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Published in: Journal of Neurology 4/2016

01-04-2016 | Original Communication

Modulation of central nystagmus by vision, proprioception, and efference copy signals: a systematic evaluation

Authors: Jeong-Yoon Choi, Ji-Soo Kim

Published in: Journal of Neurology | Issue 4/2016

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Abstract

Non-vestibular sensorimotor signals modulate the vestibular nucleus neuron to achieve current behavioral goals, and may generate or modulate nystagmus. In central lesions affecting the vestibular nuclei, non-vestibular signals such as mastication or swallowing may induce nystagmus. However, the influence of non-vestibular signals on these types of nystagmus has not been investigated in a systematic way and the underlying mechanisms of the modulation are poorly understood. In this study, several non-vestibular sensorimotor stimuli were applied to evaluate the patterns of nystagmus modulation in a patient with suspected rhombencephalitis or imaging negative small infarction, probably involving the left dorsolateral medulla. The nystagmus was induced or significantly modulated by (1) visual inputs, and (2) combined proprioceptive and efference copy signals (during voluntary motion) unrelated to body or head orientation. In contrast, isolated proprioceptive signal, mental set, or non-proprioceptive somatosensory inputs showed a negligible effect on the induction of nystagmus. Based on these modulations, we suggest that (1) the visually mediated nystagmus is due to a lesion-induced pursuit asymmetry, and (2) the nystagmus induced during voluntary motion is due to erroneous contribution of combined proprioceptive and efference copy signals during integration of non-vestibular signals for ocular motor control. Various non-vestibular sensorimotor stimulations may induce nystagmus due to dysfunction of the central vestibular neural circuity.
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Literature
3.
go back to reference Cullen KE, McCrea RA (1993) Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex, I. Secondary vestibular neurons. J Neurophysiol 70(2):828–843PubMed Cullen KE, McCrea RA (1993) Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex, I. Secondary vestibular neurons. J Neurophysiol 70(2):828–843PubMed
4.
go back to reference Gauthier GM, Vercher JL (1990) Visual vestibular interaction: vestibulo-ocular reflex suppression with head-fixed target fixation. Exp Brain Res 81(1):150–160CrossRefPubMed Gauthier GM, Vercher JL (1990) Visual vestibular interaction: vestibulo-ocular reflex suppression with head-fixed target fixation. Exp Brain Res 81(1):150–160CrossRefPubMed
5.
go back to reference Brandt T, Buchele W, Arnold F (1977) Arthrokinetic nystagmus and ego-motion sensation. Exp Brain Res 30(2–3):331–338PubMed Brandt T, Buchele W, Arnold F (1977) Arthrokinetic nystagmus and ego-motion sensation. Exp Brain Res 30(2–3):331–338PubMed
8.
go back to reference Hood JD, Korres S (1979) Vestibular suppression in peripheral and central vestibular disorders. Brain 102(4):785–804CrossRefPubMed Hood JD, Korres S (1979) Vestibular suppression in peripheral and central vestibular disorders. Brain 102(4):785–804CrossRefPubMed
9.
go back to reference Dieterich M, Bauermann T, Best C, Stoeter P, Schlindwein P (2007) Evidence for cortical visual substitution of chronic bilateral vestibular failure (an fMRI study). Brain 130(Pt 8):2108–2116. doi:10.1093/brain/awm130 CrossRefPubMed Dieterich M, Bauermann T, Best C, Stoeter P, Schlindwein P (2007) Evidence for cortical visual substitution of chronic bilateral vestibular failure (an fMRI study). Brain 130(Pt 8):2108–2116. doi:10.​1093/​brain/​awm130 CrossRefPubMed
11.
go back to reference Alpert JN (1974) Failure of fixation suppression: a pathologic effect of vision on caloric nystagmus. Neurology 24(9):891–896CrossRefPubMed Alpert JN (1974) Failure of fixation suppression: a pathologic effect of vision on caloric nystagmus. Neurology 24(9):891–896CrossRefPubMed
12.
go back to reference Takemori S, Cohen B (1974) Loss of visual suppression of vestibular nystagmus after flocculus lesions. Brain Res 72(2):213–224CrossRefPubMed Takemori S, Cohen B (1974) Loss of visual suppression of vestibular nystagmus after flocculus lesions. Brain Res 72(2):213–224CrossRefPubMed
18.
go back to reference Collewijn H, Tamminga EP (1984) Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. J Physiol 351:217–250CrossRefPubMedPubMedCentral Collewijn H, Tamminga EP (1984) Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. J Physiol 351:217–250CrossRefPubMedPubMedCentral
23.
go back to reference Takemori S, Aiba T, Shizawa R (1981) Visual suppression of caloric nystagmus in brain-stem lesions. Ann N Y Acad Sci 374:846–854CrossRefPubMed Takemori S, Aiba T, Shizawa R (1981) Visual suppression of caloric nystagmus in brain-stem lesions. Ann N Y Acad Sci 374:846–854CrossRefPubMed
25.
go back to reference Kileny P, McCabe BF, Ryu JH (1980) Effects of attention-requiring tasks on vestibular nystagmus. Ann Otol Rhinol Laryngol 89(1 Pt 1):9–12CrossRefPubMed Kileny P, McCabe BF, Ryu JH (1980) Effects of attention-requiring tasks on vestibular nystagmus. Ann Otol Rhinol Laryngol 89(1 Pt 1):9–12CrossRefPubMed
26.
go back to reference McGovern TN, Fitzgerald JE (2008) The effect of mental alerting on peripheral vestibular nystagmus during spontaneous, gaze (30 degrees left, 30 degrees right) and body positional (left and right lateral lying) testing using electronystagmography (ENG). Int J Audiol 47(10):601–606. doi:10.1080/14992020802123579 CrossRefPubMed McGovern TN, Fitzgerald JE (2008) The effect of mental alerting on peripheral vestibular nystagmus during spontaneous, gaze (30 degrees left, 30 degrees right) and body positional (left and right lateral lying) testing using electronystagmography (ENG). Int J Audiol 47(10):601–606. doi:10.​1080/​1499202080212357​9 CrossRefPubMed
27.
go back to reference Davis RI, Mann RC (1987) The effects of alerting tasks on caloric induced vestibular nystagmus. Ear Hear 8(1):58–60CrossRefPubMed Davis RI, Mann RC (1987) The effects of alerting tasks on caloric induced vestibular nystagmus. Ear Hear 8(1):58–60CrossRefPubMed
28.
go back to reference Leigh RJ, Zee DS (2006) The neurology of eye movements, 4th edn. Oxford University Press, New York Leigh RJ, Zee DS (2006) The neurology of eye movements, 4th edn. Oxford University Press, New York
29.
go back to reference Roy JE, Cullen KE (2001) Passive activation of neck proprioceptive inputs does not influence the discharge patterns of vestibular nuclei neurons. Ann N Y Acad Sci 942:486–489CrossRefPubMed Roy JE, Cullen KE (2001) Passive activation of neck proprioceptive inputs does not influence the discharge patterns of vestibular nuclei neurons. Ann N Y Acad Sci 942:486–489CrossRefPubMed
31.
go back to reference Bles W, Jelmorini M, Bekkering H, de Graaf B (1995) Arthrokinetic information affects linear self-motion perception. J Vestib Res 5(2):109–116CrossRefPubMed Bles W, Jelmorini M, Bekkering H, de Graaf B (1995) Arthrokinetic information affects linear self-motion perception. J Vestib Res 5(2):109–116CrossRefPubMed
33.
go back to reference Guedry FE, Benson AJ (1983) Modification of per- and postrotational responses by voluntary motor activity of the limbs. Exp Brain Res 52(2):190–198CrossRefPubMed Guedry FE, Benson AJ (1983) Modification of per- and postrotational responses by voluntary motor activity of the limbs. Exp Brain Res 52(2):190–198CrossRefPubMed
Metadata
Title
Modulation of central nystagmus by vision, proprioception, and efference copy signals: a systematic evaluation
Authors
Jeong-Yoon Choi
Ji-Soo Kim
Publication date
01-04-2016
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 4/2016
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-016-8032-4

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