Skip to main content
Top
Published in: The Cerebellum 5/2021

01-10-2021 | Gaze-Evoked Nystagmus | Original Paper

Asymmetry in Gaze-Holding Impairment in Acute Unilateral Ischemic Cerebellar Lesions Critically Depends on the Involvement of the Caudal Vermis and the Dentate Nucleus

Authors: F. Romano, C. J. Bockisch, B. Schuknecht, G. Bertolini, Alexander A. Tarnutzer

Published in: The Cerebellum | Issue 5/2021

Login to get access

Abstract

Stabilizing the eyes in space when looking at a target is provided by a brainstem/cerebellar gaze-holding network, including the flocculus/paraflocculus complex (non-human primate studies) and the caudal vermis, biventer, and inferior semilunar lobule (human studies). Previous research suggests that acute lateralized cerebellar lesions preferentially lead to gaze-evoked nystagmus (GEN) on ipsilesional gaze. Here, we further characterize the effect of unilateral cerebellar lesions on gaze-holding and hypothesize that the side-specific magnitude of gaze-holding impairment depends on the lesion location. Nine patients (age range = 31–62 years) with acute/subacute (≤ 10 days old) MRI-confirmed unilateral cerebellar stroke were included. Horizontal gaze holding was quantified while looking at a slowly moving (0.5°/s) flashing target (gaze angle = ±40°). Asymmetry in eye-drift velocity was calculated and compared with the different MRI patterns of cerebellar lesions. Individual peak eye-drift velocities (range = 1.7–8.8°/s) occurred at the most eccentric eye positions (gaze angle = 28–38°). We found significantly asymmetric eye-drift velocity (EDV) in eight out of nine patients. The four patients with MRI-confirmed involvement of the caudal vermis and the dentate nucleus all presented with ipsilesionally-predominant EDV, while in the five patients with lesions restricted to the cerebellar hemisphere, EDV was stronger on contralesional gaze in three out of four found with an asymmetric EDV. Involvement of the caudal vermis and the dentate nucleus is critical for determining the directional GEN asymmetry in unilateral cerebellar lesions. Thus, our findings support the occurrence of GEN without floccular/parafloccular lesions and suggest that the EDV asymmetry in relation to the side of the lesion provides information about the involvement of specific structures.
Literature
2.
go back to reference Stahl JS, Averbuch-Heller L, Leigh RJ. Acquired nystagmus. Arch Ophthalmol. 2000;118:544–9.CrossRef Stahl JS, Averbuch-Heller L, Leigh RJ. Acquired nystagmus. Arch Ophthalmol. 2000;118:544–9.CrossRef
4.
go back to reference Holmes G. A form of familial degeneration of the cerebellum. Brain. 1907;30:466–88.CrossRef Holmes G. A form of familial degeneration of the cerebellum. Brain. 1907;30:466–88.CrossRef
5.
go back to reference Cannon SC, Robinson DA. Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. J Neurophysiol. 1987;57:1383–409.CrossRef Cannon SC, Robinson DA. Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. J Neurophysiol. 1987;57:1383–409.CrossRef
7.
go back to reference Robinson DA. The effect of cerebellectomy on the cat's vestibulo-ocular integrator. Brain Res. 1974;71:195–207.CrossRef Robinson DA. The effect of cerebellectomy on the cat's vestibulo-ocular integrator. Brain Res. 1974;71:195–207.CrossRef
8.
go back to reference Godaux E, Cheron G. The hypothesis of the uniqueness of the oculomotor neural integrator: direct experimental evidence in the cat. J Physiol. 1996;492(Pt 2):517–27.CrossRef Godaux E, Cheron G. The hypothesis of the uniqueness of the oculomotor neural integrator: direct experimental evidence in the cat. J Physiol. 1996;492(Pt 2):517–27.CrossRef
11.
go back to reference Crawford JD. The oculomotor neural integrator uses a behavior-related coordinate system. J Neurosci. 1994;14:6911–23.CrossRef Crawford JD. The oculomotor neural integrator uses a behavior-related coordinate system. J Neurosci. 1994;14:6911–23.CrossRef
20.
go back to reference Bogousslavsky J, Meienberg O. Eye-movement disorders in brain-stem and cerebellar stroke. Arch Neurol. 1987;44:141–8.CrossRef Bogousslavsky J, Meienberg O. Eye-movement disorders in brain-stem and cerebellar stroke. Arch Neurol. 1987;44:141–8.CrossRef
21.
go back to reference Kase CS, Norrving B, Levine SR, Babikian VL, Chodosh EH, Wolf PA, et al. Cerebellar infarction. Clinical and anatomic observations in 66 cases. Stroke. 1993;24:76–83.CrossRef Kase CS, Norrving B, Levine SR, Babikian VL, Chodosh EH, Wolf PA, et al. Cerebellar infarction. Clinical and anatomic observations in 66 cases. Stroke. 1993;24:76–83.CrossRef
22.
go back to reference Burde RM, Stroud MH, Roper-Hall G, Wirth FP, O'Leary JL. Ocular motor dysfunction in total and hemicerebellectomized monkeys. Br J Ophthalmol. 1975;59:560–5.CrossRef Burde RM, Stroud MH, Roper-Hall G, Wirth FP, O'Leary JL. Ocular motor dysfunction in total and hemicerebellectomized monkeys. Br J Ophthalmol. 1975;59:560–5.CrossRef
23.
go back to reference Zee DS, Yamazaki A, Butler PH, Gucer G. Effects of ablation of flocculus and paraflocculus of eye movements in primate. J Neurophysiol. 1981;46:878–99.CrossRef Zee DS, Yamazaki A, Butler PH, Gucer G. Effects of ablation of flocculus and paraflocculus of eye movements in primate. J Neurophysiol. 1981;46:878–99.CrossRef
26.
go back to reference Schneider E, Dera T, Bard K, Bardins S, Boening G, Brandt T. Eye movement driven head-mounted camera: it looks where the eyes look. IEEE Conf Syst, Man Cybern. 2005;3:2437–42. Schneider E, Dera T, Bard K, Bardins S, Boening G, Brandt T. Eye movement driven head-mounted camera: it looks where the eyes look. IEEE Conf Syst, Man Cybern. 2005;3:2437–42.
27.
go back to reference Dera T, Boening G, Bardins S, Schneider E. Low-latency video tracking of horizontal, vertical, and torsional eye movements as a basis for 3-DOF realtime motion control of a head-mounted camera. IEEE Conf Syst, Man Cybern. 2006;6:5191–6. Dera T, Boening G, Bardins S, Schneider E. Low-latency video tracking of horizontal, vertical, and torsional eye movements as a basis for 3-DOF realtime motion control of a head-mounted camera. IEEE Conf Syst, Man Cybern. 2006;6:5191–6.
30.
go back to reference Carleton SC, Carpenter MB. Distribution of primary vestibular fibers in the brainstem and cerebellum of the monkey. Brain Res. 1984;294:281–98.CrossRef Carleton SC, Carpenter MB. Distribution of primary vestibular fibers in the brainstem and cerebellum of the monkey. Brain Res. 1984;294:281–98.CrossRef
33.
go back to reference Voogd J, Gerrits NM, Ruigrok TJ. Organization of the vestibulocerebellum. Ann N Y Acad Sci. 1996;781:553–79.CrossRef Voogd J, Gerrits NM, Ruigrok TJ. Organization of the vestibulocerebellum. Ann N Y Acad Sci. 1996;781:553–79.CrossRef
36.
go back to reference Lee H, Yi HA, Cho YW, Sohn CH, Whitman GT, Ying S, et al. Nodulus infarction mimicking acute peripheral vestibulopathy. Neurology. 2003;60:1700–2.CrossRef Lee H, Yi HA, Cho YW, Sohn CH, Whitman GT, Ying S, et al. Nodulus infarction mimicking acute peripheral vestibulopathy. Neurology. 2003;60:1700–2.CrossRef
41.
go back to reference Leigh RJ, Zee DS. The neurology of eye movements. 5th ed. New York: Oxford University Press; 2015.CrossRef Leigh RJ, Zee DS. The neurology of eye movements. 5th ed. New York: Oxford University Press; 2015.CrossRef
42.
go back to reference Lee SH, Park SH, Kim JS, Kim HJ, Yunusov F, Zee DS. Isolated unilateral infarction of the cerebellar tonsil: ocular motor findings. Ann Neurol. 2014;75:429–34.CrossRef Lee SH, Park SH, Kim JS, Kim HJ, Yunusov F, Zee DS. Isolated unilateral infarction of the cerebellar tonsil: ocular motor findings. Ann Neurol. 2014;75:429–34.CrossRef
Metadata
Title
Asymmetry in Gaze-Holding Impairment in Acute Unilateral Ischemic Cerebellar Lesions Critically Depends on the Involvement of the Caudal Vermis and the Dentate Nucleus
Authors
F. Romano
C. J. Bockisch
B. Schuknecht
G. Bertolini
Alexander A. Tarnutzer
Publication date
01-10-2021
Publisher
Springer US
Published in
The Cerebellum / Issue 5/2021
Print ISSN: 1473-4222
Electronic ISSN: 1473-4230
DOI
https://doi.org/10.1007/s12311-020-01141-7

Other articles of this Issue 5/2021

The Cerebellum 5/2021 Go to the issue