Recovery of the high-acceleration vestibulo-ocular reflex after vestibular neuritis

Abstract

Vestibular neuritis (VN) usually leads to a sudden gain asymmetry of the high-acceleration horizontal vestibulo-ocular reflex (VOR). We asked whether this asymmetry decreases over time indicating peripheral recovery and/or central compensation. The horizontal VOR during rapid rotational head impulses to both sides was recorded with search coils in 37 patients at different time periods (1-240 weeks) after the onset of VN. In ten patients, sequential measurements were performed. Gains of the VOR during head impulses toward the ipsilesional side significantly increased after the initial drop (average gains: < 1 week: 0.35; 1-4 weeks: 0.33; 4-40 weeks: 0.55; 40-240 weeks: 0.50). Gains on the contralesional side, however, were only slightly reduced and showed no significant change. We conclude that, in contrast to patients after hemilabyrinthectomy or unilateral vestibular neurectomy, the ocular response to ipsilesional rotations in patients after VN improves over time. This finding suggests that ipsilesional recovery is peripheral or, if central, depends on spared peripheral function. The physiology of linear and nonlinear VOR pathways predicts a considerable gain reduction for contralesional head impulses if central compensation mechanisms are not engaged. Thus, the relatively preserved gain on the contralesional side can be explained only by central "upregulation". Apparently, for high accelerations of the head, effective central compensation after VN does not aim to balance the gains of the VOR but tries to boost the contralesional gain close to normal.

Figure 1

Examples of horizontal head impulse tests in a healthy subject (A) and a patient two weeks (B) and two months (C) after a sudden vestibular asymmetry. If the vestibulo-ocular reflex (VOR) were perfectly compensatory, traces would be parallel to the abscissa (head-in-space axis); if the vestibulo-ocular reflex were absent, traces would move on a 45° slope. G_R: median gain value for head impulses to the right; G_L: median gain value for head impulses to the left. Traces are clipped beyond 10° eccentricity of head-in-space. Dashed vertical lines indicate intervals used to determine the gains (see Methods).

Figure 2

Average gain values (error bars: ±1 SD) of the four groups of patients (I, II, III, IV) and the group of healthy subjects (N). The abscissa indicates logarithmic time, except for the group of healthy subjects. In all panels, averages in the four groups of patients were significantly different from averages in the group of healthy subjects (p < 0.05 in the unpaired two-tailed t-test). Stars indicate significant differences of averages between patient groups. A. Head impulses toward the right side. B. Head impulses toward the left side. C. Gain differences (left minus right gain). Note that the gains were mirrored in subjects in whom the gain on the right side was higher than on the left side. Thus, the right side was always the weaker side and, as a result, the gain differences were always positive (see Methods).

Figure 3

Individual gain values in the ten patients who could be tested twice at different time periods after the onset of vestibular neuritis. Panels and scales are as in Figure 2. Filled circles: first measurements; open circles: consecutive measurements; filled square: average values in healthy subjects (error bars: ±1 SD).

Figure 4

Simplified diagram of the model described by Lasker et al. (2000). The input to the vestibulo-ocular reflex is angular head velocity (). This signal is passed through linear and nonlinear pathways. k_l and k_n represent the corresponding central gain elements of these two pathways. R denotes the resting rate of central vestibular neurons, which is added to the linear pathway. Td: time delay of the reflex (set to 7 ms in our simulations).

Figure 5

Performance of the model by Lasker et al. (2000) upon an actual head impulse (applied by A.P.) as input (duration = 0.4 s; amplitude = 40°; peak velocity = 470°/s; peak acceleration = 12,000°/s²). A. Position trajectory of the head impulse. The small overshoot is typical. B. Eye-in-space vs. head-in-space in the presence of an increasing right-sided deficit. Each trace represents the VOR simulated by the model in the presence of a right-sided vestibular deficit. The function of the right labyrinth was reduced in 10% steps (dashed lines) from normal (no deficit, thin solid line) to total loss (no function, thick solid line). No central elements were changed. Dashed vertical lines indicate intervals for determining the gain (see Methods). C. Gain difference (Δ Gain) as a function of ipsilesional gain (Gain_R). Data points represent the gains from panels B (triangles) and D (circles). Filled symbols: gains as a result of a total unilateral deficit. D. Axes and lines as in B, but ipsilateral R (90 → 80 Hz), contralateral k_l (1 →1.2), and contralateral k_n (0.00001 → 0.000025) were changed proportionally to the peripheral vestibular deficit. Note that the spontaneous nystagmus manifests itself indirectly by eye-in-space displacements to the right evoked by the slightest head-in-space movement to either side, although it cannot be seen directly in this plot.

Figure 6

Comparison of patients’ data with that from the model by Lasker et al. (2000) Δ Gain: differences between gains; Gain_R: gains during head impulses toward the right side, which was always the weaker side. Filled circles: individual testing sessions (N = 47 in 37 patients); filled square: average data point from healthy subjects (ellipse with horizontal and vertical radii: ±1 SD); horizontal dashed line: Δ Gain = 0; oblique dashed line: linear regression through data cloud. Gray area: all possible output values of the model when one varies the unilateral peripheral deficit (0%–100%) and gradually changes the central elements in proportion to the deficit (see Fig. 4). Line a: full changes of central elements (corresponding to Fig. 5D). Line b: no changes of central elements (corresponding to Fig. 5B).