BCI Controlled Walking Simulator For a BCI Driven FES Device

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BCI Controlled Walking Simulator For a BCI Driven FES Device Po T. Wang, MS*, Christine King, MS*, Luis A. Chui, MD**, Zoran Nenadic*, DSc*, An Do, MD** *Biomedical Engineering Department- University of California, Irvine, Irvine, CA 92697 **Department of Neurology, School of Medicine- University of California, Irvine, Irvine, CA 92697 ABSTRACT To assess the feasibility of using an EEG- based brain computer interface (BCI) to control a lower extremity funcaonal electrical samulaaon (FES) device to restore ambulaaon in individuals with paraplegia due to spinal cord injury (SCI), a BCI controlled walking simulator was developed and tested. Study paracipants underwent electroencephalogram (EEG) recordings while they imagined standing idle and walking. The EEG signal changes between these two states were used to develop and train an online, real- Ame BCI system to control the ambulaaon of an avatar within a virtual environment (VE). All paracipants were able to immediately control the ambulaaon of the avatar. The successful implementaaon of this system suggests that integraang an EEG- based BCI with a lower extremity FES device is feasible. KEYWORDS Brain Computer Interface; FuncAonal Electrical SAmulaAon; Spinal Cord Injury; Gait BACKGROUND Spinal cord injury (SCI) paaents are olen unable ambulate and perform basic motor funcaons that are essenaal for independence and acaviaes of daily living. For individuals with low cervical, or thoracic level SCI, lower extremity motor funcaon can be lost making ambulaaon impossible (1). Currently, there are no biomedical soluaons to restore lost neurological funcaon of the lower extremiaes in such SCI paaents. As a result, biomechanical soluaons have been sought. One such alternaave is a funcaonal electrical samulaaon (FES) device, which can restore motor funcaon by samulaang paralyzed muscles via an external samulator. For individuals with paraplegia from SCI, current FES systems provide an alternate method for standing support and assistance in ambulaaon (2). The only FDA- approved lower extremity FES device is the Parastep device (Sigmedics, Fairborn, Ohio), though its adopaon has been fairly limited (3). Furthermore, the control of such FES devices is typically unintuiave, relying on a manual control box. Improving upon the intuiaveness of FES device control may lead to more widespread adopaon, which may be achieved by integraaon with brain computer interface (BCI) technology. 1

BCI is a technology that uses the predictable brain electrophysiological changes associated with cogniave processes, such as those seen in electroencephalogram (EEG) during motor imagery (MI) (4), in order to control external devices. BCI control of external assisave devices can help those with severe paralysis from SCI regain motor behavior, and the ability to control and manipulate their environment by thought, thereby bypassing a damaged spinal cord. In the past 30 years, extensive work has been done to develop and refine BCI control of assisave devices to help restore basic motor funcaons in paaents with severe motor paralysis. ApplicaAons have included the BCI control of a computer mouse, virtual keyboard, virtual reality avatar, and the limited control of an upper extremity FES device (2), (5), (6). Likewise, BCIs may potenaally allow individuals affected by paraplegia due to SCI to afain thought control of lower extremity prostheses, such as FES devices, thereby effecavely bypassing a disrupted spinal cord to restore lower extremity motor funcaon. There are several obstacles in developing this integrated BCI- FES technology. First, the brain electrophysiological signals associated with human ambulaaon need to be idenafied and characterized. Once characterized, these signal features must be used to develop a predicaon model, which in turn analyzes novel brain electrophysiological signals in real Ame and determines whether an individual intends to walk or stand idle. This predicaon model can then be implemented to direct the ambulaaon of an avatar in a virtual reality environment or to control an FES device. Here, we describe the design and successful implementaaon of an EEG- based BCI to control the ambulaaon of a virtual reality avatar. RESEARCH QUESTION Hypothesis: There are predictable EEG signal changes that occur during the walking motor imagery that can be exploited for the operaaon of an online, real- Ame BCI system to control human gait. By tesang this hypothesis, we can assess the feasibility of integraang an EEG- based BCI with a lower extremity FES device to restore intuiave ambulaaon to individuals with paraplegia due to SCI. METHODOLOGY Subjects and Training Data AcquisiAon: Three healthy subjects paracipated in this study (2 male, 1 female, ages 22-39). EEG signals were acquired using a subset of 32 channels of a 10-10 InternaAonal Standard EEG cap (see Figure 1). A bioamplifier system (Nexus 32BBS, Mind Media, The Netherlands) was used to acquire signals in a common average reference mode. The signals were amplified, band- pass filtered (0.01-50 Hz) and sampled at 512 Hz. Training data was collected by commercial solware (Biotrace, Mind Media, The Netherlands) while subjects performed MI as they watched a video of a 3- D avatar alternaang between 5 minutes of standing and walking. 2

Signal Processing and ClassificaAon: The EEG signals were labeled as either idle or walking. The labeled signals were then analyzed using automated exploratory methods (7), (8) to determine the significant neurophysiological signal features that differenaate walking and idle states. EEG signals were first divided into 4- second segments, resulang in 75 trials for both idle and walking states. For each channel, spectral energies from 6 to 26 Hz were calculated in 2- Hz bins using fast Fourier transform. This resulted in 320- D data for each trial (10 Photo 1: EEG Placement System frequency bins x 32 channels). Classwise principal component analysis (7) in conjuncaon with linear discriminant analysis or approximate informaaon discriminant analysis (8) was then used to reduce the input dimension to 1- D feature space. The linear Bayesian classifier was used to classify the mental state as either idle or walking. EvaluaAon of BCI Control: Subjects were seated in front of a computer screen, while EEG data were acquired and classified in real- Ame. A custom- built Matlab (Mathworks, NaAck, MA) script was developed for this purpose. A 3- D avatar in an open field virtual environment (VE), using Garry s Mod for Half Life 2 (Source Engine, Valve CorporaAon, Bellevue, Washington), was displayed from a third person, over- the- shoulder perspecave (see Figure 2). Subjects were instructed to use walking MI to move his/her avatar to greet a series of 10 non- player characters (NPCs) posiaoned along a linear path in front of the subject s avatar, similar to Leeb et al (9). Subjects must stop within a proximity of the NPC and stand sall long enough to receive a verbal greeang. ALer this greeang, subjects were to iniaate walking towards the next NPC unal all 10 were greeted. RESULTS Analysis of the 150 trials of training data revealed that subjects had ~80.0% average predictability of idle and walking MI states based on EEG data. Considering a chance level of 50%, this demonstrates a significant predictability between the two states (p value 2.9869e- 014). Photo 2: Virtual Reality Avatar 3

ALer 10 minutes of training data collecaon, all subjects obtained meaningful control immediately upon their first afempt at compleang the assigned task. Subject 1 had 8.50±0.71 NPC (mean ± standard deviaaon) greeangs per trial, and required an average Ame of 162 sec to complete the task. Subject 2 averaged 8.00±1.00 NPC greeangs per trial, and required an average Ame of 229 sec. Subject 3 averaged 7.00±2.16 NPC greeangs per trial, and required an average Ame of 103 sec. For the purposes of comparison, a simulated random walk was generated. Using randomly generated states, 100 trials of random walk allowed the avatar to get an average of 2.7±1.30 NPCs and an average Ame of 76 sec. When compared to simulated random walk, all subjects demonstrated purposeful control (p < 0.0001). These performances are displayed in the table below (Table 1). DISCUSSION We demonstrated a successful implementaaon of a real- Ame, asynchronous BCI, to control ambulaaon within a VE. The offline EEG signal analysis of idle and walking MI demonstrated that the two states had highly predictable electrophysiological signal differences. Using these differences to build the state predicaon model for online BCI operaaon, all subjects paracipaang in this study obtained immediate and purposeful BCI control. Since this linear ambulaaon in a VE is the closest scenario to actual use of a potenaal BCI- controlled FES device, we conclude that such a concept may be feasible. Subject Score (Number of stops at NPCs out of a Average Time to Completion total score of 10) 1 8.50±0.71 162 sec 2 8.00±1.00 229 sec 3 7.00±2.16 103 sec Random Walk 2.70±1.30 76 sec Table 1: BCI Control of Avatar Results It should also be noted that the subject performances seen here are from a single experimental session for BCI- naïve individuals. Whereas other BCI techniques may require subjects to train over a extended Ame periods (from days to months (10), the technique employed here allows users to gain immediate control. This BCI technique, which employed an automated signal analysis techniques described in (7), (8), allowed for a BCI setup in which there is no manual selecaon of EEG channels or signal features. Subjects can ualize a natural MI, i.e. imaginaaon of walking to walk in the VE. Since training is brief and automated, and the cogniave process to operate the BCI is intuiave, minimal outside interference is required to set up the automated system. This may have implicaaons in future pracacal clinical BCI applicaaons. Further subject training is expected to help improve the performance. 4

To have full control over a lower extremity FES device, other degrees of freedom of control, such as turning lel and right will need to be implemented and tested in future studies. In addiaon, since the target populaaons for lower extremity FES devices are individuals who are paraplegic from SCI, further studies are also needed to determine how well this technique extends to these individuals. REFERENCES 1. Dietz V, Nakazawa K, Wirz M, Erni T. Level of Spinal Cord Lesion Determines Locomotor AcAvity in Spinal Man. Experiments in Brain Research. 128(3): 405-409 (1999). 2. Pfurtscheller G, Müller GR, Pfurtscheller J, Gerner HJ, Rupp R. Thought - Control of FuncAonal Electrical SAmulaAon to Restore Hand Grasp in a PaAent with Tetraplegia. Neuroscience Lefers. 351(1): 33-36 (2003). 3. Brissot R, Gallien P, Le Bot MP, Beaubras A, Laisné D, Beillot J, Dassonville J. Clinical Experience with FuncAonal Electrical SAmulaAon- Assisted Gait with Parastep in Spinal Cord- Injured PaAents. Spine. 25(4): 501-508 (2000). 4. Anderson KD. ConsideraAon of user prioriaes when developing neural prostheacs. J Neural Eng. 6(5): 55003 (2009). 5. Dornhege G, Millán J, Hinterberger T, McFarland D, Müller KR. Towards Brain- Computer Interfacing (1st ed.). Cambridge, MA: MIT Press (2007). 6. Wolpaw JR, Birbaumer N, McFarland DJ, Pfurtscheller G, Vaughan TM. Brain- Computer Interfaces for CommunicaAon and Control. Clinical Neurophysiology. 113(6): 767-791 (2002). 7. Das K, Rizzuto DS, Nenadic Z. Mental State EsAmaAon for Brain- Computer Interface. IEEE T. Bio- med. Eng. 56(8): 2114-2122 (2009). 8. Das K., Nenadic Z. Approximate informaaon discriminant analysis: A computaaonally simple heteroscedasac feature extracaon technique, Pafern Recogn. 41 (5): 1548-1557 (2008). 9. Leeb R, Friedman D, Müller- Putz GR, Scherer R, Slater M, Pfurtscheller G. Self- Paced (Asynchronous) BCI Control of a Wheelchair in Virtual Environments: A Case Study with a Tetraplegic. Comput Intell Neurosci: 79642 (2007). 10. Birbaumer N, Murguialday AR, Cohen L. Brain- computer interface in paralysis. Curr Opin Neurol. Dec;21(6):634-8 (2008). 5

ACKNOWLEDGMENTS This research is funded by the Roman Reed Spinal Cord Injury Research Fund of California. (RR 08-258, and RR 10-281). Author Contact Information: Po T Wang, University of California, Irvine, Irvine, CA 92697, Phone: 949-892- 3652, Email: ptwang@uci.edu 6