Why acute unilateral vestibular midbrain lesions rarely manifest with rotational vertigo: a clinical and modelling approach to head direction cell function
Journal of Neurology
https://doi.org/10.1007/s00415
Why acute unilateral vestibular midbrain lesions rarely manifest with rotational vertigo: a clinical and modelling approach to head direction cell function
Marianne Dieterich 0 1 2 3
Stefan Glasauer 0 1 2 3
Thomas Brandt 0 1 2 3
ADN DTN LMN INC MLF riMLF 0 1 2 3
0 Clinical Neuroscience, Ludwig-Maximilians Universität , Munich , Germany
1 German Center for Vertigo and Balance Disorders, Ludwig-Maximilians Universität , Munich , Germany
2 Department of Neurology, University Hospital, Ludwig- Maximilians Universität München , Marchioninistrasse 15, 81377 Munich , Germany
3 Munich Cluster for Systems Neurology (SyNergy) , Munich , Germany
A retrospective clinical study focused on the frequency of rotational vertigo in 63 patients with acute unilateral midbrain strokes involving the vestibular and ocular motor systems. In contrast to unilateral pontomedullary brainstem lesions, rotational vertigo in midbrain lesions occurred with a low frequency (14%) and transient (< 1 day) course. Swaying vertigo or unspecific dizziness (22%) and postural imbalance (31%) were more frequent. Midbrain strokes with transient rotational vertigo manifested with lesions chiefly in the caudal midbrain tegmentum, while manifestations with swaying, unspecific, or no vertigo chiefly occurred in rostral mesencephalic or meso-diencephalic lesions. We hypothesize that these different manifestations can be explained by the distribution of two separate cell systems based on semicircular canal function: the angular head-velocity cells and the head direction cells, both of which code for head rotation. Animal experiments have shown that angular head-velocity cells are located mainly in the lower brainstem up to the midbrain, whereas the head direction cells are found from the midbrain and thalamic level up to cortical regions. Due to the differences in coding, unilateral dysfunction of the angular velocity cell system should result in the sensation of rotation, while unilateral dysfunction of the head direction cell system should result in dizziness and unsteadiness. We simulated the different manifestations of vestibular dysfunction using a mathematical neural network model of the head direction cell system. This model predicted and confirmed our clinical findings that unilateral caudal and rostral brainstem lesions have different effects on vestibular function.
Midbrain stroke; Rotational vertigo; Unspecific dizziness; Vestibular system; Head-angular velocity cells; Head direction cells; Mathematical model
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Abbreviations
AVS Acute vestibular syndrome
OTR Ocular tilt reaction
SVV Subjective visual vertical
PoS Postsubiculum
Marianne Dieterich and Stefan Glasauer have equally contributed.
*
Introduction
Acute unilateral peripheral vestibular syndromes that involve
semicircular canal function and are caused by a labyrinthine
(Meniere’s disease) or vestibular nerve (acute vestibular
syndrome, AVS) disorder manifest with rotational vertigo
and horizontal-rotatory spontaneous nystagmus.
Pathophysiologically, it is well acknowledged that these signs and
symptoms are caused by a vestibular tone imbalance
generated by unequal input from the right and left ears. The side
of the unilateral lesion that causes the tone imbalance can
be determined by the direction of vertigo and spontaneous
nystagmus, which is contralateral and by the deviation of
stance and gait, which is ipsilateral to the lesion side. Similar
signs and symptoms occur with unilateral vestibular lesions
of the root entry zone of the eighth nerve affecting the
vestibular fascicle, the vestibular nucleus (chiefly medial and
superior parts) [
1–7
], the nucleus prepositus hypoglossi [
7
],
the cerebellar peduncle [
7, 8
], and the vestibular cerebellum
[
8–13
]. As these syndromes are elicited by central rather
than peripheral vestibular structures, they are called central
vestibular pseudoneuritis [
14, 15
] or, more recently, central
acute vestibular syndrome [16]. It is noteworthy that the
latter central lesions are all located at the lower brainstem and
cerebellar levels. In Fig. 1a, we have depicted the overlap of
causative MRI lesions at pontomedullary level in 23 stroke
patients reported in the literature who presented with
sustained rotational vertigo [
3–5, 7, 10
] (Fig. 1a).
The clinical manifestation of more cranial unilateral
vestibular lesions in the meso-diencephalic brainstem and
the vestibular cortex differs. In a small case study of eight
patients with acute unilateral lesions of the midbrain, only
one patient initially had rotational vertigo and two, swaying
vertigo [
17
] (Fig. 1b). Furthermore, unilateral lesions of the
vestibular thalamic subnuclei (posterolateral and
centromedian) do not manifest with rotational vertigo but rather with
thalamic astasia [
18–20
] and tilts of perceived visual vertical
[
21–23
]. Acute vestibular cortex lesions caused by strokes
in the middle cerebral arte (...truncated)