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

Bertolini G, Ramat S, Bockisch CJ, Marti S, Straumann D, Palla A - PLoS ONE (2012)

Bottom Line: 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).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.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, Zurich University Hospital, Zurich, Switzerland. bertoweb@gmail.com

ABSTRACT

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.

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Related in: MedlinePlus

Velocity storage time constants of reflexive eye and perceptual responses.Comparison of the time constants (mean ± SD) describing the velocity storage activity (τVSM) between slow-phase eye velocity (gray bars) and perceived rotational velocity (white bars) obtained by the model when letting τVSM free to change. Each block of two bars represents the results in one subject. Two patients were rotated about the earth-vertical yaw axis only, because they reported motion sickness during earth-vertical pitch rotations.
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pone-0036763-g003: Velocity storage time constants of reflexive eye and perceptual responses.Comparison of the time constants (mean ± SD) describing the velocity storage activity (τVSM) between slow-phase eye velocity (gray bars) and perceived rotational velocity (white bars) obtained by the model when letting τVSM free to change. Each block of two bars represents the results in one subject. Two patients were rotated about the earth-vertical yaw axis only, because they reported motion sickness during earth-vertical pitch rotations.

Mentions: τVSM of slow-phase eye velocity and perceived rotational velocity during trials of earth-vertical yaw and during trials of earth-vertical pitch rotations covaried in all cerebellar patients (Pearson correlation coefficient between rVOR τVSM and perception τVSM: 0.95 for yaw and 0.93 for pitch, p<0.001), indicating a possible link between the central time constant τVSM of slow-phase eye velocity and perceived rotational velocity. Figure 3 shows τVSM of slow-phase eye velocity and perceived rotational velocity (mean ± SD of all yaw and pitch traces) in individual patients.


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

Bertolini G, Ramat S, Bockisch CJ, Marti S, Straumann D, Palla A - PLoS ONE (2012)

Velocity storage time constants of reflexive eye and perceptual responses.Comparison of the time constants (mean ± SD) describing the velocity storage activity (τVSM) between slow-phase eye velocity (gray bars) and perceived rotational velocity (white bars) obtained by the model when letting τVSM free to change. Each block of two bars represents the results in one subject. Two patients were rotated about the earth-vertical yaw axis only, because they reported motion sickness during earth-vertical pitch rotations.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3376140&req=5

pone-0036763-g003: Velocity storage time constants of reflexive eye and perceptual responses.Comparison of the time constants (mean ± SD) describing the velocity storage activity (τVSM) between slow-phase eye velocity (gray bars) and perceived rotational velocity (white bars) obtained by the model when letting τVSM free to change. Each block of two bars represents the results in one subject. Two patients were rotated about the earth-vertical yaw axis only, because they reported motion sickness during earth-vertical pitch rotations.
Mentions: τVSM of slow-phase eye velocity and perceived rotational velocity during trials of earth-vertical yaw and during trials of earth-vertical pitch rotations covaried in all cerebellar patients (Pearson correlation coefficient between rVOR τVSM and perception τVSM: 0.95 for yaw and 0.93 for pitch, p<0.001), indicating a possible link between the central time constant τVSM of slow-phase eye velocity and perceived rotational velocity. Figure 3 shows τVSM of slow-phase eye velocity and perceived rotational velocity (mean ± SD of all yaw and pitch traces) in individual patients.

Bottom Line: 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).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.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, Zurich University Hospital, Zurich, Switzerland. bertoweb@gmail.com

ABSTRACT

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.

Show MeSH
Related in: MedlinePlus