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Impaired Tilt Suppression of Post-Rotatory Nystagmus and Cross-Coupled Head-Shaking Nystagmus in Cerebellar Lesions: Image Mapping Study

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Abstract

We sought to determine the cerebellar structures responsible for tilt suppression of post-rotatory nystagmus. We investigated ocular motor findings and MRI lesions in 73 patients with isolated cerebellar lesions who underwent recording of the vestibulo-ocular reflex (VOR) using rotatory chair tests. Tilt suppression of post-rotatory nystagmus was diminished in 27 patients (27/73, 37.0 %). The gains of the VOR and the TCs of per- and post-rotatory nystagmus did not differ between the patients with diminished and with normal tilt suppression. The patients with impaired tilt suppression showed perverted (“cross-coupled”) head-shaking nystagmus (pHSN) and central positional nystagmus (CPN) more frequently than those with normal responses. Tilt suppression was impaired in five (71.4 %) of the seven patients with isolated nodulus and uvular infarction. Probabilistic lesion-mapping analysis showed that the nodulus and uvula are responsible for tilt suppression. Impaired tilt suppression may be ascribed to disruption of cerebellar contribution to the vestibular velocity-storage mechanism, which integrates information from the semicircular canals and otolith organs to help derive the brain’s estimate of the head orientation relative to the pull of gravity.

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References

  1. Baloh RW, Kerber K. Baloh and Honrubia’s clinical neurophysiology of the vestibular system. New York: Oxford University Press; 2010.

    Google Scholar 

  2. Cohen B, Henn V, Raphan T, Dennett D. Velocity storage, nystagmus, and visual-vestibular interactions in humans. Ann N Y Acad Sci. 1981;374(1):421–33.

    Article  CAS  PubMed  Google Scholar 

  3. Dai M, Klein A, Cohen B, Raphan T. Model-based study of the human cupular time constant. J Vestib Res. 1998;9(4):293–301.

    Google Scholar 

  4. Leigh RJ, Zee DS. The neurology of eye movements. 4th ed. New York: Oxford University Press; 2006.

    Google Scholar 

  5. Cohen B, Matsuo V, Raphan T. Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus. J Physiol. 1977;270:321–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Laurens J, Angelaki DE. The functional significance of velocity storage and its dependence on gravity. Exp Brain Res. 2011;210:407–22.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Solomon D, Cohen B. Stabilization of gaze during circular locomotion in darkness. II. Contribution of velocity storage to compensatory eye and head nystagmus in the running monkey. J Neurophysiol. 1992;67:1158–70.

    CAS  PubMed  Google Scholar 

  8. Raphan T, Sturm D. Modeling the spatiotemporal organization of velocity storage in the vestibuloocular reflex by optokinetic studies. J Neurophysiol. 1991;66:1410–21.

    CAS  PubMed  Google Scholar 

  9. Waespe W, Cohen B, Raphan T. Dynamic modification of the vestibulo-ocular reflex by the nodulus and uvula. Science. 1985;228:199–202.

    Article  CAS  PubMed  Google Scholar 

  10. Raphan T, Cohen B, Henn V. Effects of gravity on rotatory nystagmus in monkeys. Ann N Y Acad Sci. 1981;374:44–55.

    Article  CAS  PubMed  Google Scholar 

  11. Kushiro K, Dai M, Kunin M, Yakushin SB, Cohen B, Raphan T. Compensatory and orienting eye movements induced by off-vertical axis rotation (OVAR) in monkeys. J Neurophysiol. 2002;88:2445–62.

    Article  PubMed  Google Scholar 

  12. Sheliga BM, Yakushin SB, Silvers A, Raphan T, Cohen B. Control of spatial orientation of the angular vestibulo-ocular reflex by the nodulus and uvula of the vestibulocerebellum. Ann N Y Acad Sci. 1999;871:94–122.

    Article  CAS  PubMed  Google Scholar 

  13. Wiest G, Deecke L, Trattnig S, Mueller C. Abolished tilt suppression of the vestibulo-ocular reflex caused by a selective uvulo-nodular lesion. Neurology. 1999;52(2):417–9.

    Article  CAS  PubMed  Google Scholar 

  14. Moon IS, Kim JS, Choi KD, Kim MJ, Oh SY, Lee H, et al. Isolated nodular infarction. Stroke. 2009;40(2):487–91.

    Article  PubMed  Google Scholar 

  15. Hain T, Zee D, Maria B. Tilt suppression of vestibulo-ocular reflex in patients with cerebellar lesions. Acta Otolaryngol. 1988;105:13–20.

    Article  CAS  PubMed  Google Scholar 

  16. Huh YE, Kim JS. Bedside evaluation of dizzy patients. J Clin Neurol. 2013;9:203–13.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Choi J-Y, Kim JH, Kim HJ, Glasauer S, Kim J-S. Central paroxysmal positional nystagmus characteristics and possible mechanisms. Neurology. 2015;84:2238–46.

    Article  PubMed  Google Scholar 

  18. Choi KD, Oh SY, Park SH, Kim JH, Koo JW, Kim JS. Head-shaking nystagmus in lateral medullary infarction patterns and possible mechanisms. Neurology. 2007;68(17):1337–44.

    Article  PubMed  Google Scholar 

  19. Yang Y, Kim JS, Kim S, Kim YK, Kwak YT, Han IW. Cerebellar hypoperfusion during transient global amnesia: an MRI and oculographic study. J Clin Neurol. 2009;5(2):74–80.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Choi KD, Kim JS. Head‐shaking nystagmus in central vestibulopathies. Ann N Y Acad Sci. 2009;1164:338–43.

    Article  PubMed  Google Scholar 

  21. Jeong SH, Oh SY, Kim HJ, Koo JW, Kim JS. Vestibular dysfunction in migraine: effects of associated vertigo and motion sickness. J Neurol. 2010;257(6):905–12.

    Article  PubMed  Google Scholar 

  22. Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. Neuroimage. 2006;33(1):127–38.

    Article  PubMed  Google Scholar 

  23. Huh YE, Kim JS. Patterns of spontaneous and head-shaking nystagmus in cerebellar infarction: imaging correlations. Brain. 2011;134(12):3662–71.

    Article  PubMed  Google Scholar 

  24. Voogd J, Gerrits NM, Ruigrok TJ. Organization of the vestibulocerebellum. Ann N Y Acad Sci. 1996;781(1):553–79.

    Article  CAS  PubMed  Google Scholar 

  25. Shojaku H, Sato Y, Ikarashi K, Kawasaki T. Topographical distribution of Purkinje cells in the uvula and the nodulus projecting to the vestibular nuclei in cats. Brain Res. 1987;416(1):100–12.

    Article  CAS  PubMed  Google Scholar 

  26. Shaikh AG, Palla A, Marti S, Olasagasti I, Optican LM, Zee DS, et al. Role of cerebellum in motion perception and vestibulo-ocular reflex—similarities and disparities. Cerebellum. 2013;12(1):97–107.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Carleton SC, Carpenter MB. Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey. Brain Res. 1983;278(1):29–51.

    Article  CAS  PubMed  Google Scholar 

  28. Angelaki DE, Hess BJ. Inertial representation of angular motion in the vestibular system of rhesus monkeys. II. Otolith-controlled transformation that depends on an intact cerebellar nodulus. J Neurophysiol. 1995;73:1729–51.

    CAS  PubMed  Google Scholar 

  29. Yakusheva TA, Shaikh AG, Green AM, Blazquez PM, Dickman JD, Angelaki DE. Purkinje cells in posterior cerebellar vermis encode motion in an inertial reference frame. Neuron. 2007;54(6):973–85.

    Article  CAS  PubMed  Google Scholar 

  30. Meng H, Blázquez PM, Dickman JD, Angelaki DE. Diversity of vestibular nuclei neurons targeted by cerebellar nodulus inhibition. J Physiol. 2014;592:171–88.

    Article  CAS  PubMed  Google Scholar 

  31. Wearne S, Raphan T, Cohen B. Nodulo-uvular control of central vestibular dynamics determines spatial orientation of the angular vestibulo-ocular reflexa. Ann N Y Acad Sci. 1996;781:364–84.

    Article  CAS  PubMed  Google Scholar 

  32. Solomon D, Cohen B. Stimulation of the nodulus and uvula discharges velocity storage in the vestibulo-ocular reflex. Exp Brain Res. 1994;102:57–68.

    Article  CAS  PubMed  Google Scholar 

  33. Furman JM, Wall C, Pang D. Vestibular function in periodic alternating nystagmus. Brain. 1990;113(5):1425–39.

    Article  PubMed  Google Scholar 

  34. Shaikh AG. Motion perception without nystagmus—a novel manifestation of cerebellar stroke. J Stroke Cerebrovasc Dis. 2014;23:1148–56.

    Article  PubMed  Google Scholar 

  35. Shaikh AG, Marti S, Tarnutzer AA, Palla A, Crawford TO, Straumann D, et al. Ataxia telangiectasia: a “disease model” to understand the cerebellar control of vestibular reflexes. J Neurophysiol. 2011;105:3034–41.

    Article  PubMed  Google Scholar 

  36. Walker MF, Zee DS. Directional abnormalities of vestibular and optokinetic responses in cerebellar disease. Ann N Y Acad Sci. 1999;871:205–20.

    Article  CAS  PubMed  Google Scholar 

  37. Palla A, Marti S, Straumann D. Head-shaking nystagmus depends on gravity. J Assoc Res Otolaryngol. 2005;6(1):1–8.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Waespe W, Büttner U, Henn V. Visual-vestibular interaction in the flocculus of the alert monkey. Exp Brain Res. 1981;43(3–4):337–48.

    Article  CAS  PubMed  Google Scholar 

  39. Park HK, Kim JS, Strupp M, Zee DS. Isolated floccular infarction: impaired vestibular responses to horizontal head impulse. J Neurol. 2013;260(6):1576–82.

    Article  PubMed  Google Scholar 

  40. Waespe W, Cohen B, Raphan T. Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interactions: effects of lesions. Exp Brain Res. 1983;50:9–33.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by a grant of the Korea Healthcare technology R&D Project, Ministry of Health and Welfare, Republic of Korea (HI10C2020).

Author Contributions

Dr. Lee wrote the manuscript and analyzed and interpreted the data.

Drs. Choi, Park, Koo, H.J. Kim, and Zee analyzed and interpreted the data and revised the manuscript.

Dr. J.S. Kim conducted the design, and conceptualized the study, interpreted the data, and revised the manuscript.

Author information

Authors and Affiliations

  1. Department of Neurology, Ajou University School of Medicine, Ajou University Hospital, Suwon, South Korea

    Sun-Uk Lee

  2. Department of Neurology, Seoul National University College of Medicine, Seoul National University Bundang Hospital, 173-82 Gumi-ro, Bundang-gu, Seongnam-si, Gyeonggi-do, 463-707, South Korea

    Jeong-Yoon Choi & Ji-Soo Kim

  3. Department of Biomedical Laboratory Science, Kyungdong University, Goseong-gun, Gangwon-do, South Korea

    Hyo-Jung Kim

  4. Department of Neurology, Konkuk University School of Medicine, Konkuk University Hospital, Seoul, South Korea

    Jeong-Jin Park

  5. Department of Neurology, Otolaryngology Head and Neck Surgery, Neuroscience, and Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    David S. Zee

Authors
  1. Sun-Uk Lee
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  2. Jeong-Yoon Choi
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Corresponding author

Correspondence to Ji-Soo Kim.

Ethics declarations

Study Ethics

All experiments followed the tenets of the Declaration of Helsinki and this study was approved by the Institutional Review Board of Seoul National University Bundang Hospital (B-1505-298-107).

Conflict of Interest

The authors declare that they have no conflict of interest.

Disclosures

Drs. Lee, Choi, Park, and Koo and H.J. Kim report no disclosure.

Dr. J.S. Kim serves as an associate editor of Frontiers in Neuro-otology and on the editorial boards of the Journal of Korean Society of Clinical Neurophysiology, Journal of Clinical Neurology, Frontiers in Neuro-ophthalmology, Journal of Neuro-ophthalmology, Journal of Vestibular Research, Journal of Neurology, and Medicine and received research support from SK Chemicals, Co. Ltd.

Dr. Zee receives research support from the National Institutes of Health and is an Associate Editor of Frontiers in Neuro-otology and a member of the Editorial Board of The Cerebellum. He received speaker’s honoraria from Abbott, Micromed, Sun pharmaceuticals, and the American Academy of Neurology.

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Lee, SU., Choi, JY., Kim, HJ. et al. Impaired Tilt Suppression of Post-Rotatory Nystagmus and Cross-Coupled Head-Shaking Nystagmus in Cerebellar Lesions: Image Mapping Study. Cerebellum 16, 95–102 (2017). https://doi.org/10.1007/s12311-016-0772-2

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  • DOI: https://doi.org/10.1007/s12311-016-0772-2

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