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Sensory Feedback Interferes with Mu Rhythm Based Detection of Motor Commands from Electroencephalographic Signals

Background: Electroencephalogram (EEG)-based brain-computer interfaces (BCI) represent a promising component of restorative motor therapies in individuals with partial paralysis. However, in those patients, sensory functions such as proprioception are at least partly preserved. The aim of this study...

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Autores principales: Hommelsen, Maximilian, Schneiders, Matthias, Schuld, Christian, Keyl, Philipp, Rupp, Rüdiger
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5672058/
https://www.ncbi.nlm.nih.gov/pubmed/29163103
http://dx.doi.org/10.3389/fnhum.2017.00523
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author Hommelsen, Maximilian
Schneiders, Matthias
Schuld, Christian
Keyl, Philipp
Rupp, Rüdiger
author_facet Hommelsen, Maximilian
Schneiders, Matthias
Schuld, Christian
Keyl, Philipp
Rupp, Rüdiger
author_sort Hommelsen, Maximilian
collection PubMed
description Background: Electroencephalogram (EEG)-based brain-computer interfaces (BCI) represent a promising component of restorative motor therapies in individuals with partial paralysis. However, in those patients, sensory functions such as proprioception are at least partly preserved. The aim of this study was to investigate whether afferent feedback interferes with the BCI-based detection of efferent motor commands during execution of movements. Methods: Brain activity of 13 able-bodied subjects (age: 29.1 ± 4.8 years; 11 males) was compared between a motor task (MT) consisting of an isometric, isotonic grip and a somatosensory electrical stimulation (SS) of the fingertips. Modulation of the mu rhythm (8–13 Hz) was investigated to identify changes specifically related to the generation of efferent commands. A linear discriminant analysis (LDA) was used to investigate the activation pattern on a single-trial basis. Classifiers were trained with MT vs. REST (periods without MT/SS) and tested with SS and vice versa to quantify the impact of afferent feedback on the classification results. Results: Few differences in the spatial pattern between MT and SS were found in the modulation of the mu rhythm. All were characterized by event-related desynchronization (ERD) peaks at electrodes C3, C4, and CP3. Execution of the MT was associated with a significantly stronger ERD in the majority of sensorimotor electrodes [C3 (p < 0.01); CP3 (p < 0.05); C4 (p < 0.01)]. Classification accuracy of MT vs. REST was significantly higher than SS vs. REST (77% and 63%; p < 10(-8)). Classifiers trained on MT vs. REST were able to classify SS trials significantly above chance even though no motor commands were present during SS. Classifiers trained on SS performed better in classifying MT instead of SS. Conclusion: Our results challenge the notion that the modulation of the mu rhythm is a robust phenomenon for detecting efferent commands when afferent feedback is present. Instead, they indicate that the mu ERD caused by the processing of afferent feedback generates ERD patterns in the sensorimotor cortex that are masking the ERD patterns caused by the generation of efferent commands. Thus, processing of afferent feedback represents a considerable source of false positives when the mu rhythm is used for the detection of efferent commands.
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spelling pubmed-56720582017-11-21 Sensory Feedback Interferes with Mu Rhythm Based Detection of Motor Commands from Electroencephalographic Signals Hommelsen, Maximilian Schneiders, Matthias Schuld, Christian Keyl, Philipp Rupp, Rüdiger Front Hum Neurosci Neuroscience Background: Electroencephalogram (EEG)-based brain-computer interfaces (BCI) represent a promising component of restorative motor therapies in individuals with partial paralysis. However, in those patients, sensory functions such as proprioception are at least partly preserved. The aim of this study was to investigate whether afferent feedback interferes with the BCI-based detection of efferent motor commands during execution of movements. Methods: Brain activity of 13 able-bodied subjects (age: 29.1 ± 4.8 years; 11 males) was compared between a motor task (MT) consisting of an isometric, isotonic grip and a somatosensory electrical stimulation (SS) of the fingertips. Modulation of the mu rhythm (8–13 Hz) was investigated to identify changes specifically related to the generation of efferent commands. A linear discriminant analysis (LDA) was used to investigate the activation pattern on a single-trial basis. Classifiers were trained with MT vs. REST (periods without MT/SS) and tested with SS and vice versa to quantify the impact of afferent feedback on the classification results. Results: Few differences in the spatial pattern between MT and SS were found in the modulation of the mu rhythm. All were characterized by event-related desynchronization (ERD) peaks at electrodes C3, C4, and CP3. Execution of the MT was associated with a significantly stronger ERD in the majority of sensorimotor electrodes [C3 (p < 0.01); CP3 (p < 0.05); C4 (p < 0.01)]. Classification accuracy of MT vs. REST was significantly higher than SS vs. REST (77% and 63%; p < 10(-8)). Classifiers trained on MT vs. REST were able to classify SS trials significantly above chance even though no motor commands were present during SS. Classifiers trained on SS performed better in classifying MT instead of SS. Conclusion: Our results challenge the notion that the modulation of the mu rhythm is a robust phenomenon for detecting efferent commands when afferent feedback is present. Instead, they indicate that the mu ERD caused by the processing of afferent feedback generates ERD patterns in the sensorimotor cortex that are masking the ERD patterns caused by the generation of efferent commands. Thus, processing of afferent feedback represents a considerable source of false positives when the mu rhythm is used for the detection of efferent commands. Frontiers Media S.A. 2017-11-01 /pmc/articles/PMC5672058/ /pubmed/29163103 http://dx.doi.org/10.3389/fnhum.2017.00523 Text en Copyright © 2017 Hommelsen, Schneiders, Schuld, Keyl and Rupp. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Hommelsen, Maximilian
Schneiders, Matthias
Schuld, Christian
Keyl, Philipp
Rupp, Rüdiger
Sensory Feedback Interferes with Mu Rhythm Based Detection of Motor Commands from Electroencephalographic Signals
title Sensory Feedback Interferes with Mu Rhythm Based Detection of Motor Commands from Electroencephalographic Signals
title_full Sensory Feedback Interferes with Mu Rhythm Based Detection of Motor Commands from Electroencephalographic Signals
title_fullStr Sensory Feedback Interferes with Mu Rhythm Based Detection of Motor Commands from Electroencephalographic Signals
title_full_unstemmed Sensory Feedback Interferes with Mu Rhythm Based Detection of Motor Commands from Electroencephalographic Signals
title_short Sensory Feedback Interferes with Mu Rhythm Based Detection of Motor Commands from Electroencephalographic Signals
title_sort sensory feedback interferes with mu rhythm based detection of motor commands from electroencephalographic signals
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5672058/
https://www.ncbi.nlm.nih.gov/pubmed/29163103
http://dx.doi.org/10.3389/fnhum.2017.00523
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