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Pre‐movement event‐related potentials and multivariate pattern of EEG encode action outcome prediction

Self‐initiated movements are accompanied by an efference copy, a motor command sent from motor regions to the sensory cortices, containing a prediction of the movement's sensory outcome. Previous studies have proposed pre‐motor event‐related potentials (ERPs), including the readiness potential...

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Autores principales: Ody, Edward, Kircher, Tilo, Straube, Benjamin, He, Yifei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619393/
https://www.ncbi.nlm.nih.gov/pubmed/37792296
http://dx.doi.org/10.1002/hbm.26506
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author Ody, Edward
Kircher, Tilo
Straube, Benjamin
He, Yifei
author_facet Ody, Edward
Kircher, Tilo
Straube, Benjamin
He, Yifei
author_sort Ody, Edward
collection PubMed
description Self‐initiated movements are accompanied by an efference copy, a motor command sent from motor regions to the sensory cortices, containing a prediction of the movement's sensory outcome. Previous studies have proposed pre‐motor event‐related potentials (ERPs), including the readiness potential (RP) and its lateralized sub‐component (LRP), as potential neural markers of action feedback prediction. However, it is not known how specific these neural markers are for voluntary (active) movements as compared to involuntary (passive) movements, which produce much of the same sensory feedback (tactile, proprioceptive) but are not accompanied by an efference copy. The goal of the current study was to investigate how active and passive movements are distinguishable from premotor electroencephalography (EEG), and to examine if this change of neural activity differs when participants engage in tasks that differ in their expectation of sensory outcomes. Participants made active (self‐initiated) or passive (finger moved by device) finger movements that led to either visual or auditory stimuli (100 ms delay), or to no immediate contingency effects (control). We investigated the time window before the movement onset by measuring pre‐movement ERPs time‐locked to the button press. For RP, we observed an interaction between task and movement. This was driven by movement differences in the visual and auditory but not the control conditions. LRP conversely only showed a main effect of movement. We then used multivariate pattern analysis to decode movements (active vs. passive). The results revealed ramping decoding for all tasks from around −800 ms onwards up to an accuracy of approximately 85% at the movement. Importantly, similar to RP, we observed lower decoding accuracies for the control condition than the visual and auditory conditions, but only shortly (from −200 ms) before the button press. We also decoded visual vs. auditory conditions. Here, task is decodable for both active and passive conditions, but the active condition showed increased decoding shortly before the button press. Taken together, our results provide robust evidence that pre‐movement EEG activity may represent action‐feedback prediction in which information about the subsequent sensory outcome is encoded.
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spelling pubmed-106193932023-11-02 Pre‐movement event‐related potentials and multivariate pattern of EEG encode action outcome prediction Ody, Edward Kircher, Tilo Straube, Benjamin He, Yifei Hum Brain Mapp Research Articles Self‐initiated movements are accompanied by an efference copy, a motor command sent from motor regions to the sensory cortices, containing a prediction of the movement's sensory outcome. Previous studies have proposed pre‐motor event‐related potentials (ERPs), including the readiness potential (RP) and its lateralized sub‐component (LRP), as potential neural markers of action feedback prediction. However, it is not known how specific these neural markers are for voluntary (active) movements as compared to involuntary (passive) movements, which produce much of the same sensory feedback (tactile, proprioceptive) but are not accompanied by an efference copy. The goal of the current study was to investigate how active and passive movements are distinguishable from premotor electroencephalography (EEG), and to examine if this change of neural activity differs when participants engage in tasks that differ in their expectation of sensory outcomes. Participants made active (self‐initiated) or passive (finger moved by device) finger movements that led to either visual or auditory stimuli (100 ms delay), or to no immediate contingency effects (control). We investigated the time window before the movement onset by measuring pre‐movement ERPs time‐locked to the button press. For RP, we observed an interaction between task and movement. This was driven by movement differences in the visual and auditory but not the control conditions. LRP conversely only showed a main effect of movement. We then used multivariate pattern analysis to decode movements (active vs. passive). The results revealed ramping decoding for all tasks from around −800 ms onwards up to an accuracy of approximately 85% at the movement. Importantly, similar to RP, we observed lower decoding accuracies for the control condition than the visual and auditory conditions, but only shortly (from −200 ms) before the button press. We also decoded visual vs. auditory conditions. Here, task is decodable for both active and passive conditions, but the active condition showed increased decoding shortly before the button press. Taken together, our results provide robust evidence that pre‐movement EEG activity may represent action‐feedback prediction in which information about the subsequent sensory outcome is encoded. John Wiley & Sons, Inc. 2023-10-04 /pmc/articles/PMC10619393/ /pubmed/37792296 http://dx.doi.org/10.1002/hbm.26506 Text en © 2023 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Research Articles
Ody, Edward
Kircher, Tilo
Straube, Benjamin
He, Yifei
Pre‐movement event‐related potentials and multivariate pattern of EEG encode action outcome prediction
title Pre‐movement event‐related potentials and multivariate pattern of EEG encode action outcome prediction
title_full Pre‐movement event‐related potentials and multivariate pattern of EEG encode action outcome prediction
title_fullStr Pre‐movement event‐related potentials and multivariate pattern of EEG encode action outcome prediction
title_full_unstemmed Pre‐movement event‐related potentials and multivariate pattern of EEG encode action outcome prediction
title_short Pre‐movement event‐related potentials and multivariate pattern of EEG encode action outcome prediction
title_sort pre‐movement event‐related potentials and multivariate pattern of eeg encode action outcome prediction
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619393/
https://www.ncbi.nlm.nih.gov/pubmed/37792296
http://dx.doi.org/10.1002/hbm.26506
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