Contraversive Ocular Tilt Reaction, Body Lateropulsion and Gaze-Evoked Nystagmus After Inferior Cerebellar Peduncle and Dentate Nucleus Stroke

Abstract

The inferior cerebellar peduncle (ICP) is composed of the restiform and juxtarestiform bodies and contains the afferent and efferent fibers connecting with the vestibulocerebellum. Thus, the ICP participates in control of balance by integrating the proprioceptive and vestibular function, and lesions involving the ICP may result in vertigo, nystagmus, and imbalance (1,2). The dentate nucleus is involved in voluntary motor function and cognition. Here, we report on a patient with unilateral ICP and dentate nucleus infarction presenting with ocular contrapulsion, ipsilesional spontaneous nystagmus, direction-changing horizontal gaze-evoked nystagmus (GEN), positional nystagmus, contraversive ocular tilt reaction (OTR)/subjective visual vertical (SVV) tilt, and contraversive falling. A 38-year-old man presented with sudden vertigo on the bed, especially head-turning to the right side. He also reported vomiting, diplopia, and unsteadiness, but denied headaches, or tinnitus. Patient had a history of diabetes, diabetes retinopathy, diabetes ketosis, hyperlipidemia, and fatty liver, denied history of head trauma or atrial fibrillation. Examination showed left-beating spontaneous nystagmus, GEN during lateral gazes, ocular lateropulsion to the right side (See Supplemental Digital Content, Video 1, https://links.lww.com/WNO/A682), rightward head tilt, and hypotropic right eye during the alternative cover test. He fell to the right on attempted standing (See Supplemental Digital Content, Video 2, https://links.lww.com/WNO/A683). He also showed mild dysmetria in the left arm. The remainder of neurologic examination was normal. Video-oculography documented left-beating spontaneous nystagmus with and without visual fixation with a small upbeat component (Fig. 1A) and horizontal direction-changing GEN (Fig. 1B). Smooth pursuit was impaired to the left. Horizontal saccades were normal, but pulse-step mismatch was observed during downward saccades. The left-beating spontaneous nystagmus was 11 °/s while supine with an upbeat (7 °/s) component. The left-beating nystagmus further increased (21 °/s) with a downbeat (8 °/s) and counterclockwise torsional (from the patient's viewpoint) component during head-turning to the right while supine, and changed into right-beating (2 °/s) during head-turning to the left while supine. He also showed left-beating nystagmus (13 °/s) with upbeat (4 °/s) and counterclockwise torsional components during leftward Dix-Hallpike maneuver, and left-beating nystagmus (23 °/s) with downbeat (1 °/s) and counterclockwise torsional components during rightward Dix-Hallpike maneuver. During straight head hanging, he showed left-beating nystagmus (17 °/s) with upbeat (9 °/s) and counterclockwise torsional components. SVV (14.4°, normal range: −2.5° to 2.5°) and horizontal (17.2°, normal range: −2.5° to 2.5°) were tilted to the right. Fundus photographs showed an abnormal extorsion of the right eye (16.2°, normal range: 0–12.6°), and intorsion of the left eye (−4.1°) (Fig. 1C). The results of video head impulse tests and caloric tests were normal. Diffusion-weighted MRI disclosed an infarction involving the left ICP and dentate nucleus at the pontine level (Fig. 1D, E). The patient was considered to probably have large atherosclerotic ischemic stroke.FIG. 1.: A. Video-oculography (Interacoustics, Middelfart, Denmark) shows spontaneous left-beating nystagmus with a weak upbeat component. B. Gaze test shows horizontal direction-changing gaze-evoked nystagmus. C. Fundus photographs show abnormal extorsion of the right eye (16.2°) and intorsion of the left eye (−4.1°). D and E. Diffusion-weighted MRI demonstrates an acute infarction restricted to the left inferior cerebellar peduncle and dentate nucleus. LB indicates left beating; RB, right beating; SPV, slow angular velocity; UB, up beating.The presence of ipsilesional spontaneous nystagmus, ipsiversive falling, and contraversive OTR/SVV tilt was noted in patients with unilateral ICP lesions (1). Contraversive OTR and SVV tilt were reported in patients with unilateral dentate nucleus lesions (3). These findings were explained by the disinhibition of the cerebellar nodulus and dentate nucleus over the ipsilesional vestibular nuclear complex, generating a slow-phase drift of eyes toward the intact side and a fast-phase toward the lesion side (1). Body lateropulsion is an irresistible body thrust leading to a fall in individuals without vertigo, paresis, sensory loss, or cerebellar deficits. Patients with body lateropulsion have been reported in lesions involving the reticulospinal tract (1), the descending lateral vestibulospinal tract (1), the dorsal spinocerebellar tract (DSCT) (1), the vestibulo-thalamic pathway, the dentatorubrothalamic pathway, or the thalamocortical fascicle. A previous study described body ipsipulsion in patients with lesions involving the ICP (1). There are no previous reports of body lateropulsion because of an isolated unilateral dentate nucleus. However, damage to the cerebellothalamocortical projections could cause body lateropulsion (4). Body ipsipulsion has also been described in lesions involving the superior cerebellar peduncles (SCP) (4), and contrapulsion in lesions involving the red nucleus. The dentate nucleus receives proprioceptive information on the length and tension of muscle fibers via the ascending projections from DSCT running in the ICP. The dentate nucleus also receives descending projections from the premotor and supplementary motor cortices that are involved in planning and initiating voluntary movements. Its efferent projection passes through the SCP and contralateral red nucleus and ends in the contralateral ventrolateral thalamus where it participates in the timing and fine-tuning of random movements. The contrapulsion of the body observed in our patient suggests that lesions involving the dentate nucleus may cause body lateropulsion in the opposite direction although the effect of simultaneous damage to the ICP and dentate nucleus on body lateropulsion remains to be elucidated. Ocular contrapulsion refers to directional bias of eye motion away from the lesion side without restriction of eye motion. Ocular contrapulsion is often accompanied by saccadic lateropulsion (hypometric saccades toward the lesion and hypermetric saccades away from the lesion). Ocular contrapulsion has been reported in lesions involving the superior cerebellum or medial medulla by damaging the fibers from the fastigial nucleus to the paramedian pontine reticular formation or the olivocerebellar fibers before decussation (5). Ocular contrapulsion in our patient may be ascribed to interruption of the inhibitory fibers from Purkinje cells (PC) of the dorsal ocular motor vermis to the ipsilateral caudal fastigial nucleus or combined damage to the SCP that lies just above the ICP. Our patient showed horizontal GEN, indicating a failure of neural integration. Crucial structures for horizontal gaze holding are the medial vestibular nucleus, nucleus prepositus hypoglossi, flocculus, and paraflocculus (tonsil). Even though the ICP and dentate nucleus are not part of the neural integrator, GEN may occur because of interruption of cerebellar inflow from the brainstem integrators that passes through the ICP. Central positional nystagmus (CPN) was another finding in our patient. A previous report also described various patterns of CPN in patients with lesions involving the ICP, which may be ascribed to damage of the fibers running from the nodulus/uvula through the ICP to the vestibular nucleus (2). In conclusion, lesions involving the ICP and dentate nucleus may show ocular contrapulsion with ipsiversive spontaneous nystagmus, GEN, positional nystagmus, body contrapulsion, and contraversive OTR/SVV tilt. STATEMENT OF AUTHORSHIP Conception and design: X. Yang; Acquisition of data: Y. X. Wu, X. Ling, T. T. Zhao, Y. F. Feng, Z. X. Wang, J.-S. Kim; Analysis and interpretation of data: Y. X. Wu, X. Ling, T. T. Zhao, Y. F. Feng, Z. X. Wang, J.-S. Kim. Drafting the manuscript: Y. X. Wu, X. Ling; Revising the manuscript for intellectual content: Z. X. Wang, J.-S. Kim. Final approval of the completed manuscript: Y. X. Wu, X. Ling, T. T. Zhao, Y. F. Feng, Z. X. Wang, J.-S. Kim, X. Yang.