Beyond passive observation: feedback anticipation and observation activate the mirror system in virtual finger movement control via P300-BCI

Action observation (AO) is widely used as a post-stroke therapy to activate sensorimotor circuits through the mirror neuron system. However, passive observation is often considered to be less effective and less interactive than goal-directed movement observation, leading to the suggestion that obser...

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Published in	Frontiers in human neuroscience Vol. 17; p. 1180056
Main Authors	Syrov, Nikolay, Yakovlev, Lev, Miroshnikov, Andrei, Kaplan, Alexander
Format	Journal Article
Language	English
Published	Switzerland Frontiers Research Foundation 04.05.2023 Frontiers Media S.A
Subjects	Accuracy action observation (AO) Brain Brain research brain–computer interface (BCI) Computer applications EEG Electroencephalography error-related potentials (ErrPs) Feedback feedback anticipation Implants mirror neurons Neurology Neuroscience Rehabilitation sensorimotor cortex Sensorimotor system Stroke Synchronization brain–computer interface (BCI) action observation (AO) sensorimotor cortex beta synchronization mirror neurons error-related potentials (ErrPs) feedback anticipation
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Abstract	Action observation (AO) is widely used as a post-stroke therapy to activate sensorimotor circuits through the mirror neuron system. However, passive observation is often considered to be less effective and less interactive than goal-directed movement observation, leading to the suggestion that observation of goal-directed actions may have stronger therapeutic potential, as goal-directed AO has been shown to activate mechanisms for monitoring action errors. Some studies have also suggested the use of AO as a form of Brain–computer interface (BCI) feedback. In this study, we investigated the potential for observation of virtual hand movements within a P300-based BCI as a feedback system to activate the mirror neuron system. We also explored the role of feedback anticipation and estimation mechanisms during movement observation. Twenty healthy subjects participated in the study. We analyzed event-related desynchronization and synchronization (ERD/S) of sensorimotor EEG rhythms and Error-related potentials (ErrPs) during observation of virtual hand finger flexion presented as feedback in the P300-BCI loop and compared the dynamics of ERD/S and ErrPs during observation of correct feedback and errors. We also analyzed these EEG markers during passive AO under two conditions: when subjects anticipated the action demonstration and when the action was unexpected. A pre-action mu-ERD was found both before passive AO and during action anticipation within the BCI loop. Furthermore, a significant increase in beta-ERS was found during AO within incorrect BCI feedback trials. We suggest that the BCI feedback may exaggerate the passive-AO effect, as it engages feedback anticipation and estimation mechanisms as well as movement error monitoring simultaneously. The results of this study provide insights into the potential of P300-BCI with AO-feedback as a tool for neurorehabilitation.
AbstractList	Action observation (AO) is widely used as a post-stroke therapy to activate sensorimotor circuits through the mirror neuron system. However, passive observation is often considered to be less effective and less interactive than goal-directed movement observation, leading to the suggestion that observation of goal-directed actions may have stronger therapeutic potential, as goal-directed AO has been shown to activate mechanisms for monitoring action errors. Some studies have also suggested the use of AO as a form of Brain-computer interface (BCI) feedback. In this study, we investigated the potential for observation of virtual hand movements within a P300-based BCI as a feedback system to activate the mirror neuron system. We also explored the role of feedback anticipation and estimation mechanisms during movement observation. Twenty healthy subjects participated in the study. We analyzed event-related desynchronization and synchronization (ERD/S) of sensorimotor EEG rhythms and Error-related potentials (ErrPs) during observation of virtual hand finger flexion presented as feedback in the P300-BCI loop and compared the dynamics of ERD/S and ErrPs during observation of correct feedback and errors. We also analyzed these EEG markers during passive AO under two conditions: when subjects anticipated the action demonstration and when the action was unexpected. A pre-action mu-ERD was found both before passive AO and during action anticipation within the BCI loop. Furthermore, a significant increase in beta-ERS was found during AO within incorrect BCI feedback trials. We suggest that the BCI feedback may exaggerate the passive-AO effect, as it engages feedback anticipation and estimation mechanisms as well as movement error monitoring simultaneously. The results of this study provide insights into the potential of P300-BCI with AO-feedback as a tool for neurorehabilitation. Action observation (AO) is widely used as a post-stroke therapy to activate sensorimotor circuits through the mirror neuron system. However, passive observation is often considered to be less effective and less interactive than goal-directed movement observation, leading to the suggestion that observation of goal-directed actions may have stronger therapeutic potential, as goal-directed AO has been shown to activate mechanisms for monitoring action errors. Some studies have also suggested the use of AO as a form of Brain-computer interface (BCI) feedback. In this study, we investigated the potential for observation of virtual hand movements within a P300-based BCI as a feedback system to activate the mirror neuron system. We also explored the role of feedback anticipation and estimation mechanisms during movement observation. Twenty healthy subjects participated in the study. We analyzed event-related desynchronization and synchronization (ERD/S) of sensorimotor EEG rhythms and Error-related potentials (ErrPs) during observation of virtual hand finger flexion presented as feedback in the P300-BCI loop and compared the dynamics of ERD/S and ErrPs during observation of correct feedback and errors. We also analyzed these EEG markers during passive AO under two conditions: when subjects anticipated the action demonstration and when the action was unexpected. A pre-action mu-ERD was found both before passive AO and during action anticipation within the BCI loop. Furthermore, a significant increase in beta-ERS was found during AO within incorrect BCI feedback trials. We suggest that the BCI feedback may exaggerate the passive-AO effect, as it engages feedback anticipation and estimation mechanisms as well as movement error monitoring simultaneously. The results of this study provide insights into the potential of P300-BCI with AO-feedback as a tool for neurorehabilitation.Action observation (AO) is widely used as a post-stroke therapy to activate sensorimotor circuits through the mirror neuron system. However, passive observation is often considered to be less effective and less interactive than goal-directed movement observation, leading to the suggestion that observation of goal-directed actions may have stronger therapeutic potential, as goal-directed AO has been shown to activate mechanisms for monitoring action errors. Some studies have also suggested the use of AO as a form of Brain-computer interface (BCI) feedback. In this study, we investigated the potential for observation of virtual hand movements within a P300-based BCI as a feedback system to activate the mirror neuron system. We also explored the role of feedback anticipation and estimation mechanisms during movement observation. Twenty healthy subjects participated in the study. We analyzed event-related desynchronization and synchronization (ERD/S) of sensorimotor EEG rhythms and Error-related potentials (ErrPs) during observation of virtual hand finger flexion presented as feedback in the P300-BCI loop and compared the dynamics of ERD/S and ErrPs during observation of correct feedback and errors. We also analyzed these EEG markers during passive AO under two conditions: when subjects anticipated the action demonstration and when the action was unexpected. A pre-action mu-ERD was found both before passive AO and during action anticipation within the BCI loop. Furthermore, a significant increase in beta-ERS was found during AO within incorrect BCI feedback trials. We suggest that the BCI feedback may exaggerate the passive-AO effect, as it engages feedback anticipation and estimation mechanisms as well as movement error monitoring simultaneously. The results of this study provide insights into the potential of P300-BCI with AO-feedback as a tool for neurorehabilitation. Action observation (AO) is widely used as a post-stroke therapy to activate sensorimotor circuits through the mirror neuron system. However, passive observation is often considered to be less effective and less interactive than goal-directed movement observation, leading to the suggestion that observation of goal-directed actions may have stronger therapeutic potential, as goal-directed AO has been shown to activate mechanisms for monitoring action errors. Some studies have also suggested the use of AO as a form of BCI feedback. In this study, we investigated the potential for observation of virtual hand movements within a P300-based brain-computer interface as a feedback system to activate the mirror neuron system. We also explored the role of feedback anticipation and estimation mechanisms during movement observation. By analyzing event-related desynchronization and synchronization (ERD/S) of sensorimotor EEG rhythms and Error-related Potentials (ErrPs), we traced the cortical activity of 20 healthy subjects during observation of virtual hand finger flexion presented as feedback in the P300-BCI loop and compared the dynamics of ERD/S and ErrPs during observation of correct feedback and errors. We also analyzed these EEG markers during passive AO under two conditions: when subjects anticipated the action demonstration and when the action was unexpected. A pre-action mu-ERD was found both before passive AO and during action anticipation within the BCI loop. Furthermore, a significant increase in beta-ERS was found during AO within incorrect BCI feedback trials. We suggest that the BCI feedback may exaggerate the passive-AO effect, as it engages feedback anticipation and estimation mechanisms as well as movement error monitoring simultaneously. The results of this study provide insights into the potential of P300-BCI with AO-feedback as a tool for neurorehabilitation.
Author	Yakovlev, Lev Miroshnikov, Andrei Syrov, Nikolay Kaplan, Alexander
AuthorAffiliation	3 Department of Human and Animal Physiology, Faculty of Biology, Lomonosov Moscow State University , Moscow , Russia 1 V. Zelman Center for Neurobiology and Brain Rehabilitation, Skolkovo Institute of Science and Technology , Moscow , Russia 2 Baltic Center for Neurotechnology and Artificial Intelligence, Immanuel Kant Baltic Federal University , Kaliningrad , Russia
AuthorAffiliation_xml	– name: 3 Department of Human and Animal Physiology, Faculty of Biology, Lomonosov Moscow State University , Moscow , Russia – name: 2 Baltic Center for Neurotechnology and Artificial Intelligence, Immanuel Kant Baltic Federal University , Kaliningrad , Russia – name: 1 V. Zelman Center for Neurobiology and Brain Rehabilitation, Skolkovo Institute of Science and Technology , Moscow , Russia
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/37213933$$D View this record in MEDLINE/PubMed
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Copyright	Copyright © 2023 Syrov, Yakovlev, Miroshnikov and Kaplan. 2023. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Copyright © 2023 Syrov, Yakovlev, Miroshnikov and Kaplan. 2023 Syrov, Yakovlev, Miroshnikov and Kaplan
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Keywords	brain–computer interface (BCI) action observation (AO) sensorimotor cortex beta synchronization mirror neurons error-related potentials (ErrPs) feedback anticipation
Language	English
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Reviewed by: Xiaogang Chen, Chinese Academy of Medical Sciences and Peking Union Medical College, China; Erwei Yin, Tianjin Artificial Intelligence Innovation Center (TAIIC), China Edited by: Floriana Pichiorri, Santa Lucia Foundation (IRCCS), Italy
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Snippet	Action observation (AO) is widely used as a post-stroke therapy to activate sensorimotor circuits through the mirror neuron system. However, passive...
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SubjectTerms	Accuracy action observation (AO) Brain Brain research brain–computer interface (BCI) Computer applications EEG Electroencephalography error-related potentials (ErrPs) Feedback feedback anticipation Implants mirror neurons Neurology Neuroscience Rehabilitation sensorimotor cortex Sensorimotor system Stroke Synchronization
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Title	Beyond passive observation: feedback anticipation and observation activate the mirror system in virtual finger movement control via P300-BCI
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