Brain-Computer Interface and Functional Electrical Stimulation for

Neurorehabilitation of Hand in Sub-acute Tetraplegic Patients

Functional and Neurological Outcomes

Bethel C. A. Osuagwu

, Leslie Wallace

Mathew Fraser

and Aleksandra Vuckovic

School of Engineering, College of Engineering and Science, University of Glasgow, Glasgow, U.K.

Queen Elizabeth National Spinal Injuries Unit, Southern General Hospital, Glasgow, U.K.

Keywords: Brain Computer Interface, Functional Electrical Stimulation, Neurorehabilitation, Tetraplegia, Hand.

Abstract: The aim of this paper is to compare neurological and functional outcomes between two groups of subacute

hospitalised patients with incomplete tetraplegia receiving two experimental therapies. Seven patients

received 20 sessions of Brain Computer Interface (BCI) controlled Functional Electrical Stimulation (FES)

while five patients received 20 sessions of passive FES. The treatment assessment measures were EEG during

movement attempt, Somatosensory evoked potential (SSEP) of the ulnar and median nerve and the range of

movement of both wrists. Patients in both groups initially had intense cortical activity during a movement

attempt, which was wide-spread, not restricted to the sensory-motor cortex. Following the treatment, cortical

activity restored towards the activity in able-bodied people in BCI-FES group only. SSEP also returned in 3

patients in BCI-FES group while in FES group no changes were noticed. The range of movement improved

in both groups and results are inconclusive due to the small number of participants. This study confirms the

feasibility of prolonged BCI-FES therapy in a hospital setting. The results indicate better neurological

recovery in BCI-FES group. Larger and longer studies are required to assess the potential advantage of BCI-

FES on functional recovery.

1 INTRODUCTION

Brain Computer Interfaces (BCI) controlled

functional electrical stimulation (FES) has two main

applications for neurologically injured patients: to

restore the lost function as an assistive device for a

long term use (Pfurtscheller et al. 2003) or to improve

a partially preserved function. In the latter case, BCI-

FES is used as a rehabilitative device on a short-term

basis (Fei et al. 2008, Daly et al. 2009, Tan et al. 2011,

Tam et al. 2011, Young et al. 2014, Mukaino et al.

2014, Li et al. 2014). The main advantage of

rehabilitation based on BCI-FES over FES alone is

that it is based on patient’s active intention to move

and it simultaneously activates sensory and motor

pathways, thus promoting neuroplasticity based on

associative, Hebbian learning (Hebb 1949).

Experiments on able-bodied people showed that

Motor Evoked Potential (MEP) is enhanced more

when the grasp function was guided by BCI-FES than

when it was guided by either BCI or FES alone

(McGie et al.2014).

Most publications advocating BCI-FES for

rehabilitation purposes are case studies on stroke

patients (Fei et al. 2008, Daly et al. 2009, Tan et al.

2011, Tam et al. 2011, Young et al. 2014, Mukaino et

al. 2014). Larger studies or studies including other

groups of patients are rare. Only recently a BCI-FES

study on stroke patients has been published including

a control and a treatment group (Li et al. 2014). Li et

al. showed that patients receiving BCI-FES achieved

better functional and neurological recovery than

patients receiving FES alone. Another randomised

controlled trial on stroke patients (Kim et al. 2015)

showed better functional improvement in patients

receiving BCI-FES as compared to patients receiving

FES only, but failed to present any result showing

brain activity pre and post therapy. Also recently, our

group showed the feasibility of BCI-FES therapy on

spinal cord injured patients. In that study on two

patients early after injury, we showed that BCI-FES

could be therapeutically used in incomplete

tetraplegic patients in a hospital setting (Vuckovic et

al. 2015). In the current study, we further explore the

potential of BCI-FES for rehabilitation of hand

functions in people with tetraplegia (high level spinal

Osuagwu, B., Wallace, L., Fraser, M. and Vuckovic, A..

Brain-Computer Interface and Functional Electrical Stimulation for Neurorehabilitation of Hand in Sub-acute Tetraplegic Patients - Functional and Neurological Outcomes.

In Proceedings of the 3rd International Congress on Neurotechnology, Electronics and Informatics (NEUROTECHNIX 2015), pages 15-23

ISBN: 978-989-758-161-8

cord injury SCI). We compare neurological and

functional outcome between the group of patients

receiving 20 sessions of BCI-FES hand therapy with

a matched control group receiving the same number

of therapy sessions with passive FES.

2 MATHERIALS AND METHODS

2.1 Patients

Twelve subacute patients with tetraplegia (12 male,

51.7±18.4 min 20, max 75) participated in the study.

All patients were three months or less post-injury,

were still at the hospital and had therefore received

daily standard hand therapy in addition to the

experimental therapy (Table 1). Their level of injury

was cervical, C4-C7 affecting both hands. All patients

had incomplete injury, ASIA B or C, meaning that

they had partially preserved sensation by no

preserved movement (ASIA B) or had partially

preserved both sensation and movement (ASIA C)

(Marino et al., 2003). Because of the small number of

patients with SCI, a semi-random order of

recruitment was created in advance assigning patients

to the one or the other treatment group. Patients were

assigned upon recruitment to a corresponding group

(20 patients in total are planned for the whole study,

that is still running).

The study has been approved by the National

Healthcare Service Regional Ethical Committee. This

study is a registered clinical trial NCT01852279.

2.2 Initial and Final Assessments

The study consisted of three phases: initial

assessment, treatment and final assessment. Initial

and final assessment consisted of identical tests. Test

were divided into neurological and functional. The

neurological tests comprised of

electroencephalography (EEG) recording during left

and right hand movement attempts (MA) and somato-

sensory evoked potential (SSEP) of the median and

ulnar nerves of both hands. The functional

assessments consisted of measurement of the range of

movement of the left and right wrist and Manual

Oxford Scale muscle test MMT (Porter, 2013) of

hand and arm muscles. MMT test has 6 grades (0=no

contractions felt in the muscle, 5=hold test position

against strong pressure). Due to the nature of the

injury, initially patients had better preserved

voluntary control of muscles in shoulders and upper

arms (MMT=3 to 4) than of the forearm, wrist and

hand. Initial MMT of the forearm/hand muscles was

between 0 and 2 (MMT=2 moves through the range

of motion through a horizontal plane, i.e. cannot resist

gravity). Formarm/hand muscles involved supinator,

pronator, extensor digitorum communis, extensor

carpi radialis brevis and longus, flexor carpi radialis

and flexor digitorum profundis. Due to the large

number of assessed muscles, the MMT outcome will

be presented elsewhere. Functional and neurological

assessments were performed on different days, to

minimise patients’ discomfort.

2.2.1 Cue-based Movement Attempt

A standard cue-based paradigm was implemented

with rtsBCI, a part of the open source Biosig toolbox

(Vidaurre et al. 2011), implemented under Simulink,

MATLAB (Mathworks, USA). Patients sited in their

wheelchairs approximately 1.5 from a computer

screen. A trial started at t=-3 s and ended at t=3 s. At

t=-1s a warning cue (a cross) was presented at the

screen. At t=0s an execution cue (an arrow) appeared

on the screen. After t=3s the screen stayed blank for

a random period of 1-3 s before the next trial. Total

time between two trials was random, between 7s and

9s. There were two types of arrows, an arrow pointing

to the right for MA of the right hand and to the left for

the MA of the left hand. Patients were instructed to

attempt waving their hand continuously from t=0s till

t=3s. Note that unlike able-bodied persons, paralysed

people can differentiate between imagination of

movement and movement attempt, in the absence of

overt movements. Because the aim of the study was

the restoration of voluntary hand movement, we

considered MA being more appropriate task than the

imagination of movement. There were 120 trials (60

for each hand) divided in 4 runs each consisting of 30

trails (15 for each hand)

During this task patients’ EEG was measured with

48 electrodes placed according to the 10/10 system

(Jurcak et al, 2007) using usbamp device (Guger

technologies, Austria). Electrodes covered the central

region of the sensory-motor cortex, parietal cortex

and sparsely covered the frontal and occipito-

temporal cortices. Forty seven electrodes were used

to record EEG while one electrode was placed at the

lateral cantus of the orbicularis oculi of the right eye

to record electrooculogram (EOG). EEG was

recorded with respect to the linked-ear reference with

the sampling frequency of 256 samples/s. Impedance

was kept under 5 kΩ. A ground electrode was placed

at the electrode location AFz. EEG signal was filtered

on-line between 0.5 and 60 Hz and notch-filtered at

NEUROTECHNIX 2015 - International Congress on Neurotechnology, Electronics and Informatics

Table 1: Information about patients. First 7 patients

received BCI-FES therapy, last five received FES therapy.

Patient Injury level ASIA Age

1 C6 C 70

2 C4 B 25

3 C6 B 32

4 C5 C 20

5 C6 C 74

6 C5 B 51

7 C6/7 C 61

8 C5 C 36

9 C5/6 C 61

10 C6 C 75

11 C4 B 51

12 C6 C 64

50 Hz using the IIR digital Butterworth filter built

into a modular amplifier.

2.2.2 Off-line Analysis of EEG during

Movement Attempt

Continuous data were split into trials starting at t=-3

and ending at t=3s, with respect to the execution cue.

Datasets of each patients were decomposed into

independent components (IC) (Hyvarinen, and Oja,

2000) using Infomax algorithm implemented in

EEGlab (Delorme and Makeig, 2004) under Matlab

(Mathworks, USA). Components were visually

inspected and components corresponding to noise

(line noise, EOG, EMG and ECG) were removed and

signal was back projected into EEG domain. A

common average reference was computed for all

channels.

Time-frequency analysis was performed in

EEGlab based on event-related spectral perturbation,

which is an extension of the event-related

synchronisation/desynchronisation (ERD/ERS)

(Pfurtscheller and da Sliva, 1999). A baseline period

was from t=-2s till t=-1s. The Morlet wavelet

transform was used to perform a time-frequency

analysis in 3-60 Hz, with a Hanning-tapered window

applied and the number of cycles set to 3 at the lowest

frequency.

An average ERD/ERS across patients was created

using Study structure in EEGlab. Average ERD/ERS

scalp maps for a chosen frequency band and time

window were created through Study structure. The

statistical non-parametric method with Holm’s

correction for multiple comparisons (Holm, 1979)

was used to test for statistically significant differences

between ERD/ERS scalp maps before and after

treatments of patients within a group, with a

significance level set to p=0.05.

Figure 1: BCI setup showing computation of TDP.

2.2.3 Somato-sensory Evoked Potential

Somatosensory evoked potential is a response of the

central nervous system to an electrical stimulation

(Gugino and Chabot, 1990). The SSEP may infer

motor functions on the assumption that an injury

severe enough to a damage the sensory pathways

may also affect motor pathways. The SSEP was

analysed to detect the latency and the amplitude of the

N20 peaks that occurs around 20ms following an

electrical stimulus. In able-bodied people N20 latency

is highly repeatable. The increased delay of N20 is an

indicator of the damage of the neural pathways. The

damage results in axon demyelination which causes

reduced propagation velocity along the axon,

manifested as the increased latency of N20 peak. In

more severe cases, the amplitude of N20 is reduced

or it is completely absent (Curt and Dietz 1999). The

recovery of the neural pathways, followed by re-

myelination, results in re-appearance of the N20 and

in reduced N20 latency.

In the current study SSEP was measured for the

left and right median and ulnar nerves, as these two

nerves share innervation of the wrist and fingers. All

the four nerves were stimulated separately, one at the

time using a single pulse electrical stimulation

(Model DS7, Digitimer,UK). Electrodes were

attached on the surface of the skin above the

corresponding nerves at the wrist. A stimulation

intensity was set so that a small visible twitch could

be observed at the thumb for the median nerve and at

the little finger for the ulnar nerve. For each nerve,

electrical stimulation was delivered 250 times with a

frequency of 3 Hz. SSEP of the right hand median and

ulnar nerve was measured at the electrode location

CP3 and of the left hand nerves at the electrode

location CP4. EEG was recorded with usbamp, with

a sample rate of 4800 Hz, band passed between 2-

2000 Hz and notch filtered at 50 Hz. Individual

responses were averaged with respect to the onset of

stimulation.

Brain-Computer Interface and Functional Electrical Stimulation for Neurorehabilitation of Hand in Sub-acute Tetraplegic Patients -

Functional and Neurological Outcomes

2.2.4 Measurement of the Range of Motion

of the Wrist

In patients with incomplete tetraplegia who have

partially preserved control of movement, the range of

motion (ROM) is reduced, as compared to the able-

bodied people. The ROM of the right and left hand

wrist, during extension and flexion was measured

using Zebris system (Zebris Medical GmbH,

Germany). The measurement procedure is based on

the travel time measurement of ultrasonic pulses. The

pulses are emitted by three stationary transmitters and

are recorded by small markers which are ultrasound

microphones. The Zebris system markers were placed

on bony landmarks on the subject’s hand at the radius

(marker 1), carpometacarpal joint (marker 2) and the

carpometacarpal bone (of the index finger or the

thumb, marker 3). The ROM was calculated as an

angle between intersecting imaginary lines formed

between markers 1-2 and markers 2-3.

2.3 Therapy Sessions

Treatment consisted of 20 sessions, each lasting

approximately one hour, organised 3-5 times weekly,

depending on patients’ availability. One group of

patients received active therapy; they attempted hand

movement that was detected by BCI which then

activated FES applied to their hand muscles (BCI-

FES group). The other group of patients received

passive on-off FES therapy (FES group). They got

the same amount of FES stimulation as BCI-FES

group but the stimulator was activated automatically.

In both groups, therapy was applied on both hands, as

spinal cord injury typically affects both hands, though

not necessarily to the same extent.

2.3.1 Off-line Brain Computer Interface

based on Movement Attempt

The BCI algorithm was based on time-domain

parameters (TDP) (Vidaurre et al. 2009). On each

day, a quick off-line session was recorded consisting

of 20 trials for each hand, following the experimental

protocol described in 2.2.1. In our previous study on

able-bodied people (Osuagwu and Vuckovic 2014),

we showed that such short recording session results

in an initial classification accuracy between 75% and

100%. Note that off-line classifier parameters are

further updated and refined during on-line BCI, as

described later in the text. During therapy sessions,

patients’ EEG was recorded from three pairs of

bipolar electrodes located over the sensory-motor

cortex, CP3-CF3, CPz-CFz and CP4-CF4. EEG was

recorded with usbamp, band-filtered online between

0.5 and 30 Hz (5

order Butterworth filter), with

sampling frequency 256 Hz. The ground electrode

was attached to the ear. The impedance was kept

under 5 kΩ.

Time domain parameters were calculated for 7-30

Hz EEG frequency band using equation 1

()

tdX

TDP ,...0var =













(1)

Where X(j) is a wide-band EEG, t is a current sample,

j is a derivative (p=9), ‘var’ is a variance operator and

‹.› was used to present smoothing/averaging

operator. Smoothing was a result of applying a one

second long moving average filter. The variance

operator in this equation acts as the band-power

operator since the variance of the band-passed filtered

signal is equal to the bandpower (Vidaurre et al.

2009). The BCI setup showing computation of TDP

is shown in Fig. 1. The squaring and smoothing (Fig.

1), performed over 1s is a part of a band-power

calculation. Following this, logarithmic

transformation of TDP parameters was performed to

enforce normal distribution required for classifier

based on linear discriminant analysis (LDA)

(Fukunaga, 1990).

2.3.2 On-line Brain Computer Interface

based on Movement Attempt

During therapy a session, BCI was used on-line with

classifiers to discriminate between a hand movement

and no movement. To improve performance of BCI

on-line LDA classifier, the mean values of both

classes and the within class covariance matrix were

updated during training. The on-line adaptation was

necessary due to small number of off-line trials. Short

off-line training was needed due to a limited time

patients had for the study, which had to fit within their

daily routine (typically 1 hour for BCI setup and for

training of both hands).

The difficulty of activation of BCI was adjustable,

so difficulty can be e.g. increased to reduce the false

positive rate or decreased to make a task easier for a

patients who is tired or has a low concentration. The

difficulty was adjusted by setting the length of EEG

sequence in which a desired class (left or right hand)

had to be successfully detected. A classifier made a

decision based on EEG sequence of length b

(typically b=1.5-2s, while maximum allowed length

B=3s or 768 samples). However, a classifier could

make a decision based on a portion period called f.

NEUROTECHNIX 2015 - International Congress on Neurotechnology, Electronics and Informatics

So if a total sequence for a particular training day is

b=2s, with maximum sequence B=3s and f=75% then

difficulty d is 50%.

5.0

75.02

⋅

(2)

On each therapy session a patient performed 30-

40 MA of each hand, separated in sub-sessions

consisting of 20 trials. Each successfully detected

movement attempt resulted in the activation of FES,

as described below. During therapy sessions, patient

sit in front of a computer screen. They were instructed

to attempt a movement upon the appearance of a

visual cue. A feedback in the form of a gauge was

provided to patients. They were told that during MA,

when the gauge indicator reaches 0, there will be

activation of a set of electrodes attached to their hand

muscles in a predefined order. After each 10 trial sub-

session patients got visual information on the screen

about their performance.

2.3.3 Functional Electrical Stimulation

Functional electrical stimulation was delivered using

a multichannel FES device (Rehastim, Hasomed,

Germany). Four bipolar electrodes were attached over

the wrist and hand/thumb extensor and flexor muscles

to assist patients to perform grasp by opening and

closing their hand. The electrodes were attached to

sequentially stimulate the extensor digitorum,

extensor pollicis longus, flexor digitorum

superficialis and flexor policis brevis. The first two

muscles are extensors and the latter two are flexor

muscles. Stimulation of the first two muscles resulted

in opening of the hand and four fingers (index finger

to pinkie), followed by thumb abduction; subsequent

stimulation of two flexor muscles resulted in closing

of the hand. The whole stimulation sequence lasted

10s. Frequency of stimulation was 26 Hz, pulse width

was 200 µs and the current amplitude varied between

15 mA and 35 mA and was individually chosen for

each patient to produce visible muscle contraction

without discomfort. The same setup was used for both

patient groups. The main difference was that BCI-

FES group had to activate FES by attempting to open

and close hand and for FES group stimulator was

activated automatically in 10s on and 10 off sequence.

3 RESULTS

3.1 Attempted Movement ERD/ERS

Average ERD/ERS scalp maps during MA for both

groups were created for θ, α, β1 (12-16 Hz) and β1

(16-24 Hz) bands. A difference in scalp maps before

and after therapy was calculated for each group.

Largest difference were found for BCI-FES group in

β1 for both hands (Fig 2). Both groups had strong

parietally shifted activity before the therapy. Only in

patients, receiving BCI-FES, following the therapy,

the activity ‘restored’, shifting back to the central

cortical region. The lateralisation of ERD during MA

of the left and right hand can also be noticed in Fig

2a,b, column ‘BCI-FES’, row ‘After’. Red dots in

bottom rows in Fig 2a and b show electrodes, located

Figure 2: Event related synchronisation/ desynchronisation

scalp maps for 12-16 Hz, averaged over t=0.5-2s, during

movement attempt in two patient groups before and after 20

therapy sessions. (a) the right hand and (b) the left hand.

Brain-Computer Interface and Functional Electrical Stimulation for Neurorehabilitation of Hand in Sub-acute Tetraplegic Patients -

Functional and Neurological Outcomes

in the parietal cortex in BCI-FES group, in which

ERD has significantly changed after the therapy.

Previous studies indicate that parietal shift is due to

an injury (Fig 2a.,b, both groups, row ‘Before’) and

that in patients who functionally recover, cortical

activity shifts back towards the central region (Green

et al. 1998), as in able-bodied people. In BCI-FES

group similar trend could be noticed in all other

frequency bands, being also statistically significant

for the left hand in the α band, and for the right hand

in the θ band. No statistically significant changes

(apart from one electrode showed in Fig 2a, bottom

row) were noticed in FES group.

3.2 Somato-sensory Evoked Potential

Seven patients from BCI-FES and four from BCI

were available for this test. Table 2 shows in how

many patients N20 peak was visible in SSEP of the

medial and ulnar nerve. Results in the table are

presented as pre/post therapy.

Table 2: The number of patients who had visible N20 peak

in their SSEP pre/post therapy in both patent groups.

Median Ulnar

left right left right

BCI/FES 4/6 2/5 1/3 1/2

FES 2/2 1/0 1/1 0/0

In all patients in BCI-FES group, who initially had

visible SSEP, the N20 latency was reduced post-

therapy. The average N20 latency over 7 SSEP in

total was 25.0±3.1 ms pre-therapy and 23.5±2.7ms

post-therapy, being an indicator of neurological

recovery. On the contrary, in FES group, N20 latency

slightly increased from 23.5±1.6 ms to 23.9±1.9 ms.

Figure 3 shows an example of N20 pre and post

therapy in patient 1 who received BCI-FES therapy.

Location of the N20 has shifted towards a lower

latency post therapy and the amplitude (peak to peak)

increased.

3.3 The Range of Motion

Five patients from BCI-FES group and three patients

from FES were available for both initial and final

assessment of ROM of the wrist. All patients in both

groups, except patient 11 from FES group, had the

increased range of motion of wrist following the

therapy (Fig 4). Numerical values of ROM before and

after the therapy, expressed as the degrees of an angle,

are shown separately for flexion and extension of the

right hand wrist. An increase in ROM indicates

functional recovery. Due to the small number of

participants it was not possible to perform a statistical

analysis.

4 DISCUSSION

This study demonstrates the application of BCI-FES

as a rehabilitative device for patients with incomplete

tetraplegia. We used BCI based on time domain

parameters with on-line adaptation (Vidaurre et al.

2009), which allowed short off-line training. Patients

who are still in a hospital and receive standard

treatment, have a very limited time for a BCI-FES

therapy (Rupp 2014). BCI algorithms should

therefore have quick electrode setup and should

require minimum (if any) daily offline adjustment of

parameters. We used 6 electrodes for 3 bipolar

recording, that is much smaller than the number of

electrodes used for algorithms based on common

spatial patterns (16-63 electrodes, Fei et al. 2008, Li

et al. 2014) and comparable with the number of

electrodes for algorithms based on time-frequency

parameters in a selected frequency band (2-12

electrodes, Tam et al. 2011, Mukaino et al. 2014,

Young et al. 2014, Vuckovic et al. 2015).

Due to the injury to the spinal cord rather than to

the brain, most research groups consider BCI-FES to

Figure 3: Somato-sensory evoked potential of the left ulnar

nerve (note N20 peaks between 20 and 30 ms) in patient 1.

be an assistive rather than rehabilitative device for

spinal cord injured patients. This paper, however,

compares neurological and functional outcome of two

hand therapies in incomplete sub-acute tetraplegic

patients. A BCI-FES therapy involved active

participation of patients, resulting in the combined

activation of efferent and afferent pathways while

FES therapy involved passive stimulation of muscles.

0 10 20 30 40 50

-4

-2

t/ms

Amplitude(micro volts)

Pre

Post

NEUROTECHNIX 2015 - International Congress on Neurotechnology, Electronics and Informatics

Previous BCI-FES rehabilitation studies on stroke

patients reported increased ERD, from electrode

located over the sensory-motor cortex, following a

therapy (Li et al. 2014, Mukaino et al. 2014). In a

subset of 4 patients included in this study we noticed

the same phenomena (Osuagwu and Vuckovic 2014).

However the novelty of the current study is that we

looked at scalp maps rather than at isolated

electrodes, which enabled us to notice the spatial

restoration of cortical activity. Before the therapy,

both groups had strong, parietal shift of cortical

activity during MA. Following the therapy, only BCI-

FES group, actively involved in the therapy, restored

centrally located cortical activity during MA. This

trend (parietal activity following injury, shifting

towards central region upon recovery) has been

previously reported in patients with spinal cord

injury, where restoration of cortical activity was

related to functional recovery (Green et al. 1998).

This results is in-line with fMRI single case study

(Mukaino et al. 2014) which showed initial diffuse

blood oxygenation level and lateralisation of this

activity following BCI-FES training.

SSEP was not used in BCI-FES studies in stroke

patients because they had injury to the brain. In SCI

patients however, this is a useful additional indicator

of recovery. In BCI-FES patients group, SSEP

following recovery showed re-appearance of N20

peak and reduced latency of the existing peaks.

Though this was primarily noticed in BCI-FES group,

due to the small number of patients, a statistical

comparison between groups was not performed. Curt

and Dietz (1999) showed a relation between the SSEP

of the lower limbs and the recovery of walking which

could be translated to recovery of the upper limbs.

Improvement in ROM was noticed in both groups.

In summary, while BCI-FES therapy results in a

better neurological recovery, the results of functional

recovery are inconclusive, partially due to the small

number of patients being available for the ROM test.

ROM is a functional assessment also used in studies

on stroke patients (Kim et al. 2015). Studies on stroke

patients additionally used Action Research Arm Test

(ARAT) and Fugl Meyer Assessment of Motor

Recovery to demonstrate better functional

improvements in patients receiving BCI-FES (Li et

al. 2014, Kim et al. 2015). SCI patients in the current

study had more severe motor deficit than stroke

patients and were not initially able to perform any of

these task; therefore individual muscle strength was

measured using MMT test. MMT is not a

straightforward measure as each muscle should be

observed individually, and unlike ARAT and FMA

test, results of individual assessments should not be

Figure 4: The range of motion during flexion and extension

of the right hand wrist before and after therapy for each

single patient in both groups.

summed up over the muscles. This made MMT

analysis complex, beyond the scope of this study.

A neurological recovery normally precedes a

functional recovery. Patients in this study received 20

therapy sessions and had the last assessment shortly

after the last therapy session. It is possible that FES

patients would reach the same level of neurological

recovery as BCI-FES patients but after a prolonged

period of time. Alternatively, BCI-FES group might

Brain-Computer Interface and Functional Electrical Stimulation for Neurorehabilitation of Hand in Sub-acute Tetraplegic Patients -

Functional and Neurological Outcomes

have shown long-term larger functional recovery than

FES group due to better neurological recovery. It

would be necessary to follow up patients for a

prolonged period of time (e.g. up to 6 months) to

establish whether those who showed better

neurological recovery would achieve better

functional recovery. Studies on the larger number of

patients are required to establish a clear correlation

between neurological recovery, as measured by the

cortical activity, and functional recovery.

Neurological recovery might potentially prevent

secondary consequences of SCI, such as spasticity

and central neuropathic pain (Pikov, 2002). These

complications are caused by disuse plasticity in the

spinal cord but reflect themselves in the cortical

activity (Wrigley et al. 2009, Vuckovic et al. 2014).

In our recent study, we trained 5 chronic paraplegic

patients with long-standing central neuropathic pain

to voluntary modulate their brain activity over the

sensory-motor cortex (neurofeedback), which

resulted in reduced pain and in some patients in self-

reported reduction of spasticity (Hassan et al. 2015).

In the current study we demonstrated the restoration

of the activity of the sensory-motor cortex as a result

of BCI-FES training. In a long term, this might

prevent secondary consequences of SCI. In the future,

it would be useful having BCI-FES studies with

follow up measures of spasticity and central

neuropathic pain.

5 CONCLUSIONS

The study indicates that BCI-FES therapy of the hand

in sub-acute incomplete tetraplegic patients provides

better neurological recovery than passive FES

therapy. Larger and longer studies are required to

compare functional outcomes of these two therapies

and explore the potential of preventing secondary

complications by early BCI-FES interventions.

ACKNOWLEDGEMENTS

This work has been partially funded by EPSRC PhD

scholarship EP/P505534/1. We would like to thank

Dr Purcell and Dr McLane for their help with

recruiting patients and to all patients for participating

in the study.

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Brain-Computer Interface and Functional Electrical Stimulation for Neurorehabilitation of Hand in Sub-acute Tetraplegic Patients -

Functional and Neurological Outcomes