Neuroscience Letters 351 (2003) 3336 www.elsevier.

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Thought control of functional electrical stimulation to restore hand grasp in a patient with tetraplegia
Gert Pfurtschellera,b,*, Gernot R. Mullera, Jorg Pfurtschellerc, Hans Jurgen Gernerd, Rudiger Ruppd
a

Department of Medical Informatics, Institute of Biomedical Engineering, Graz University of Technology, Inffeldgasse 16a, A-8010 Graz, Austria b Ludwig Boltzmann Institute of Medical Informatics and Neuroinformatics, Inffeldgasse 16a, A-8010 Graz, Austria c Department for Traumatology, Hospital Villach, Nikolaigasse 43, 9500 Villach, Austria d Orthopedic Hospital of Heidelberg University, Department II, Schlierbacher Landstrabe 200a, 69118 Heidelberg, Germany Received 30 April 2003; received in revised form 14 July 2003; accepted 4 August 2003

Abstract The aim of the present study was to demonstrate the rst time the non-invasive restoration of hand grasp function in a tetraplegic patient by electroencephalogram (EEG)-recording and functional electrical stimulation (FES) using surface electrodes. The patient was able to generate bursts of beta oscillations in the EEG by imagination of foot movement. These beta bursts were analyzed and classied by a brain-computer interface (BCI) and the output signal used to control a FES device. The patient was able to grasp a cylinder with the paralyzed hand. q 2003 Elsevier Ireland Ltd. All rights reserved.
Keywords: Brain-computer interface (BCI); Functional electrical stimulation (FES); Tetraplegia; Grasp function restoration; Neuroprosthesis

Since the pioneering work of Nicolelis [12] with implanted electrodes in monkeys cortex and the control of a multijoint robot arm by thoughts it is a highly realistic perspective that a brain-computer interface (BCI) [13] might help patients with paralyzed limbs to restore their motor functions through functional electrical stimulation (FES). In this case, however, arrays of microwires have to be implanted and the type of intended movement has to be predicted by on-line processing of neural assembly activity. In the last few years also implantable systems for FES of muscles (neuroprosthesis) have shown their efciency concerning functional restoration in chronic applications [6]. In the future, both, the data acquisition and the muscle stimulation will very likely be done invasively. In the meantime non-invasive electroencephalogram (EEG) recordings can be used to generate a control signal for the operation of the FES. Such an EEG-based control of an implantable neuroprosthesis was reported by Lauer et al. [4]. Here we report for the rst time a thought-based FES control using surface electrodes in a tetraplegic. The tetraplegic patient we report in this study is a 28 year old man suffering from a traumatic spinal cord injury since April 1998. He is affected by a complete motor and sensory
* Corresponding author. Tel.: 43-316-873-5301; fax: 43-316-8735349. E-mail address: pfurtscheller@tugraz.at (G. Pfurtscheller).

lesion below C5 and an incomplete lesion below C4. As a preparation for the FES the patient got his muscles stimulated for a training period of 10 months (45 min per day, 5 days a week) until he got a strong and fatigue resistant contraction of the paralyzed muscles of the arm and shoulder. The residual volitional muscle activation of his left upper extremity is as followed. Shoulder: active abduction and exion up to 908; full rotational range of motion (ROM); grade 3/5 before grade 4/5 after training; full passive ROM. Elbow: active exion grade 3/5 before grade 4/5 after training; no active extension (triceps grade 0/5); pro- and supination possible (partly trick movement); full passive ROM. Forearm, hand and ngers: M. extensor carpi radialis (ECR) showed a palpable active contraction (grade 1/5) without change over training; all other muscles grade 0/5; almost full passive ROM in nger joints; full wrist, thumb and forearm ROM. Since the patient is able to perform restricted movements only with his left upper extremity (right elbow exion grade 1/5) which are necessary to move objects in space it was obvious to use the left hand for a hand grasp restoration. In 1999 we started BCI training with different types of motor imagery in order to check for alternative methods for

0304-3940/03/$ - see front matter q 2003 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/S0304-3940(03)00947-9

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G. Pfurtscheller et al. / Neuroscience Letters 351 (2003) 3336

operation of environmental control systems. (Details about this training are reported elsewhere [7]). The most interesting result was that thousands of foot movement imaginations in the course of the training phase over a period of several months resulted from 1 day to another in the induction of stable and midcentral focused beta oscillations with a dominant frequency of 17 Hz [7]. A close explanation is that the imagery task may have changed the properties of neural networks in the midcentral area close to the primary foot representation area and the supplementary motor area in such a way, that foot motor imagery is accompanied by oscillatory activity in the beta band. This result is somewhat surprising, since activation of a cortical area or network is generally accompanied by a desynchronization of oscillatory activity in the frequency band below 30 Hz [8] and not by a synchronization process. These induced beta oscillations could be found not only in the rst year after the training phase but can still be induced, whenever the subject imagines a foot movement, even though just a small number of control sessions with motor imagery have been performed during the last years. Obviously, these beta oscillations offer a comfortable brain switch to control a FES. The aim of the following experiment was to proof the feasibility of controlling the FES with surface electrodes via a BCI. In Fig. 1 the experimental setup is displayed. EEG was bipolarly recorded from two electrode pairs located over the right hand (2.5 cm anterior and posterior to position C3) and over the foot representation areas (2.5 cm anterior and posterior to position Cz), amplied (high pass lter 0.5 Hz, low pass lter 30 Hz) and digitized (sampling frequency was 128 Hz). The signals were processed by a Matlab program and real-time Simulink Model (MathWorks Inc., USA) [3]. After bandltering and logarithmizing, a Fishers linear discriminant analysis was used for single trial separation [5, 9]. The classier was trained in a short training session while the subject performed 160 cue-dependent right hand or foot movement imaginations. Whenever the output of the classier in the online session exceeded a predened threshold, a switch signal was generated. This signal is conducted to the accumulator driven neuromuscular stimulation unit via an optoelectronic coupler. Surface electrodes, placed at the forearm of the patient (see also Fig. 1), are used to apply the stimulation pulses for activation of the paralyzed muscles. The moving hand provides a visual feedback for the patient. We used an eight channel microcomputer-controlled stimulator (Microstim 8, Krauth and Timmermann, Germany) with biphasic (xed pulse width of 300 ms for each phase), rectangular, constant-current pulses for stimulation of muscles from the forearm and the hand of the tetraplegic patient. The frequency of the stimulation pulses during the experiment was set to 16 Hz in order to achieve a sufciently smooth and strong contraction of the muscles without extensive fatigue. The current setting of the FES electrodes was chosen in

Fig. 1. EEG-based BCI system operates a FES device with three pairs of surface electrodes. The six positions of the electrodes are indicated. The patient is able to grasp a cylinder with the paralyzed hand when the FES is switched-on by beta burst in the EEG induced by foot movement imagination.

such a way that the patient was enabled to perform a switchtriggered lateral hand grasp, by which at objects could be grasped between the exed ngers and the exing thumb. To achieve this kind of grasp four basic functional muscle groups have to be accessed: The nger (M. ext. digitorum communis EDC) and thumb (M. ext. pollicis longus EPL) extensors for hand opening, the nger exors (M. ex. digitorum supercialis FDS, M. ex. digitorum profundus) for hand closing, the thumb exor (M. ex. pollicis longus FPL) for grasping and the wrist extensors (M. ext. carpi radialis longus/brevis ECRL/ECRB) for stabilization of the hand. The activation pattern of the muscles for lateral prehension was divided into the following grasp phases whereby each mentally induced beta burst triggered a sequential phase transition: A. hand opening by activation of EDC and EPL electrodes; B. closing of ngers by deactivation of EDC and moderate activation of FDS and FPL (minimal closing of thumb because EPL electrode still active); C. closing of thumb by deactivation of EPL electrode and full activation of FDS and FPL;

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D. opening of hand by deactivation of FDS and FPL and activation of EDC and EPL; E. idling state, deactivation of EDC and EPL, hand is relaxed. These ve phases were implemented in the stimulator with commercially available software. The stimulation amplitude was adjusted for each channel independently according to the desired motion. In our actual setup we used a three channel conguration: a pair of small, round electrodes (diameter 32 mm) were placed near the motor point of EDC, of EPL and one pair near the motor points of FDS and FPL. We failed to stabilize the wrist with the use of short stimulation pulses because of an almost completely denervated ECRL. We were not using an indifferent-different electrode conguration in order to avoid contractions of other muscles (spill-over) caused by unknown current paths or summation at the indifferent electrode. Keeping the thumb in extended position during exion of the ngers was achieved by stimulating simultaneously the M. exor pollicis longus (FPL) and the M. extensor pollicis longus (EPL). The stimulation amplitude of the EPL electrodes was set to a level at which a strong activation of the thumb extensor occurs and the amplitude of the FDS/FPL electrodes was adjusted to the lowest level necessary for a sufcient closing of the ngers. Due to this activation scheme we did not need electrodes for the stimulation of the short muscles of the thumb [1], which are difcult to x, tend to come off easily and thereby limit the usefulness of FES for activities of daily living. When in the BCI the rst imagination (foot movement) was detected, the stimulator was started and hand opening was induced by EDC and EPL stimulation (phase A). Each repetition of the foot movement imagination resulted into a shift to the next subsequent grasp phase, stepwise from (B) to (D). A refractory period of 5 s after each switch excluded the possibility of switching too fast. If the last phase (D) was reached the next switch signal from the BCI stopped the stimulation and the FES device moved into an idling state (E). Then the device was ready for repetition of the whole grasping sequence. Serious problems with an EEG-based BCI are in generally contaminations of the EEG activity by muscle (EMG) artefacts. They are of particular importance, especially if EEG electrodes are placed over frontal and temporal regions. In our case the most relevant brain signal used for grasp control is restricted to the midcentral area as demonstrated by full head 60-channel EEG recordings. If only two bipolar EEG channels are used, the EMG activity is visible in the lateralized EEG channel (Fig. 2B, 20 60 Hz), but completely absent in the midcentral EEG recordings (Fig. 2D, 20 60 Hz). Therefore an impact of EMG activity on the BCI output signal can be ruled out completely. The bandpass ltered EEG of both are displayed in Figs. 2A,C. The rst three foot movement imaginations associ-

Fig. 2. (A, C) Bandpass ltered (1519 Hz) EEG channels C3 and Cz recorded during the rst 3 foot movement imaginations (i1, i2 and i3) of one complete grasp sequence. The vertical lines indicate the start-on of the individual grasp phases. (B, D) Bandpower time courses (1519 and 20 60 Hz) of EEG channels C3 and Cz averaged over the ve grasp phases with movement start at second 0 (amplitudes in arbitrary units).

ated with induced beta oscillations are marked with i1, i2 and i3. A strong bandpower increase can be observed especially at channel Cz after during every motor imagery (Fig. 2D). In fact, a classier would not be necessary because the beta oscillations are large enough to be detected by a single threshold detector. In principle, EEG signals can be contaminated by both, EMG signals and by artifacts resulting from the use of FES devices. Since electrical stimulators for functional neuromuscular stimulation with surface electrodes are based on stimulation pulses with an amplitude up to 150 V and with low frequencies (10 20 Hz), we rst conducted some experiments concerning the signal to noise ratio of recorded EEG signals while simultaneously using a FES device. Bipolar EEG derivations were chosen to minimize environmental inuences and stimulation artefacts in the main EEG frequency range up to 30 Hz. Higher harmonics of the stimulation signal are found in the EEG spectra, but they do not increase the error rate of the classication process. We have experienced from our clinical practice that electrical stimulation with surface electrodes has some limitations concerning selective stimulation especially of deeper muscle groups, reproduction of grasp patterns on a day-by-day basis, and position-independent stability of the grasp pattern. Due to these restrictions systems based on

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G. Pfurtscheller et al. / Neuroscience Letters 351 (2003) 3336 implantable neuroprosthesis for functional electrostimulation of the upper extremity, Handchir. Mikrochir. Plast. Chir. 33 (3) (2001) 149152. C. Guger, A. Schlogl, C. Neuper, D. Walterspacher, T. Strein, G. Pfurtscheller, Rapid prototyping of an EEG-based brain-computer interface (BCI), IEEE Trans. Neural. Syst. Rehabil. Eng. 9 (1) (2001) 49 58. R.T. Lauer, P.G. Peckham, K.L. Kilgore, EEG-based control of a hand grasp neuroprosthesis, NeuroReport 10 (1999) 17671771. K. Lugger, D. Flotzinger, A. Schlogl, M. Pregenzer, G. Pfurtscheller, Feature extraction for on-line EEG classication using principal component analysis and linear discriminants, Med. Biol. Eng. Comput. 36 (1998) 309 314. P.H. Peckham, M.W. Keith, K.L. Kilgore, J.H. Grill, K.S. Wuolle, G.B. Thrope, P. Gorman, J. Hobby, M.J. Mulcahey, S. Carroll, V.R. Hentz, A. Wiegner, Efcacy of an implanted neuroprosthesis for restoring hand grasp in tetraplegia: a multicenter study, Arch. Phys. Med. Rehabil. 82 (10) (2001) 13801388. G. Pfurtscheller, C. Guger, G. Muller, G. Krausz, C. Neuper, Brain oscillations control hand orthosis in a tetraplegic, Neurosci. Lett. 292 (2000) 211 214. G. Pfurtscheller, F.H. Lopes da Silva, Event-related EEG/MEG synchronization and desynchronization: basic principles, Clin. Neurophys. 110 (1999) 18421857. G. Pfurtscheller, C. Neuper, Motor imagery and direct brain-computer interface communication, Proc. IEEE 89 (7) (2001) 11231134. M.R. Popovic, D.B. Popovic, T. Keller, Neuroprostheses for grasping, Neurol. Res. 24 (5) (2002) 443452. P. Taylor, J. Esnouf, J. Hobby, The functional impact of the Freehand System on tetraplegic hand function, clinical results, Spinal Cord 40 (11) (2002) 560566. J. Wessberg, C.R. Stambaugh, J.D. Kralik, P.D. Beck, M. Laubach, J.K. Chapin, J. Kim, S.J. Biggs, M.A. Srinivasan, M.A. Nicolelis, Real-time prediction of hand trajectory by ensembles of cortical neurons in primates, Nature 408 (2000) 361 367. J.R. Wolpaw, N. Birbaumer, D.J. McFarland, G. Pfurtscheller, T.M. Vaughan, Brain-computer interfaces for communication and control, Clin. Neurophysiol. 113 (6) (2002) 767791.

surface electrodes are only used for testing purposes or in temporary applications [10]. Over the last few years implantable neuroprostheses especially for the restoration of grasp function in tetraplegic patients have become available for chronic use [2]. These devices overcome the limitations mentioned above and have already shown to be of high benet for their users in everyday life [11]. Since the stimulation system with surface electrodes uses basically the same pulse waveforms and frequencies as implantable systems, the experiment described here may serve as a noninvasive evidence for the feasibility of controlling an implantable neuroprosthesis via a BCI. By using multichannel EEG-recordings and migration to implantable systems it is likely to control even more degrees of freedom independently. This provides the basis for the development of thought-controlled neuroprostheses which might help patients with severe paralysis to regain control over their body.

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Acknowledgements This project was supported by the Austrian Federal Ministry of Transport, Innovation and Technology, project GZ140.587/2 and the Allgemeine Unfallversicherungsanstalt (AUVA).

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