Why acute unilateral vestibular midbrain lesions rarely manifest with rotational vertigo: a clinical and modelling approach to head direction cell function

Journal of Neurology, Mar 2018

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.

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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 - 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)


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Marianne Dieterich, Stefan Glasauer, Thomas Brandt. Why acute unilateral vestibular midbrain lesions rarely manifest with rotational vertigo: a clinical and modelling approach to head direction cell function, Journal of Neurology, 2018, pp. 1-15, DOI: 10.1007/s00415-018-8828-5