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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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Proposed model structure according to the Raphan, Cohen, and Matsuo model with corresponding modifications for self-motion perception.Block diagram representation of the velocity storage model as previously developed for the rotational vestibulo-ocular reflex (solid lines) [10], [33] and recently modified [13] for rotational self-motion perception (dashed-dotted lines) under the assumption of a common central processing (see text for details). Insert A: Example of the output of the block accounting for the semicircular canal (SCC) dynamics. Insert B: Example of the output of the block representing the central velocity storage mechanism. Insert C: Output of the model (bold black line) generating a curve that best fits slow-phase eye velocity responses (gray traces) of the rotational vestibulo-ocular reflex. The thin and dashed black lines in insert C represent the two components (SCC and velocity storage mechanism) generating the overall data fit (bold line). g1−4: gains, i.e. strength or weight of individual pathway contributions.
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pone-0036763-g001: Proposed model structure according to the Raphan, Cohen, and Matsuo model with corresponding modifications for self-motion perception.Block diagram representation of the velocity storage model as previously developed for the rotational vestibulo-ocular reflex (solid lines) [10], [33] and recently modified [13] for rotational self-motion perception (dashed-dotted lines) under the assumption of a common central processing (see text for details). Insert A: Example of the output of the block accounting for the semicircular canal (SCC) dynamics. Insert B: Example of the output of the block representing the central velocity storage mechanism. Insert C: Output of the model (bold black line) generating a curve that best fits slow-phase eye velocity responses (gray traces) of the rotational vestibulo-ocular reflex. The thin and dashed black lines in insert C represent the two components (SCC and velocity storage mechanism) generating the overall data fit (bold line). g1−4: gains, i.e. strength or weight of individual pathway contributions.

Mentions: A model previously developed for monkeys representing the step responses of the rotational vestibulo-ocular reflex (rVOR) was fitted to our data [10], [33]. Figure 1 (solid lines) provides a graphical representation of this model together with an example of the slow-phase eye velocity responses of one cerebellar patient (indexed as 8 in Table 1) to one trial of earth-vertical yaw rotation (gray trace in insert C). The function that generates the curve that best fits slow-phase eye velocity (bold trace in insert C) can be divided into two components. The first, accounting for the semicircular canal activity, is a single exponential with a time constant τC and is shown in the figure by solid thin traces (see inserts A and C). The second component of the function represents the central processing called the velocity storage mechanism and is the difference of two exponentials with two different time constants, τC and τVSM. It is depicted as dashed traces (see inserts B and C).


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)

Proposed model structure according to the Raphan, Cohen, and Matsuo model with corresponding modifications for self-motion perception.Block diagram representation of the velocity storage model as previously developed for the rotational vestibulo-ocular reflex (solid lines) [10], [33] and recently modified [13] for rotational self-motion perception (dashed-dotted lines) under the assumption of a common central processing (see text for details). Insert A: Example of the output of the block accounting for the semicircular canal (SCC) dynamics. Insert B: Example of the output of the block representing the central velocity storage mechanism. Insert C: Output of the model (bold black line) generating a curve that best fits slow-phase eye velocity responses (gray traces) of the rotational vestibulo-ocular reflex. The thin and dashed black lines in insert C represent the two components (SCC and velocity storage mechanism) generating the overall data fit (bold line). g1−4: gains, i.e. strength or weight of individual pathway contributions.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3376140&req=5

pone-0036763-g001: Proposed model structure according to the Raphan, Cohen, and Matsuo model with corresponding modifications for self-motion perception.Block diagram representation of the velocity storage model as previously developed for the rotational vestibulo-ocular reflex (solid lines) [10], [33] and recently modified [13] for rotational self-motion perception (dashed-dotted lines) under the assumption of a common central processing (see text for details). Insert A: Example of the output of the block accounting for the semicircular canal (SCC) dynamics. Insert B: Example of the output of the block representing the central velocity storage mechanism. Insert C: Output of the model (bold black line) generating a curve that best fits slow-phase eye velocity responses (gray traces) of the rotational vestibulo-ocular reflex. The thin and dashed black lines in insert C represent the two components (SCC and velocity storage mechanism) generating the overall data fit (bold line). g1−4: gains, i.e. strength or weight of individual pathway contributions.
Mentions: A model previously developed for monkeys representing the step responses of the rotational vestibulo-ocular reflex (rVOR) was fitted to our data [10], [33]. Figure 1 (solid lines) provides a graphical representation of this model together with an example of the slow-phase eye velocity responses of one cerebellar patient (indexed as 8 in Table 1) to one trial of earth-vertical yaw rotation (gray trace in insert C). The function that generates the curve that best fits slow-phase eye velocity (bold trace in insert C) can be divided into two components. The first, accounting for the semicircular canal activity, is a single exponential with a time constant τC and is shown in the figure by solid thin traces (see inserts A and C). The second component of the function represents the central processing called the velocity storage mechanism and is the difference of two exponentials with two different time constants, τC and τVSM. It is depicted as dashed traces (see inserts B and C).

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