Cargando…

The effect of self‐generated versus externally generated actions on timing, duration, and amplitude of blood oxygen level dependent response for visual feedback processing

It has been widely assumed that internal forward models use efference copies to create predictions about the sensory consequences of our own actions. While these predictions have frequently been associated with a reduced blood oxygen level dependent (BOLD) response in sensory cortices, the timing an...

Descripción completa

Detalles Bibliográficos
Autores principales: Kavroulakis, Eleftherios, van Kemenade, Bianca M., Arikan, Belkis Ezgi, Kircher, Tilo, Straube, Benjamin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9582366/
https://www.ncbi.nlm.nih.gov/pubmed/36056611
http://dx.doi.org/10.1002/hbm.26053
_version_ 1784812818897305600
author Kavroulakis, Eleftherios
van Kemenade, Bianca M.
Arikan, Belkis Ezgi
Kircher, Tilo
Straube, Benjamin
author_facet Kavroulakis, Eleftherios
van Kemenade, Bianca M.
Arikan, Belkis Ezgi
Kircher, Tilo
Straube, Benjamin
author_sort Kavroulakis, Eleftherios
collection PubMed
description It has been widely assumed that internal forward models use efference copies to create predictions about the sensory consequences of our own actions. While these predictions have frequently been associated with a reduced blood oxygen level dependent (BOLD) response in sensory cortices, the timing and duration of the hemodynamic response for the processing of video feedback of self‐generated (active) versus externally generated (passive) movements is poorly understood. In the present study, we tested the hypothesis that predictive mechanisms for self‐generated actions lead to early and shorter neural processing compared with externally generated movements. We investigated active and passive movements using a custom‐made fMRI‐compatible movement device. Visual video feedback of the active and passive movements was presented in real time or with variable delays. Participants had to judge whether the feedback was delayed. Timing and duration of BOLD impulse response was calculated using a first (temporal derivative [TD]) and second‐order (dispersion derivative [DD]) Taylor approximation. Our reanalysis confirmed our previous finding of reduced BOLD response for active compared to passive movements. Moreover, we found positive effects of the TD and DD in the supplementary motor area, cerebellum, visual cortices, and subcortical structures, indicating earlier and shorter hemodynamic responses for active compared to passive movements. Furthermore, earlier activation in the putamen for active compared to passive conditions was associated with reduced delay detection performance. These findings indicate that efference copy‐based predictive mechanisms enable earlier processing of action feedback, which might have reduced the ability to detect short delays between action and feedback.
format Online
Article
Text
id pubmed-9582366
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher John Wiley & Sons, Inc.
record_format MEDLINE/PubMed
spelling pubmed-95823662022-10-21 The effect of self‐generated versus externally generated actions on timing, duration, and amplitude of blood oxygen level dependent response for visual feedback processing Kavroulakis, Eleftherios van Kemenade, Bianca M. Arikan, Belkis Ezgi Kircher, Tilo Straube, Benjamin Hum Brain Mapp Research Articles It has been widely assumed that internal forward models use efference copies to create predictions about the sensory consequences of our own actions. While these predictions have frequently been associated with a reduced blood oxygen level dependent (BOLD) response in sensory cortices, the timing and duration of the hemodynamic response for the processing of video feedback of self‐generated (active) versus externally generated (passive) movements is poorly understood. In the present study, we tested the hypothesis that predictive mechanisms for self‐generated actions lead to early and shorter neural processing compared with externally generated movements. We investigated active and passive movements using a custom‐made fMRI‐compatible movement device. Visual video feedback of the active and passive movements was presented in real time or with variable delays. Participants had to judge whether the feedback was delayed. Timing and duration of BOLD impulse response was calculated using a first (temporal derivative [TD]) and second‐order (dispersion derivative [DD]) Taylor approximation. Our reanalysis confirmed our previous finding of reduced BOLD response for active compared to passive movements. Moreover, we found positive effects of the TD and DD in the supplementary motor area, cerebellum, visual cortices, and subcortical structures, indicating earlier and shorter hemodynamic responses for active compared to passive movements. Furthermore, earlier activation in the putamen for active compared to passive conditions was associated with reduced delay detection performance. These findings indicate that efference copy‐based predictive mechanisms enable earlier processing of action feedback, which might have reduced the ability to detect short delays between action and feedback. John Wiley & Sons, Inc. 2022-09-02 /pmc/articles/PMC9582366/ /pubmed/36056611 http://dx.doi.org/10.1002/hbm.26053 Text en © 2022 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Research Articles
Kavroulakis, Eleftherios
van Kemenade, Bianca M.
Arikan, Belkis Ezgi
Kircher, Tilo
Straube, Benjamin
The effect of self‐generated versus externally generated actions on timing, duration, and amplitude of blood oxygen level dependent response for visual feedback processing
title The effect of self‐generated versus externally generated actions on timing, duration, and amplitude of blood oxygen level dependent response for visual feedback processing
title_full The effect of self‐generated versus externally generated actions on timing, duration, and amplitude of blood oxygen level dependent response for visual feedback processing
title_fullStr The effect of self‐generated versus externally generated actions on timing, duration, and amplitude of blood oxygen level dependent response for visual feedback processing
title_full_unstemmed The effect of self‐generated versus externally generated actions on timing, duration, and amplitude of blood oxygen level dependent response for visual feedback processing
title_short The effect of self‐generated versus externally generated actions on timing, duration, and amplitude of blood oxygen level dependent response for visual feedback processing
title_sort effect of self‐generated versus externally generated actions on timing, duration, and amplitude of blood oxygen level dependent response for visual feedback processing
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9582366/
https://www.ncbi.nlm.nih.gov/pubmed/36056611
http://dx.doi.org/10.1002/hbm.26053
work_keys_str_mv AT kavroulakiseleftherios theeffectofselfgeneratedversusexternallygeneratedactionsontimingdurationandamplitudeofbloodoxygenleveldependentresponseforvisualfeedbackprocessing
AT vankemenadebiancam theeffectofselfgeneratedversusexternallygeneratedactionsontimingdurationandamplitudeofbloodoxygenleveldependentresponseforvisualfeedbackprocessing
AT arikanbelkisezgi theeffectofselfgeneratedversusexternallygeneratedactionsontimingdurationandamplitudeofbloodoxygenleveldependentresponseforvisualfeedbackprocessing
AT kirchertilo theeffectofselfgeneratedversusexternallygeneratedactionsontimingdurationandamplitudeofbloodoxygenleveldependentresponseforvisualfeedbackprocessing
AT straubebenjamin theeffectofselfgeneratedversusexternallygeneratedactionsontimingdurationandamplitudeofbloodoxygenleveldependentresponseforvisualfeedbackprocessing
AT kavroulakiseleftherios effectofselfgeneratedversusexternallygeneratedactionsontimingdurationandamplitudeofbloodoxygenleveldependentresponseforvisualfeedbackprocessing
AT vankemenadebiancam effectofselfgeneratedversusexternallygeneratedactionsontimingdurationandamplitudeofbloodoxygenleveldependentresponseforvisualfeedbackprocessing
AT arikanbelkisezgi effectofselfgeneratedversusexternallygeneratedactionsontimingdurationandamplitudeofbloodoxygenleveldependentresponseforvisualfeedbackprocessing
AT kirchertilo effectofselfgeneratedversusexternallygeneratedactionsontimingdurationandamplitudeofbloodoxygenleveldependentresponseforvisualfeedbackprocessing
AT straubebenjamin effectofselfgeneratedversusexternallygeneratedactionsontimingdurationandamplitudeofbloodoxygenleveldependentresponseforvisualfeedbackprocessing