Does Inferior-Olive Hypersynchrony Affect Vestibular Heading Perception?
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.
KeywordsMotion perception Inferior olive Cerebellum Multisensory integration
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.
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.
- 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.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
- 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
- 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