Vestibulo-ocular reflexes (VOR) were evaluated with a reactive torque helmet that imposed high-frequency oscillation (2-20 Hz) or step displacements of the head in the horizontal plane. The present paper describes the results in patients with vestibular deficiencies (labyrinthine defective; LD); experimental and analytical techniques and results for normal subjects were described in Part 1 of this paper. The patient groups included: total unilateral LD (related to acoustic neuroma; n = 40); severe (clinically total) bilateral LD (n = 7); bilateral hyporeflexia (n = 14); unilateral hyporeflexia (n = 11); and patients with LD phenomena that had subsided (n = 3). Helmet-induced head steps provided the most specific information. Characteristically, gain was lowered in one direction or both directions after unilateral or bilateral vestibular lesions, respectively; in general, the magnitude of the gain reduction correlated well with the degree of complaints and disability. Surprisingly, delay was systematically prolonged (up to several tens of milliseconds) in all groups of subjects with manifest vestibular pathology. These results suggest that the determination of delay, in addition to gain of the VOR, is feasible and important in the evaluation of vestibular function. The results of head oscillation generally supported the results for steps, but were somewhat less specific. The responses to manually generated head steps roughly agreed with those to helmet-induced steps, but because of the non-uniform acceleration they allowed a less exact analysis of VOR function.

We evaluated changes in the subjectively perceived gravitational vertical as an index of imbalance in the function of the right and left otolith organs. In addition to normal subjects (n = 25), we measured patients with a longstanding (mean 4.5 year +/- 3.2 SD; range 0.5-11.5 years) unilateral vestibular loss after surgery for acoustic neuroma (n = 32), patients with partial unilateral vestibular loss (n = 7) and patients with bilateral vestibular hyporeflexia (n = 8). Normal subjects could accurately align a vertical luminous bar to the gravitational vertical in an otherwise completely dark room (mean setting -0.14 degree +/- 1.11 SD). Patients with left-sided (complete; n = 13) or right-sided (complete; n = 19 and partial; n = 7) unilateral vestibular loss made mean angular settings at 2.55 degrees +/- 1.57 (SD) leftward and 2.22 degrees (+/-1.96 SD) rightward, respectively. These means differed highly significantly from the normal mean (p < 0.00001). In the time interval investigated (0.5-11.5 years) the magnitude of the tilt angle showed no correlation with the time elapsed since the operation. The mean setting by patients with clinically bilateral vestibular loss (-1.17 degrees +/- 1.96 SD; n = 8) did not significantly differ from the control group. The systematic tilts of the subjective vertical in patients with a unilateral vestibular impairment were correlated with their imbalance in canal-ocular reflexes, as reflected by drift during head-oscillation at 2 Hz (r2 = 0.44) and asymmetries in VOR-gain for head-steps (r2 = 0.48-0.67). These correlations were largely determined, by the signs of the asymmetries; correlation between the absolute values of the VOR gain asymmetries and subjective vertical angles proved to be virtually absent. We conclude that the setting of the subjective vertical is a very sensitive tool in detecting a left-right imbalance in otolith function, and that small but significant deviations towards the defective side may persist for many years (probably permanently) after unilateral lesions of the labyrinth or the vestibular nerve.

1. We probed the gain and phase of the vestibuloocular reflex (VOR) during the execution of voluntary gaze saccades, with continuous oscillation or acceleration pulses, applied through a torque helmet. 2. Small-amplitude (< 1 degree), high-frequency (10-14 Hz) head oscillations in the horizontal or vertical plane were superimposed on ongoing horizontal gaze saccades (40-100 degrees). Torque pulses to the head ("with" or "against" gaze) were superimposed on 40 degrees horizontal saccades. Eye and head movements were precisely measured with sensor coils in magnetic fields. 3. Techniques were developed to separate the oscillatory (horizontal or vertical) component from the gaze shift and obtain VOR gain and phase with Fourier techniques from the relation between eye-in-head and head oscillations. These involved either subtraction of exactly matching saccades with and without oscillation (drawback: low yield) or time shifting of successive trials to synchronize the oscillations (drawback: slight time blurring of saccades). 4. The results of these matching and synchronization methods were essentially identical and consistent. Presaccadic gain values of the horizontal VOR (typically about unity) were reduced by, on average, approximately 20 and 50% during horizontal saccades of 40 and 100 degrees, respectively. These percentages may be truncated because of methodological limitations, but even after taking these into account (on the basis of simulation experiments with 2 different, theoretical profiles of suppression) our results do not support a complete saccadic VOR suppression for any substantial fraction of saccadic duration. Qualitatively similar changes were found when the vertical VOR was probed during 100 degrees horizontal saccades. 5. Concomitantly with the reductions in gain, VOR phase was advanced by approximately 20 degrees during the saccade. 6. In the wake of gaze saccades, VOR gain was consistently elevated (to approximately 1.0) above the presaccadic level (approximately 0.9). We submit that this mechanism ensures stable fixation of the newly acquired target at a time when the head is still moving substantially. 7. Although the responses to head torque pulses showed idiosyncratic asymmetries, analysis of the differences in eye and head movements for pulses with and against consistently showed a sharp fall of VOR gain at saccadic onset, following an approximately exponential course with a time constant of approximately 50 ms. This decay may be assumed to reflect VOR gain for a period of approximately 50 ms, after which secondary gaze control mechanisms become dominant. 8. The time course of the gain decay and phase shift of the VOR suggest that suppression of the "integrative (position) loop" of the VOR circuit was more complete than suppression of the direct, "velocity" pathway.

High-frequency head rotations in the 2-20 Hz range and passive, unpredictable head acceleration impulses were produced by a new technique, utilizing a helmet with a torque motor oscillating a mass. Unrestrained head and eye movements were recorded using magnetic sensor coils in a homogeneous magnetic field. In order to analyze the influence of the visual system on the vestibulo-ocular reflex (VOR), we took measurements under three experimental conditions: (1) with a stationary visual target; (2) in total darkness with the subject imagining the stationary target; and (3) with a head-fixed target. The results in 15 healthy subjects were highly consistent. At 2 Hz, VOR gain was near unity; above 2 Hz, VOR gain started to decrease, but this trend reversed beyond 8 Hz, where the gain increased continuously up to 1.1-1.3 at 20 Hz. Phase lag increased with frequency, from a few deg at 2 Hz to about 45 degrees at 20 Hz. Above 2 Hz, VOR gain was not significantly different for the three experimental conditions. Head acceleration impulses produced a VOR with near-unity gain in both directions. We also tested three subjects with clinically total bilateral loss of labyrinthine functions. These labyrinthine-defective subjects showed, in comparison to the normal subjects, strikingly lower gains and much longer delays in the VOR during sinusoidal and step-like head movements. These results suggest that our new torque-driven helmet technique is effective, safe and convenient, enabling the assessment of the VOR at relatively high frequencies where both visual and mental influences are minimized.

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