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Task-evoked pupillary responses track precision-weighted prediction errors and learning rate during interceptive visuomotor actions

In this study, we examined the relationship between physiological encoding of surprise and the learning of anticipatory eye movements. Active inference portrays perception and action as interconnected inference processes, driven by the imperative to minimise the surprise of sensory observations. To...

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Autores principales: Harris, D. J., Arthur, T., Vine, S. J., Liu, J., Abd Rahman, H. R., Han, F., Wilson, M. R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9772236/
https://www.ncbi.nlm.nih.gov/pubmed/36543845
http://dx.doi.org/10.1038/s41598-022-26544-w
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author Harris, D. J.
Arthur, T.
Vine, S. J.
Liu, J.
Abd Rahman, H. R.
Han, F.
Wilson, M. R.
author_facet Harris, D. J.
Arthur, T.
Vine, S. J.
Liu, J.
Abd Rahman, H. R.
Han, F.
Wilson, M. R.
author_sort Harris, D. J.
collection PubMed
description In this study, we examined the relationship between physiological encoding of surprise and the learning of anticipatory eye movements. Active inference portrays perception and action as interconnected inference processes, driven by the imperative to minimise the surprise of sensory observations. To examine this characterisation of oculomotor learning during a hand–eye coordination task, we tested whether anticipatory eye movements were updated in accordance with Bayesian principles and whether trial-by-trial learning rates tracked pupil dilation as a marker of ‘surprise’. Forty-four participants completed an interception task in immersive virtual reality that required them to hit bouncing balls that had either expected or unexpected bounce profiles. We recorded anticipatory eye movements known to index participants’ beliefs about likely ball bounce trajectories. By fitting a hierarchical Bayesian inference model to the trial-wise trajectories of these predictive eye movements, we were able to estimate each individual’s expectations about bounce trajectories, rates of belief updating, and precision-weighted prediction errors. We found that the task-evoked pupil response tracked prediction errors and learning rates but not beliefs about ball bounciness or environmental volatility. These findings are partially consistent with active inference accounts and shed light on how encoding of surprise may shape the control of action.
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spelling pubmed-97722362022-12-23 Task-evoked pupillary responses track precision-weighted prediction errors and learning rate during interceptive visuomotor actions Harris, D. J. Arthur, T. Vine, S. J. Liu, J. Abd Rahman, H. R. Han, F. Wilson, M. R. Sci Rep Article In this study, we examined the relationship between physiological encoding of surprise and the learning of anticipatory eye movements. Active inference portrays perception and action as interconnected inference processes, driven by the imperative to minimise the surprise of sensory observations. To examine this characterisation of oculomotor learning during a hand–eye coordination task, we tested whether anticipatory eye movements were updated in accordance with Bayesian principles and whether trial-by-trial learning rates tracked pupil dilation as a marker of ‘surprise’. Forty-four participants completed an interception task in immersive virtual reality that required them to hit bouncing balls that had either expected or unexpected bounce profiles. We recorded anticipatory eye movements known to index participants’ beliefs about likely ball bounce trajectories. By fitting a hierarchical Bayesian inference model to the trial-wise trajectories of these predictive eye movements, we were able to estimate each individual’s expectations about bounce trajectories, rates of belief updating, and precision-weighted prediction errors. We found that the task-evoked pupil response tracked prediction errors and learning rates but not beliefs about ball bounciness or environmental volatility. These findings are partially consistent with active inference accounts and shed light on how encoding of surprise may shape the control of action. Nature Publishing Group UK 2022-12-21 /pmc/articles/PMC9772236/ /pubmed/36543845 http://dx.doi.org/10.1038/s41598-022-26544-w Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Harris, D. J.
Arthur, T.
Vine, S. J.
Liu, J.
Abd Rahman, H. R.
Han, F.
Wilson, M. R.
Task-evoked pupillary responses track precision-weighted prediction errors and learning rate during interceptive visuomotor actions
title Task-evoked pupillary responses track precision-weighted prediction errors and learning rate during interceptive visuomotor actions
title_full Task-evoked pupillary responses track precision-weighted prediction errors and learning rate during interceptive visuomotor actions
title_fullStr Task-evoked pupillary responses track precision-weighted prediction errors and learning rate during interceptive visuomotor actions
title_full_unstemmed Task-evoked pupillary responses track precision-weighted prediction errors and learning rate during interceptive visuomotor actions
title_short Task-evoked pupillary responses track precision-weighted prediction errors and learning rate during interceptive visuomotor actions
title_sort task-evoked pupillary responses track precision-weighted prediction errors and learning rate during interceptive visuomotor actions
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9772236/
https://www.ncbi.nlm.nih.gov/pubmed/36543845
http://dx.doi.org/10.1038/s41598-022-26544-w
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