Rotational vertebral artery occlusion syndrome with vertigo due to “labyrinthine excitation”

Transient ischemia of the brainstem or labyrinth?

According to anatomic and histopathologic studies, the labyrinth is vulnerable to ischemia for two reasons:

• 1. The labyrinthine artery, a single vessel with a small caliber, provides the arterial blood supply to the membranous labyrinth. It is an end artery with very few collaterals.4

• 2. Animal experiments showed that the vestibular and cochlear nerve fibers become unexcitable within 20 seconds to several minutes after complete blood flow interruption, and the receptor and resting potentials of the ear diminish.5

On the other hand, selective ischemia of vestibular nuclei neurons could also cause isolated episodic vertigo. Yamanaka et al.6 showed that neurons in the vestibular nucleus but not vestibular ganglial cells changed their firing rate when ischemic. In our patient, a central origin of the symptoms is less likely (and it occurs very rarely7) because the structures next to the vestibular nuclei in the brainstem would also be affected during brainstem ischemia and additional symptoms would be apparent, as in Wallenberg’s syndrome. Although it is a fact that the vertigo may be so distressing that the patient himself does not always notice additional symptoms,3 our patient was questioned and examined during more than 10 attacks, and we were not able to detect any other symptoms or signs typical of brainstem dysfunction.

If in the labyrinth, which ear and which SCCs were causative?

During the attacks the patient had tinnitus only in the right ear after he turned his head toward the left. This suggests transient ischemia of the common cochlear artery of the right labyrinth.

Cohen et al.8 reported that combined stimulation of the right anterior and horizontal SCC nerves in the cat led to upward, counterclockwise torsional and horizontal slow eye movements toward the left and a compensatory mixed, downward clockwise nystagmus with a horizontal component toward the right. We observed this very same nystagmus pattern in our patient. If all three SCCs were affected, the opposite vertical components of the anterior and posterior canal signals would cancel each other, resulting in a torsional horizontal nystagmus without a vertical component.8 If the attacks were due to a dysfunction of the anterior and horizontal SCC (both supplied by the single anterior labyrinthine artery), why was the posterior SCC (supplied by the posterior labyrinthine artery) spared? Anatomic studies have shown that there are more collaterals (intraosseous branches) to the posterior than to the anterior labyrinthine artery.4 Moreover, a recent histopathologic observation in a patient with an internal auditory artery infarction whose inferior vestibular labyrinth was also spared provides clinical support.9

Hypo- or hyperfunction of the labyrinth?

Neurons, axons,10 and hair cells are known to respond initially to ischemia by depolarizing. This first causes a transiently increased excitability with “positive symptoms” because the membrane potential comes closer to the activation potential of the axonal sodium channel.10 In hair cells the spontaneous rate of excitatory neurotransmitter release also increases during membrane depolarization. SCC afferents in the bullfrog showed “a substantial increase in firing rate during the first few minutes” of ischemia.5 In cases of longer ischemia, however, the membrane potential depolarizes further and the axonal membrane becomes unexcitable.5 The ischemia in our patient lasted for a maximum of only 5 seconds (he could not tolerate longer periods). During this time the membrane may depolarize, causing a transient hyperexcitability of the vestibular nerve or the hair cells or both, which would lead to the “irritative” nystagmus described earlier. We find support for this view in 1) the patient’s report of another “positive symptom”—a low-frequency tinnitus in his right ear and 2) the well-known changes in the direction of nystagmus in Menière’s disease, in which normal excitability changes either to hyperexcitability with irritative nystagmus and tinnitus or to hypoexcitability with paralytic nystagmus. Pathophysiologically, the extracellular potassium concentration in the perilymph increases and leads to membrane depolarization. Both the nystagmus and tinnitus in the right ear in our patient represent transient, ischemia-induced hyperfunction rather than hypofunction, which agrees with the direction of the nystagmus.