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

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.

Keywords: beta rhythms; brain-computer interface; brain-machine interface; brain-robot interface; neurorehabilitation; operant conditioning; reinforcement learning; stroke.

Figure 1

Time course of the neurofeedback training sessions. Each session comprised at least four runs (eight runs for P4, P5, P7, and P8) with a 2 min break between runs. Each run included 15 trials with relaxation and imagery trial performed in a randomized order. The feedback modality was interleaved between visual and proprioceptive across consecutive runs. Each trial started with a 2 s interval of imagery/relaxation without feedback followed by a 2.5 s section during which real time visual or proprioceptive feedback was provided. Following a 4 s inter-trial interval the next trial started.

Figure 2

Time course of a MI trial for right hand finger flexion with BRI. Each imagery trial starts with a 2 s period of right hand finger flexion imagery without feedback provision. Then at t = 2 s, contingent proprioceptive feedback is provided through stepwise flexion of the orthosis. The feedback section lasts for 2.5 s and at t = 4.5 s the trial ends and after a 4 s interatrial interval the next trial starts.

Figure 3

Spectral analysis of imagery and relaxation with feedback. Section (A) illustrates the log-transformed (10log₁₀) spectral power of imagery and relaxation trials during visual or proprioceptive feedback for eight participants. The solid lines represent mean spectral power for each task and their circumscribing shaded area indicates the standard deviation. Section (B) presents the results of repeated measures 2-way ANOVA that analyses the task (levels: relaxation and MI) and feedback modality (levels: visual and proprioceptive) effects on the log-transformed and z-cored spectral power in α and β bands for eight participants. The horizontal line in each boxplot, represents the mean value and the lower and upper whiskers depict the minimum and maximum values for each condition, respectively (sample size: 8; ^*p < 0.05; ^***p < 0.001; prop: proprioceptive).

Figure 4

Spectral analysis of imagery and relaxation without feedback. (A) Illustrates the log-transformed (10log₁₀) spectral power of imagery/relaxation trials without feedback (i.e., during the delay period before visual or proprioceptive feedback onset). The solid lines represent mean spectral power for each task and their circumscribing shaded area indicate the standard deviation. (B) Illustrates the results of repeated measures 2-way ANOVA that analyses the task (levels: relaxation and MI) and the modality effects before feedback (levels: visual and proprioceptive) onset on the log-transformed and z-cored spectral power in α and β bands for eight participants. The horizontal line in each boxplot, represents the mean value and the lower and upper whiskers depict the minimum and maximum values for each condition, respectively (sample size: 8; ^*p < 0.05; ^**p < 0.01; prop: proprioceptive).

Figure 5

Accuracy and ERD duration with and without feedback. (A) Classification accuracy with visual or proprioceptive feedback in α and β bands. (B) Event-related desynchronization (ERD) duration with visual or proprioceptive feedback in α and β bands. (C) Classification accuracy without visual or proprioceptive feedback in α and β bands. (D) ERD duration without visual or proprioceptive feedback in α and β bands. The horizontal line in each boxplot, represents the mean value and the lower and upper whiskers depict the minimum and maximum values for each condition, respectively (^*p < 0.05; ^**p < 0.01).