Is vestibular self-motion perception controlled by the velocity storage? Insights from patients with chronic degeneration of the vestibulo-cerebellum.

BACKGROUND: The rotational vestibulo-ocular reflex (rVOR) generates compensatory eye movements in response to rotational head accelerations. The velocity-storage mechanism (VSM), which is controlled by the vestibulo-cerebellar nodulus and uvula, determines the rVOR time constant. In healthy subjects...

Full description

Bibliographic Details
Main Authors: Giovanni Bertolini, Stefano Ramat, Christopher J Bockisch, Sarah Marti, Dominik Straumann, Antonella Palla
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3376140?pdf=render
id doaj-a26272cc50174aea8e2f2a2ab4d82575
record_format Article
spelling doaj-a26272cc50174aea8e2f2a2ab4d825752020-11-25T02:32:26ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0176e3676310.1371/journal.pone.0036763Is vestibular self-motion perception controlled by the velocity storage? Insights from patients with chronic degeneration of the vestibulo-cerebellum.Giovanni BertoliniStefano RamatChristopher J BockischSarah MartiDominik StraumannAntonella PallaBACKGROUND: The rotational vestibulo-ocular reflex (rVOR) generates compensatory eye movements in response to rotational head accelerations. The velocity-storage mechanism (VSM), which is controlled by the vestibulo-cerebellar nodulus and uvula, determines the rVOR time constant. In healthy subjects, it has been suggested that self-motion perception in response to earth-vertical axis rotations depends on the VSM in a similar way as reflexive eye movements. We aimed at further investigating this hypothesis and speculated that if the rVOR and rotational self-motion perception share a common VSM, alteration in the latter, such as those occurring after a loss of the regulatory control by vestibulo-cerebellar structures, would result in similar reflexive and perceptual response changes. We therefore set out to explore both responses in patients with vestibulo-cerebellar degeneration. METHODOLOGY/PRINCIPAL FINDINGS: Reflexive eye movements and perceived rotational velocity were simultaneously recorded in 14 patients with chronic vestibulo-cerebellar degeneration (28-81 yrs) and 12 age-matched healthy subjects (30-72 yrs) after the sudden deceleration (90°/s2) from constant-velocity (90°/s) rotations about the earth-vertical yaw and pitch axes. rVOR and perceived rotational velocity data were analyzed using a two-exponential model with a direct pathway, representing semicircular canal activity, and an indirect pathway, implementing the VSM. We found that VSM time constants of rVOR and perceived rotational velocity co-varied in cerebellar patients and in healthy controls (Pearson correlation coefficient for yaw 0.95; for pitch 0.93, p<0.01). When constraining model parameters to use the same VSM time constant for rVOR and perceived rotational velocity, moreover, no significant deterioration of the quality of fit was found for both populations (variance-accounted-for >0.8). CONCLUSIONS/SIGNIFICANCE: Our results confirm that self-motion perception in response to rotational velocity-steps may be controlled by the same velocity storage network that controls reflexive eye movements and that no additional, e.g. cortical, mechanisms are required to explain perceptual dynamics.http://europepmc.org/articles/PMC3376140?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Giovanni Bertolini
Stefano Ramat
Christopher J Bockisch
Sarah Marti
Dominik Straumann
Antonella Palla
spellingShingle Giovanni Bertolini
Stefano Ramat
Christopher J Bockisch
Sarah Marti
Dominik Straumann
Antonella Palla
Is vestibular self-motion perception controlled by the velocity storage? Insights from patients with chronic degeneration of the vestibulo-cerebellum.
PLoS ONE
author_facet Giovanni Bertolini
Stefano Ramat
Christopher J Bockisch
Sarah Marti
Dominik Straumann
Antonella Palla
author_sort Giovanni Bertolini
title Is vestibular self-motion perception controlled by the velocity storage? Insights from patients with chronic degeneration of the vestibulo-cerebellum.
title_short Is vestibular self-motion perception controlled by the velocity storage? Insights from patients with chronic degeneration of the vestibulo-cerebellum.
title_full Is vestibular self-motion perception controlled by the velocity storage? Insights from patients with chronic degeneration of the vestibulo-cerebellum.
title_fullStr Is vestibular self-motion perception controlled by the velocity storage? Insights from patients with chronic degeneration of the vestibulo-cerebellum.
title_full_unstemmed Is vestibular self-motion perception controlled by the velocity storage? Insights from patients with chronic degeneration of the vestibulo-cerebellum.
title_sort is vestibular self-motion perception controlled by the velocity storage? insights from patients with chronic degeneration of the vestibulo-cerebellum.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2012-01-01
description BACKGROUND: The rotational vestibulo-ocular reflex (rVOR) generates compensatory eye movements in response to rotational head accelerations. The velocity-storage mechanism (VSM), which is controlled by the vestibulo-cerebellar nodulus and uvula, determines the rVOR time constant. In healthy subjects, it has been suggested that self-motion perception in response to earth-vertical axis rotations depends on the VSM in a similar way as reflexive eye movements. We aimed at further investigating this hypothesis and speculated that if the rVOR and rotational self-motion perception share a common VSM, alteration in the latter, such as those occurring after a loss of the regulatory control by vestibulo-cerebellar structures, would result in similar reflexive and perceptual response changes. We therefore set out to explore both responses in patients with vestibulo-cerebellar degeneration. METHODOLOGY/PRINCIPAL FINDINGS: Reflexive eye movements and perceived rotational velocity were simultaneously recorded in 14 patients with chronic vestibulo-cerebellar degeneration (28-81 yrs) and 12 age-matched healthy subjects (30-72 yrs) after the sudden deceleration (90°/s2) from constant-velocity (90°/s) rotations about the earth-vertical yaw and pitch axes. rVOR and perceived rotational velocity data were analyzed using a two-exponential model with a direct pathway, representing semicircular canal activity, and an indirect pathway, implementing the VSM. We found that VSM time constants of rVOR and perceived rotational velocity co-varied in cerebellar patients and in healthy controls (Pearson correlation coefficient for yaw 0.95; for pitch 0.93, p<0.01). When constraining model parameters to use the same VSM time constant for rVOR and perceived rotational velocity, moreover, no significant deterioration of the quality of fit was found for both populations (variance-accounted-for >0.8). CONCLUSIONS/SIGNIFICANCE: Our results confirm that self-motion perception in response to rotational velocity-steps may be controlled by the same velocity storage network that controls reflexive eye movements and that no additional, e.g. cortical, mechanisms are required to explain perceptual dynamics.
url http://europepmc.org/articles/PMC3376140?pdf=render
work_keys_str_mv AT giovannibertolini isvestibularselfmotionperceptioncontrolledbythevelocitystorageinsightsfrompatientswithchronicdegenerationofthevestibulocerebellum
AT stefanoramat isvestibularselfmotionperceptioncontrolledbythevelocitystorageinsightsfrompatientswithchronicdegenerationofthevestibulocerebellum
AT christopherjbockisch isvestibularselfmotionperceptioncontrolledbythevelocitystorageinsightsfrompatientswithchronicdegenerationofthevestibulocerebellum
AT sarahmarti isvestibularselfmotionperceptioncontrolledbythevelocitystorageinsightsfrompatientswithchronicdegenerationofthevestibulocerebellum
AT dominikstraumann isvestibularselfmotionperceptioncontrolledbythevelocitystorageinsightsfrompatientswithchronicdegenerationofthevestibulocerebellum
AT antonellapalla isvestibularselfmotionperceptioncontrolledbythevelocitystorageinsightsfrompatientswithchronicdegenerationofthevestibulocerebellum
_version_ 1724819189768650752