Labyrinthine lesions and motion sickness susceptibility

Abstract

The angular vestibulo-ocular reflex (aVOR) has a fast pathway, which mediates compensatory eye movements, and a slow (velocity storage) pathway, which determines its low frequency characteristics and orients eye velocity toward gravity. We have proposed that motion sickness is generated through velocity storage, when its orientation vector, which lies close to the gravitational vertical, is misaligned with eye velocity during head motion. The duration of the misalignment, determined by the dominant time constant of velocity storage, causes the buildup of motion sickness. To test this hypothesis, we studied bilateral labyrinthine-defective subjects with short vestibular time constants but normal aVOR gains for their motion sickness susceptibility. Time constants and gains were taken from rotational responses. Motion sickness was generated by rolling the head while rotating, and susceptibility was assessed by the number of head movements made before reaching intolerable levels of nausea. More head movements signified lower motion sickness susceptibility. Labyrinthine-defective subjects made more head movements on their first exposure to roll while rotating than normals (39.8 +/- 7.2 vs 13.7 +/- 5.5; P < 0.0001). Normals were tested eight times, which habituated their time constants and reduced their motion sickness susceptibility. Combining data from all subjects, there was a strong inverse relationship between time constants and number of head movements (r = 0.94), but none between motion sickness susceptibility and aVOR gains. This provides further evidence that motion sickness is generated through velocity storage, not the direct pathway, and suggests that motion sickness susceptibility can be reduced by reducing the aVOR time constant.

Fig. 1

Head positions during pretesting (a) and during testing with roll while rotating (b–f). The top row shows the head position of the subject, the circular arrows shows the direction of rotation. The third trace is chair velocity, which begins with the subject stationary, i.e., at 0°/s. The chair is accelerated to 138°/s, and then stopped. It is then accelerated in the opposite direction to −138°/s with the subject upright (b). The subject then successively tilts his/her head to the right (c), to upright (d), to the left (e), and back to upright (f) until either reaching 50 head movements or intolerable nausea. Each head position from c to f is held until the nystagmus generated by the head movement has disappeared. g Simplified model of angular vestibulo-ocular reflex. SCC: semicircular canals. See text for details

Fig. 2

Comparison of the per-rotatory response of a labyrinthine-defective subject (S1) with the average responses to rotation of 16 normal subjects (Dai et al. 2003). All subjects were rotated at 138°/s. The desaccaded slow phase eye velocity (H VEL) of the labyrinthine-defective subject is shown by the gray trace, and is fit by a first order exponential function (dashed line). The averaged normal aVOR responses are shown by the black line (upward arrow)

Fig. 3

a Number of head movements made during roll while rotating as a function of aVOR time constant in labyrinthine-defective subjects (filled circles) and by normal subjects in eight tests (filled squares). The diagonal upward arrow shows the direction of change in the time constants of the normal subjects from the first to the eighth test. b aVOR gains of labyrinthine-defective (circles) and normal subjects (squares). The upward arrow shows the gains from the first to the eighth tests of the normal subjects