Proprioceptive Feedback Facilitates Motor Imagery-Related Operant Learning of Sensorimotor β-Band Modulation

Sam Darvishi,Alireza Gharabaghi,Michael C Ridding,Mathias Baumert,Chadwick B Boulay,Derek Abbott

doi:10.3389/fnins.2017.00060

Sam Darvishi, Alireza Gharabaghi + Show 4 more

Open Access

https://doi.org/10.3389/fnins.2017.00060

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Abstract

Motor imagery (MI) activates the sensorimotor system independent of actual movements and might be facilitated by neurofeedback. Knowledge on the interaction between feedback modality and the involved frequency bands during MI-related brain self-regulation is still scarce. Previous studies compared the cortical activity during the MI task with concurrent feedback (MI with feedback condition) to cortical activity during the relaxation task where no feedback was provided (relaxation without feedback condition). The observed differences might, therefore, be related to either the task or the feedback. A proper comparison would necessitate studying a relaxation condition with feedback and a MI task condition without feedback as well. Right-handed healthy subjects performed two tasks, i.e., MI and relaxation, in alternating order. Each of the tasks (MI vs. relaxation) was studied with and without feedback. The respective event-driven oscillatory activity, i.e., sensorimotor desynchronization (during MI) or synchronization (during relaxation), was rewarded with contingent feedback. Importantly, feedback onset was delayed to study the task-related cortical activity in the absence of feedback provision during the delay period. The reward modality was alternated every 15 trials between proprioceptive and visual feedback. Proprioceptive input was superior to visual input to increase the range of task-related spectral perturbations in the α- and β-band, and was necessary to consistently achieve MI-related sensorimotor desynchronization (ERD) significantly below baseline. These effects occurred in task periods without feedback as well. The increased accuracy and duration of learned brain self-regulation achieved in the proprioceptive condition was specific to the β-band. MI-related operant learning of brain self-regulation is facilitated by proprioceptive feedback and mediated in the sensorimotor β-band.

Highlights

When motor learning via physical practice (Doyon and Benali, 2005; Halsband and Lange, 2006; Malouin et al, 2013) is compromised due to motor deficits following stroke, motor imagery (MI) may provide an alternative training modality (Halsband and Lange, 2006; Boe et al, 2014)
A detailed exploration would necessitate a refined study design for disentangling the contribution of the task condition and the feedback modality, separately: Previous studies compared the cortical activity during the Motor imagery (MI) task with concurrent feedback (MI with feedback condition) to cortical activity during the relaxation task where no feedback was provided
We employed the following indices to compare the effect of visual and proprioceptive feedback on MI performance with and without feedback: (i) the spectral power in α and β-bands during MI/relaxation tasks; (ii) accuracy, i.e., the percentage of trials in which the feedback conformed to the MI task, i.e., equivalent to the classical target hit rate in the cursor position update paradigm, (iii) event-related desynchronization (ERD) duration in imagery trials, i.e., the average percentage of times in each trial that the classifier output conformed to the MI task and moved either the orthosis or the cursor in the expected direction

Summary

INTRODUCTION

When motor learning via physical practice (Doyon and Benali, 2005; Halsband and Lange, 2006; Malouin et al, 2013) is compromised due to motor deficits following stroke, motor imagery (MI) may provide an alternative training modality (Halsband and Lange, 2006; Boe et al, 2014). MI activates the sensorimotor system independent of actual movements (Gao et al, 2011; Szameitat et al, 2012) and may be facilitated by neurofeedback contingent to the event related changes in the oscillatory activities i.e., ERD/ERS (Bauer and Gharabaghi, 2015a; Pichiorri et al, 2015; Vukelic and Gharabaghi, 2015a) Such a feedback may be provided via visual or proprioceptive input (Bai et al, 2014; Boe et al, 2014; Vukelic et al, 2014; Bauer et al, 2015; Vukelic and Gharabaghi, 2015a). We applied a delayed feedback onset paradigm to study the cortical activity over the sensorimotor cortex in the absence/presence of feedback provision

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