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Does Inferior-Olive Hypersynchrony Affect Vestibular Heading Perception?

  • Sinem Balta Beylergil
  • Palak Gupta
  • Aasef G. ShaikhEmail author
Original Paper

Abstract

Multisensory integration is critical for resolving ambiguities in isolated sensory systems assuring accurate perception of one’s own linear motion, i.e., heading. The vestibular signal, a critical source of information for heading perception, is transformed in appropriate coordinates suitable for multisensory integration—such transformation takes place under cerebellar supervision. Deficiency in cerebellar function due to Purkinje cell loss results in inaccurate multisensory integration and impaired heading perception. Here, we predict that a classic movement disorder, the syndrome of oculopalatal tremor (OPT), also presents with inaccurate heading direction perception. The characteristic feature of oculopalatal tremor is pseudohypertrophic inferior olive that constantly sends spontaneous, hypersynchronous, abnormal, and meaningless signals to the cerebellum. Such malicious olive signal can impair heading perception. We examined vestibular heading perception in 6 individuals with OPT and 9 age-matched healthy controls (HC). We used a two-alternative forced choice task performed during passive en bloc translation. Compared with age-matched HC, OPT group had significantly higher heading direction perception threshold indicating a less sensitive vestibular system to variations in heading direction. Using computational simulations, we show that the addition of the abnormal noise into the cerebellar system results in decreased spatiotemporal tuning behavior of the cerebellar output. Such impairment in spatiotemporal tuning causes reduced ability to perceive heading direction. Hyperactivity in the inferior-olive cerebellar pathway impairs the heading direction perception. We suggest that this impairment stems from abnormal noise into the cerebellum due to hypersynchronized inferior olive.

Keywords

Motion perception Inferior olive Cerebellum Multisensory integration 

Notes

Acknowledgments

The authors thank Dr. Mark Walker and Dr. Cameron McIntyre for the help and support. The authors also thank the medical illustration team of Cleveland Functional Electrical Stimulation (FES) Center.

Funding Information

This work was supported by the Career Development Award from the American Academy of Neurology, George C. Cotzias Memorial Fellowship (AGS), network models in dystonia grant from the Dystonia Medical Research Foundation, and the philanthropic support to the Department of Neurology at University Hospitals—The Alan Woll Fund.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interest.

References

  1. 1.
    Bertolini G, Ramat S, Bockisch CJ, Marti S, Straumann D, Palla A. Is vestibular self-motion perception controlled by the velocity storage? Insights from patients with chronic degeneration of the vestibulo-cerebellum. PLoS One. 2012;7:e36763.  https://doi.org/10.1371/journal.pone.0036763.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Shaikh AG. Motion perception without nystagmus—a novel manifestation of cerebellar stroke. J Stroke Cerebrovasc Dis. 2014;23:1148–56.  https://doi.org/10.1016/j.jstrokecerebrovasdis.2013.10.005.CrossRefPubMedGoogle Scholar
  3. 3.
    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;12:97–107.  https://doi.org/10.1007/s12311-012-0401-7.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Angelaki DE, Shaikh AG, Green AM, Dickman JD. Neurons compute internal models of the physical laws of motion. Nature. 2004;430:560–4.  https://doi.org/10.1038/nature02754.CrossRefPubMedGoogle Scholar
  5. 5.
    Gu Y, DeAngelis GC, Angelaki DE. A functional link between area MSTd and heading perception based on vestibular signals. Nat Neurosci. 2007;10:1038–47.  https://doi.org/10.1038/nn1935.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Shaikh AG, Green AM, Ghasia FF, Newlands SD, Dickman JD, Angelaki DE. Sensory convergence solves a motion ambiguity problem. Curr Biol. 2005;15:1657–62.  https://doi.org/10.1016/j.cub.2005.08.009.CrossRefPubMedGoogle Scholar
  7. 7.
    Shaikh AG, Meng H, Angelaki DE. Multiple reference frames for motion in the primate cerebellum. J Neurosci. 2004;24:4491–7.  https://doi.org/10.1523/JNEUROSCI.0109-04.2004.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    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;54:973–85.  https://doi.org/10.1016/j.neuron.2007.06.003.CrossRefPubMedGoogle Scholar
  9. 9.
    Ruigrok TJ, de Zeeuw CI, Voogd J. Hypertrophy of inferior olivary neurons: a degenerative, regenerative or plasticity phenomenon. Eur J Morphol. 1990;28:224–39.PubMedGoogle Scholar
  10. 10.
    Ruigrok TJ, Osse RJ, Voogd J. Organization of inferior olivary projections to the flocculus and ventral paraflocculus of the rat cerebellum. J Comp Neurol. 1992;316:129–50.  https://doi.org/10.1002/cne.903160202.CrossRefPubMedGoogle Scholar
  11. 11.
    Shaikh AG, Wong AL, Optican LM, Zee DS. Impaired motor learning in a disorder of the inferior olive: is the cerebellum confused? Cerebellum. 2017;16:158–67.  https://doi.org/10.1007/s12311-016-0785-x.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Crane BT. Fore-aft translation aftereffects. Exp Brain Res. 2012;219:477–87.  https://doi.org/10.1007/s00221-012-3105-9.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Crane BT. The influence of head and body tilt on human fore-aft translation perception. Exp Brain Res. 2014;232:3897–905.  https://doi.org/10.1007/s00221-014-4060-4.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Roditi RE, Crane BT. Suprathreshold asymmetries in human motion perception. Exp Brain Res. 2012;219:369–79.  https://doi.org/10.1007/s00221-012-3099-3.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Beylergil SB, Ozinga S, Walker MF, McIntyre CC, Shaikh AG. Vestibular heading perception in Parkinson’s disease. Prog Brain Res. 2019;249:307–19.  https://doi.org/10.1016/bs.pbr.2019.03.034.CrossRefPubMedGoogle Scholar
  16. 16.
    Bermudez Rey MC, Clark TK, Wang W, Leeder T, Bian Y, Merfeld DM. Vestibular perceptual thresholds increase above the age of 40. Front Neurol. 2016;7:162.  https://doi.org/10.3389/fneur.2016.00162.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Barnett-Cowan M, Dyde RT, Fox SH, Moro E, Hutchison WD, Harris LR. Multisensory determinants of orientation perception in Parkinson’s disease. Neuroscience. 2010;167:1138–50.  https://doi.org/10.1016/j.neuroscience.2010.02.065.CrossRefPubMedGoogle Scholar
  18. 18.
    Bertolini G, Wicki A, Baumann CR, Straumann D, Palla A. Impaired tilt perception in Parkinson’s disease: a central vestibular integration failure. PLoS One. 2015;10:e0124253.  https://doi.org/10.1371/journal.pone.0124253.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Shaikh AG, Straumann D, Palla A. Motion illusion-evidence towards human vestibulo-thalamic projections. Cerebellum. 2017;16:656–63.  https://doi.org/10.1007/s12311-017-0844-y.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    DeAngelis GC, Angelaki DE. Visual-vestibular integration for self-motion perception. In: Murray MM, Wallace MT, editors. The neural bases of multisensory processes. Boca Raton: CRC Press; 2012.Google Scholar
  21. 21.
    Yousif N, Bhatt H, Bain PG, Nandi D, Seemungal BM. The effect of pedunculopontine nucleus deep brain stimulation on postural sway and vestibular perception. Eur J Neurol. 2016;23:668–70.  https://doi.org/10.1111/ene.12947.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Shaikh AG, Hong S, Liao K, Tian J, Solomon D, Zee DS, et al. Oculopalatal tremor explained by a model of inferior olivary hypertrophy and cerebellar plasticity. Brain. 2010;133:923–40.  https://doi.org/10.1093/brain/awp323.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT. Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. Brain. 1996;119(Pt 4):1183–98.  https://doi.org/10.1093/brain/119.4.1183.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Department of Biomedical EngineeringCase Western Reserve UniversityClevelandUSA
  2. 2.Daroff-Dell’Osso Ocular Motility and Vestibular Laboratory, National VA Parkinson Consortium Center, Neurology ServiceLouis Stokes Cleveland VA Medical CenterClevelandUSA
  3. 3.Department of NeurologyCase Western Reserve UniversityClevelandUSA
  4. 4.Neurological InstituteUniversity HospitalsClevelandUSA

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