc.

Figure 12

Examples of head impulse test (HIT) results. (2) Internuclear ophthalmoplegia. Binocular search-coil recording of head (red) and eye (left: green, right: blue) in internuclear ophthalmoplegia. (A) Top: in left internuclear ophthalmplegia (INO) during ipsilesional horizontal canal (HC) (i.e., leftward) plane (HC) impulses, vestibulo-ocular reflex (VOR) was dysconjugate: gains were lower for the adducting than abducting eye, as measured by the VOR dysconjugacy index (VOR-DI), the ratio of abducting to adducting eye gain. During contralesional HC impulses, conjugacy was maintained. Abducting eye gains during either HC impulses were mildly reduced, possibly due to additional partial abducens nerve or supranuclear gaze involvement. All vertical canal function was preserved except for contralesional posterior canal (PC). Bottom: saccades elicited during ipsilesional HC impulses were also dysconjugate, as measured by the compensatory saccade dysconjugacy index (CS-DI), but more severely affected than VOR-DI. (B) Top: in bilateral INO during HC impulses to either side, dysconjugacy was present, albeit asymmetrically in this case. Abducting eye gains were lower compared to unilateral INO, possibly due to defective disfacilitation of the medial rectus motoneurons by the excitatory abducens interneurons, which are normally inhibited by type 1 vestibular neurons. All vertical canal function was impaired, but anterior canal was relatively less affected than PC. Bottom: like in unilateral INO, CS-DI was more severely affected than VOR-DI.

Figure 13

Examples of head impulse test (HIT) results. (3) Acute Wernicke’s encephalopathy. (A) Binocular search-coil recording of head (green) and eye (left: red, right: blue) velocity demonstrating severe loss of horizontal canal (HC) function with slow, overt saccades, but preservation of vertical canal function during individual canal plane HIT. Increased posterior canal function with anticompensatory saccades might be related to the presence of spontaneous upbeat nystagmus. Hexagonal bars depict gains from each canal. (B) Monocular, right eye (blue) video HIT recording of another patient, again demonstrating severe loss of HC function with preservation of vertical canal function. Reproduced from the study by Akdal et al. (93), used with permission from Elsevier.

Figure 14

Examples of head impulse test results. (4) Gaucher’s disease (GD). (A) Monocular search-coil recording of head (red) and left eye in patient 1 (P1) with GD. Gains for each canal were substantially reduced, but there was a paucity of compensatory saccades especially during horizontal canal impulses. Vestibulo-ocular reflex (VOR) onset latency was prolonged. (B) Phase-plane plots of eye versus head velocity for normal (pink), patient 1 (P1, light green), and patient 2 (P2, dark green). Normal phase-plane plot is slightly curved but approximates the diagonal (dotted gray line), indicating near matching of eye to head velocity. In both P1 and P2, due to gain deficit and latency delay, the curve is markedly deviated from the diagonal. Reproduced from the study by Chen et al. (143), used with permission from Springer.

Figure 15

Bilateral vestibular loss (BVL) with anterior canal sparing. Video head impulse measures of patients with BVL often reveal relative sparing of anterior semicircular canal function. This clinical pattern may possibly indicate gentamicin vestibulotoxicity or Menière’s disease, but also occurs in BVL of unknown origin as in this patient.