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Multiple timescales in the adaptation of the rotational VOR


Colagiorgio, P; Bertolini, G; Bockisch, C J; Straumann, D; Ramat, S (2015). Multiple timescales in the adaptation of the rotational VOR. Journal of Neurophysiology, 113(9):3130-3142.

Abstract

Goal-directed movements, such as pointing and saccades, have been shown to share similar neural architectures, in spite of the different neuromuscular systems producing them. Such structure involve an inverse model of the actuator being controlled, which produces the commands innervating the muscles, and a forward model of the actuator, which predicts the sensory consequences of such commands and allows online movement corrections. Recent studies have shown that goal-directed movements also share similar motor-learning and motor-memory mechanisms, which are based on multiple timescales. The hypothesis that also the rotational vestibulo-ocular reflex (rVOR) may be based on a similar architecture has been presented recently. We hypothesize that multiple timescales are the brain's solution to the plasticity-stability dilemma, allowing adaptation to temporary and sudden changes while keeping stable motor-control abilities. If that were the case, then we would also expect the adaptation of reflex movements to follow the same principles. Thus we studied rVOR gain adaptation in eight healthy human subjects using a custom paradigm aimed at investigating the existence of spontaneous recovery, which we considered as the hallmark of multiple timescales in motor learning. Our experimental results show that spontaneous recovery occurred in six of eight subjects. Thus we developed a mathematical model of rVOR adaptation based on two hidden-states processes, which adapts the cerebellar-forward model of the ocular motor plant, and show that it accurately simulates our experimental data on rVOR gain adaptation, whereas a single timescale learning process fails to do so.

Abstract

Goal-directed movements, such as pointing and saccades, have been shown to share similar neural architectures, in spite of the different neuromuscular systems producing them. Such structure involve an inverse model of the actuator being controlled, which produces the commands innervating the muscles, and a forward model of the actuator, which predicts the sensory consequences of such commands and allows online movement corrections. Recent studies have shown that goal-directed movements also share similar motor-learning and motor-memory mechanisms, which are based on multiple timescales. The hypothesis that also the rotational vestibulo-ocular reflex (rVOR) may be based on a similar architecture has been presented recently. We hypothesize that multiple timescales are the brain's solution to the plasticity-stability dilemma, allowing adaptation to temporary and sudden changes while keeping stable motor-control abilities. If that were the case, then we would also expect the adaptation of reflex movements to follow the same principles. Thus we studied rVOR gain adaptation in eight healthy human subjects using a custom paradigm aimed at investigating the existence of spontaneous recovery, which we considered as the hallmark of multiple timescales in motor learning. Our experimental results show that spontaneous recovery occurred in six of eight subjects. Thus we developed a mathematical model of rVOR adaptation based on two hidden-states processes, which adapts the cerebellar-forward model of the ocular motor plant, and show that it accurately simulates our experimental data on rVOR gain adaptation, whereas a single timescale learning process fails to do so.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:04 Faculty of Medicine > University Hospital Zurich > Ophthalmology Clinic
04 Faculty of Medicine > University Hospital Zurich > Clinic for Neurology
04 Faculty of Medicine > University Hospital Zurich > Clinic for Otorhinolaryngology
04 Faculty of Medicine > Neuroscience Center Zurich
04 Faculty of Medicine > Center for Integrative Human Physiology
Dewey Decimal Classification:610 Medicine & health
Language:English
Date:1 May 2015
Deposited On:11 Dec 2015 07:27
Last Modified:05 Apr 2016 19:35
Publisher:American Physiological Society
ISSN:0022-3077
Additional Information:All journals are free accessible after 12 months via HighWire Press
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1152/jn.00688.2014
PubMed ID:25744882

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