Eye movements and vestibular function during syncope

Thomas Lempert, Michael von Brevern
Introduction

When transient loss of consciousness is accompanied by convulsions and upward deviation of the eyes, it is usually diagnosed as an epileptic seizure. In a recent study1, however, we observed both myoclonus and upward eye movements in most induced syncopal attacks. This study was undertaken to investigate the ocular-motor features and vestibular function during syncope in more detail2.

Methods

Syncope was self-induced by 25 healthy volunteers on a tilt table by a sequence of 20 s of hyperventilation while supine, quick head-up tilt, and finally a 10-second Valsalva maneuver. This procedure is known to lower cerebral perfusion rapidly by combining the effects of hypocarbic cerebral vasoconstriction, orthostasis and a decreased venous return to the heart which reduces cardiac output. Subjects were advised to fixate a target 30 cm straight ahead. A high-resolution S-VHS camera was mounted on the tilt table to cover both eyes. Four subjects had also DC-electrooculography (EOG) for eye movement recording.

In a second experiment, syncope was induced during vestibular stimulation. Three subjects were seated upright on a chair which oscillated sinusoidally around an earth vertical axis (0.25 Hz/33° or 0.5 Hz/25°). Syncope was induced with eyes open in the dark by 20 s hyperventilation and a subsequent Valsalva maneuver. Eye movements were recorded by DC-EOG. The vestibular response was measured as the peak velocity of the compensatory horizontal slow phase. The ratio of peak eye velocity to peak chair velocity indicates the gain of the vestibulo-ocular reflex (VOR).

Results

Fourteen of 25 subjects experienced syncope on the tilt table. Eyes remained open in all 14 subjects. Six had downbeat nystagmus (DBN) at the onset that evolved into upward eye deviation (Figure 1), whereas seven showed isolated tonic upward deviation. In one subject the eyes remained in primary position. Upgaze was followed by a lateral eye deviation in nine subjects. All subjects showed a downward VOR during backtilt. During syncope with concurrent vestibular stimulation, the gain of the vestibulo-ocular reflex (VOR) increased by 65% on the average. Afterwards, the gain returned to the previous level.

Discussion
We observed a consistent pattern of syncopal eye movements that included downbeat nystagmus and slow upward eye deviations. In addition, we found an increased VOR gain in three subjects who self-induced syncope during vestibular stimulation. The slow upward eye deviation appeared to be the slow phase of DBN without resetting fast phases. Clinically, DBN results from brainstem or cerebellar lesions. In experimental animals, DBN has been produced by midline lesions in the dorsal pontomedullary region or by ablation of the flocculus. Considering the high oxygen demand of the cerebellum and its susceptibility to hypoxic injury a cerebellar origin of syncopal DBN seems most likely. Similarly, the increased VOR gain during syncope indicates release of the vestibular system from cerebellar control. Therefore DBN, upward eye deviation, and vestibular hyperexcitability suggest cerebellar dysfunction early in the course of syncope.
References
  1. Lempert T, Bauer M, Schmidt D. Syncope: a videometric analysis of 56 episodes of transient cerebral hypoxia. Ann Neurol 1994; 36:233-237.
  2. Lempert T, v. Brevern M. The eye movements of syncope. Neurology 1996; 46:1086-1088.