Proprioceptive feedback and brain computer interface (BCI) based neuroprostheses

Abstract

Brain computer interface (BCI) technology has been proposed for motor neurorehabilitation, motor replacement and assistive technologies. It is an open question whether proprioceptive feedback affects the regulation of brain oscillations and therefore BCI control. We developed a BCI coupled on-line with a robotic hand exoskeleton for flexing and extending the fingers. 24 healthy participants performed five different tasks of closing and opening the hand: (1) motor imagery of the hand movement without any overt movement and without feedback, (2) motor imagery with movement as online feedback (participants see and feel their hand, with the exoskeleton moving according to their brain signals, (3) passive (the orthosis passively opens and closes the hand without imagery) and (4) active (overt) movement of the hand and rest. Performance was defined as the difference in power of the sensorimotor rhythm during motor task and rest and calculated offline for different tasks. Participants were divided in three groups depending on the feedback receiving during task 2 (the other tasks were the same for all participants). Group 1 (n = 9) received contingent positive feedback (participants' sensorimotor rhythm (SMR) desynchronization was directly linked to hand orthosis movements), group 2 (n = 8) contingent "negative" feedback (participants' sensorimotor rhythm synchronization was directly linked to hand orthosis movements) and group 3 (n = 7) sham feedback (no link between brain oscillations and orthosis movements). We observed that proprioceptive feedback (feeling and seeing hand movements) improved BCI performance significantly. Furthermore, in the contingent positive group only a significant motor learning effect was observed enhancing SMR desynchronization during motor imagery without feedback in time. Furthermore, we observed a significantly stronger SMR desynchronization in the contingent positive group compared to the other groups during active and passive movements. To summarize, we demonstrated that the use of contingent positive proprioceptive feedback BCI enhanced SMR desynchronization during motor tasks.

Figure 1. Experimental Design.

A) Timing of an experimental trial. Each trial starts with a baseline of 3 seconds followed by an auditory instruction period. 2 seconds after the instruction a “Start” cue is presented and 5 seconds later an “End” cue. B) BCI. Participant wearing the 128 EEG channels cap seated with the hand attached to the orthosis showing the components used during all tasks C) Close look at the orthosis with the fingers attached. D) Schematic of the 128 channels and shaded in grey the 61 channels used during the experiments.

Figure 2. Motor task power distributions.

EEG frequency domain power topoplots for each motor task averaged over all participants of the contingent positive group (all 9 participants were right handed and performed the task with the right hand). The EEG power from 3 representative frequency bins (8–12; 12–18; 18–25 Hz) was averaged over the 5 seconds of each task and subtracted from the one obtained using the same process during rest. Red and blue color correspond to event related desynchronization (ERD) and to event related synchronization (ERS) with respect to rest in dB. The activity distribution is very similar for all motor tasks presenting a clear contralateral motor and parietal activation and an ipsilateral motor-pre-motor activation.

Figure 3. BCI performance using 2 different measures.

The midpoint of each box corresponds to the median value and the upper and lower margines correspond to the 25 and 75 percentiles. Differences marked with an asterisk are statistically significant. A) Number of orthosis moving onsets per session for each group during motor imagery without any feedback, with proprioceptive feedback (orthosis moved through BCI) (MIT&F) (task 2), passive and active movements (with natural visual and proprioceptive feedback). The contingent positive group outperformed the other 2 groups significantly and shows a significant learning effect during motor imagery without feedback (MIT) (task 1). B) Percent time moving the orthosis per session for each feedback group in the different tasks. The contingent positive and sham feedback percent of time moving the orthosis is always significantly higher compared to the contingent negative group with the exception of the motor imagery task without feedback (MIT) (task 1). In this condition the contingent positive group showed significantly higher BCI performance compared to the other feedback groups.