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Motion Illusion—Evidence towards Human Vestibulo-Thalamic Projections

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Abstract

Contemporary studies speculated that cerebellar network responsible for motion perception projects to the cerebral cortex via vestibulo-thalamus. Here, we sought for the physiological properties of vestibulo-thalamic pathway responsible for the motion perception. Healthy subjects and the patient with focal vestibulo-thalamic lacunar stroke spun a hand-held rheostat to approximate the value of perceived angular velocity during whole-body passive earth-vertical axis rotations in yaw plane. Vestibulo-ocular reflex was simultaneously measured with high-resolution search coils (paradigm 1). In primates, the vestibulo-thalamic projections remain medial and then dorsomedial to the subthalamus. Therefore, the paradigm 2 assessed the effects of high-frequency subthalamic nucleus electrical stimulation through the medial and caudal deep brain stimulation electrode in five subjects with Parkinson’s disease. Paradigm 1 discovered directional mismatch of perceived rotation in a patient with vestibulo-thalamic lacune. There was no such mismatch in vestibulo-ocular reflex. Healthy subjects did not have such directional discrepancy of perceived motion. The results confirmed that perceived angular motion is relayed through the thalamus. Stimulation through medial and caudal-most electrode of subthalamic deep brain stimulator in paradigm 2 resulted in perception of rotational motion in the horizontal semicircular canal plane. One patient perceived riding a swing, a complex motion, possibly the combination of vertical canal and otolith-derived signals representing pitch and fore-aft motion, respectively. The results examined physiological properties of the vestibulo-thalamic pathway that passes in proximity to the subthalamic nucleus conducting pure semicircular canal signals and convergent signals from the semicircular canals and the otoliths.

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References

  1. 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. doi:10.1016/j.neuron.2007.06.003.

    Article  CAS  PubMed  Google Scholar 

  2. Shaikh AG, Palla A, Marti S, Olasagasti I, Optican LM, Zee DS, Straumann D. Role of cerebellum in motion perception and vestibulo-ocular reflex-similarities and disparities. Cerebellum. 2013;12:97–107. doi:10.1007/s12311-012-0401-7.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Shaikh AG, Meng H, Angelaki DE. Multiple reference frames for motion in the primate cerebellum. J Neurosci. 2004;24:4491–7. doi:10.1523/JNEUROSCI.0109-04.2004.

    Article  CAS  PubMed  Google Scholar 

  4. 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. doi:10.1016/j.cub.2005.08.009.

    Article  CAS  PubMed  Google Scholar 

  5. Shaikh AG. Motion perception without nystagmus—a novel manifestation of cerebellar stroke. J Stroke Cerebrovasc Dis. 2014;23:1148–56. doi:10.1016/j.jstrokecerebrovasdis.2013.10.005.

    Article  PubMed  Google Scholar 

  6. Green AM, Shaikh AG, Angelaki DE. Sensory vestibular contributions to constructing internal models of self-motion. J Neural Eng. 2005;2:S164–79. doi:10.1088/1741-2560/2/3/S02.

    Article  PubMed  Google Scholar 

  7. Angelaki DE, Shaikh AG, Green AM, Dickman JD. Neurons compute internal models of the physical laws of motion. Nature. 2004;430:560–4. doi:10.1038/nature02754.

    Article  CAS  PubMed  Google Scholar 

  8. 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. doi:10.1371/journal.pone.0124253.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Bertolini G, Ramat S, Laurens J, Bockisch CJ, Marti S, Straumann D, Palla A. Velocity storage contribution to vestibular self-motion perception in healthy human subjects. J Neurophysiol. 2011;105:209–23. doi:10.1152/jn.00154.2010.

    Article  CAS  PubMed  Google Scholar 

  10. 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. doi:10.1371/journal.pone.0036763.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 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; doi:10.1111/ene.12947.

    PubMed  PubMed Central  Google Scholar 

  12. Seemungal BM, Masaoutis P, Green DA, Plant GT, Bronstein AM. Symptomatic recovery in miller fisher syndrome parallels vestibular-perceptual and not vestibular-ocular reflex function. Front Neurol. 2011;2:2. doi:10.3389/fneur.2011.00002.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Meng H, May PJ, Dickman JD, Angelaki DE. Vestibular signals in primate thalamus: properties and origins. J Neurosci. 2007;27:13590–602. doi:10.1523/JNEUROSCI.3931-07.2007.

    Article  CAS  PubMed  Google Scholar 

  14. Meng H, Angelaki DE. Responses of ventral posterior thalamus neurons to three-dimensional vestibular and optic flow stimulation. J Neurophysiol. 2010;103:817–26. doi:10.1152/jn.00729.2009.

    Article  PubMed  Google Scholar 

  15. Liu S, Yakusheva T, Deangelis GC, Angelaki DE. Direction discrimination thresholds of vestibular and cerebellar nuclei neurons. J Neurosci. 2010;30:439–48. doi:10.1523/JNEUROSCI.3192-09.2010.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Kleine JF, Guan Y, Kipiani E, Glonti L, Hoshi M, Buttner U. Trunk position influences vestibular responses of fastigial nucleus neurons in the alert monkey. J Neurophysiol. 2004;91:2090–100. doi:10.1152/jn.00849.2003.

    Article  CAS  PubMed  Google Scholar 

  17. Hawrylyshyn PA, Rubin AM, Tasker RR, Organ LW, Fredrickson JM. Vestibulothalamic projections in man—a sixth primary sensory pathway. J Neurophysiol. 1978;41:394–401.

    CAS  PubMed  Google Scholar 

  18. Nigmatullina Y, Hellyer PJ, Nachev P, Sharp DJ, Seemungal BM. The neuroanatomical correlates of training-related perceptuo-reflex uncoupling in dancers. Cereb Cortex. 2015;25:554–62. doi:10.1093/cercor/bht266.

    Article  PubMed  Google Scholar 

  19. Bergamin O, Zee DS, Roberts DC, Landau K, Lasker AG, Straumann D. Three-dimensional Hess screen test with binocular dual search coils in a three-field magnetic system. Invest Ophthalmol Vis Sci. 2001;42:660–7.

    CAS  PubMed  Google Scholar 

  20. Okada T, Grunfeld E, Shallo-Hoffmann J, Bronstein AM. Vestibular perception of angular velocity in normal subjects and in patients with congenital nystagmus. Brain. 1999;122(Pt 7):1293–303.

    Article  PubMed  Google Scholar 

  21. Straumann D. Off-line computing of slow-phase eye velocity profiles evoked by velocity steps or caloric stimulation. Int J Biomed Comput. 1991;29:61–5.

    Article  CAS  PubMed  Google Scholar 

  22. Baier B, Vogt T, Rohde F, Cuvenhaus H, Conrad J, and Dieterich M. Deep brain stimulation of the nucleus ventralis intermedius: a thalamic site of graviceptive modulation. Brain Struct Funct. 2015.

  23. Mike A, Balas I, Varga D, Janszky J, Nagy F, Kovacs N. Subjective visual vertical may be altered by bilateral subthalamic deep brain stimulation. Mov Disord. 2009;24:1556–7.

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank Mahlon DeLong, MD and Andre Machado, MD, PhD for the insights and support. Aasef Shaikh was supported by Dystonia Coallition/Dystonia Medical Research Foundation Career Development award and Dystonia Medical Research Foundation clinical fellowship.

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Authors and Affiliations

  1. Department of Neurology, Case Western Reserve University, Cleveland, OH, USA

    Aasef G. Shaikh

  2. Neurology Service, Cleveland VA Medical Center, Cleveland, OH, USA

    Aasef G. Shaikh

  3. Daroff-DelOsso Ocular Motility Laboratory, Cleveland VA Medical Center, Cleveland, OH, USA

    Aasef G. Shaikh

  4. Department of Neurology, University Hospitals, Case Western Reserve University, 11100 Euclid Avenue, Cleveland, OH, 44110, USA

    Aasef G. Shaikh

  5. Department of Neurology, University Hospital Zurich, University of Zurich, Zurich, Switzerland

    Dominik Straumann & Antonella Palla

Authors
  1. Aasef G. Shaikh
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  2. Dominik Straumann
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  3. Antonella Palla
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Correspondence to Aasef G. Shaikh.

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Compliance with Ethical Standards

The experimental protocol was approved by an ethics committee of the Canton of Zurich and adhered to the Declaration of Helsinki for research involving human subjects.

Disclosure and Conflict of Interest

The authors have no conflict of interests of financial disclosures other than funding support mentioned in Acknowledgements.

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Shaikh, A.G., Straumann, D. & Palla, A. Motion Illusion—Evidence towards Human Vestibulo-Thalamic Projections. Cerebellum 16, 656–663 (2017). https://doi.org/10.1007/s12311-017-0844-y

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  • DOI: https://doi.org/10.1007/s12311-017-0844-y

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