You are on page 1of 13

Home Search Collections Journals About Contact us My IOPscience

A hybrid BCI based on EEG and fNIRS signals improves the performance of decoding motor

imagery of both force and speed of hand clenching

This content has been downloaded from IOPscience. Please scroll down to see the full text.

2015 J. Neural Eng. 12 036004

(http://iopscience.iop.org/1741-2552/12/3/036004)

View the table of contents for this issue, or go to the journal homepage for more

Download details:

IP Address: 169.230.243.252
This content was downloaded on 07/04/2015 at 02:18

Please note that terms and conditions apply.


Journal of Neural Engineering

J. Neural Eng. 12 (2015) 036004 (12pp) doi:10.1088/1741-2560/12/3/036004

A hybrid BCI based on EEG and fNIRS


signals improves the performance of
decoding motor imagery of both force and
speed of hand clenching
Xuxian Yin1,2,7, Baolei Xu1,7, Changhao Jiang3,7, Yunfa Fu4,7,
Zhidong Wang1,5, Hongyi Li1,6 and Gang Shi1
1
State Key Laboratory of Robotics, Shenyang Institute of Automation (SIA), Chinese Academy of
Sciences (CAS), Shenyang 110016, People’s Republic of China
2
University of Chinese Academy of Sciences, Beijing 100049, People’s Republic of China
3
Key Laboratory of Motor and Brain imaging, Capital Institute of Physical Education, Beijing 100088,
People’s Republic of China
4
School of Automation and Information Engineering, Kunming University of Science and Technology,
Kunming 650500, People’s Republic of China
5
Dept. of Advanced Robotics, Chiba Institute of Technology, Chiba 2750016, Japan
6
School of Mechanical Engineering & Automation, Northeastern University, Shenyang 110004, People’s
Republic of China

E-mail: blxu@sina.cn

Received 28 November 2014, revised 11 January 2015


Accepted for publication 19 February 2015
Published 2 April 2015

Abstract
Objective. In order to increase the number of states classified by a brain–computer interface
(BCI), we utilized a motor imagery task where subjects imagined both force and speed of hand
clenching. Approach. The BCI utilized simultaneously recorded electroencephalographic (EEG)
and functional near-infrared spectroscopy (fNIRS) signals. The time-phase-frequency feature
was extracted from EEG, whereas the HbD [the difference of oxy-hemoglobin (HbO) and deoxy-
hemoglobin (Hb)] feature was used to improve the classification accuracy of fNIRS. The EEG
and fNIRS features were combined and optimized using the joint mutual information (JMI)
feature selection criterion; then the extracted features were classified with the extreme learning
machines (ELMs). Main results. In this study, the averaged classification accuracy of EEG
signals achieved by the time-phase-frequency feature improved by 7%, to 18%, more than the
single-type feature, and improved by 15% more than common spatial pattern (CSP) feature. The
HbD feature of fNIRS signals improved the accuracy by 1%, to 4%, more than Hb, HbO, or HbT
(total hemoglobin). The EEG–fNIRS feature for decoding motor imagery of both force and
speed of hand clenching achieved an accuracy of 89% ± 2%, and improved the accuracy by 1%
to 5% more than the sole EEG or fNIRS feature. Significance. Our novel motor imagery
paradigm improves BCI performance by increasing the number of extracted commands. Both the
time-phase-frequency and the HbD feature improve the classification accuracy of EEG and
fNIRS signals, respectively, and the hybrid EEG–fNIRS technique achieves a higher decoding
accuracy for two-class motor imagery, which may provide the framework for future multi-modal
online BCI systems.

Keywords: EEG-fNIRS, hand clenching force and speed, motor imagery, joint mutual
information (JMI), extreme learning machines (ELMs)
7
These authors contributed equally to the study.

1741-2560/15/036004+12$33.00 1 © 2015 IOP Publishing Ltd Printed in the UK


J. Neural Eng. 12 (2015) 036004 X Yin et al

(Some figures may appear in colour only in the online journal)

1. Introduction study can detect different movement intentions with limited


latencies, but this design is based on actual movement. Yuan
The brain–computer interface (BCI) is a type of technology et al [23] investigated the relationship between hand clench-
that decodes user intentions and directly realizes device ing speed and EEG activity and found that activities in alpha
control using brain signals without the participation of the and beta frequency bands were linearly correlated with the
peripheral nervous system and muscles [1]. First proposed by hand clenching speed. However, it is unknown if hand
Vidal in 1973 [2], BCI has acquired great developments in the clenching force and speed motor imageries can be dis-
past two decades [3–6]. This technology is used for the tinguished. Consequently, this study investigates motor
communication of locked-in patients and neurological reha- parameter imageries associated with both force and speed of
bilitation of stroke patients [7, 8] as well as for the enter- hand clenching. This paradigm is a feasible approach in
tainment of healthy users [9, 10]. In the literature, several generating considerable BCI commands.
techniques have been used to analyze brain activities, The hybrid BCI using the EEG–fNIRS combination can
including electroencephalography (EEG) and functional near- resolve the particular limitations of single modality and
infrared spectroscopy (fNIRS). improve the classification accuracy. Fazli et al [24] demon-
EEG is the most used non-invasive brain signal for BCI strated that the performance of motor imagery-based BCI can
systems because of its high temporal resolution and low cost. be enhanced by combining the measurements of EEG and
Here, the key step to achieve a high decoding accuracy is to fNIRS signals. In the current study, the hybrid EEG and
extract task-relevant features. Many researchers have inves- fNIRS signals are recorded simultaneously and then com-
tigated the features of time, spatial, or frequency domains for bined to improve the classification accuracy of decoding
EEG decoding, such as power spectral, band power, event- motor imagery of both force and speed of hand clenching.
related de-synchronization/synchronization (ERD/ERS), and Results demonstrate that the classification of motor imagery
spatial patterns. However, few studies have focused on phase- of both force and speed of hand clenching is possible, and that
domain features. Lachaux et al [11] introduced phase locking the EEG–fNIRS features can achieve accuracy levels of
value (PLV) as a statistical measure to evaluate the phase 89% ± 2%; further, this method is more accurate compared
synchrony phenomenon between two EEG channels, whereas with that using single-modality features.
Gysels et al [12] proposed that PLV is useful for spontaneous
EEG classification during mental tasks. Moreover, Li et al
[13] compared PLV with the phase interval value (PIV) for 2. Materials and methods
classification of motor imagery for BCI applications, and their
results demonstrated that PIV performed better than PLV. In 2.1. Experiment paradigm
this study, time-, phase-, and frequency-domain features are A paradigm based on motor parameter imagery associated
combined to classify different motor imageries for BCI. with hand clenching force and speed is proposed in this study
Results show that the time -phase-frequency feature can sig- to increase the BCI command number. Unlike paradigms
nificantly improve the classification accuracy. using motor imageries of different limbs, the two different
fNIRS is another promising non-invasive approach for motor imagery tasks in this study come from the same limb
BCI systems since Coyle et al first applied it in BCI research (i.e., the right hand). The hand clenching speed task refers to
in 2004 [14]. This technology measures de-oxyhemoglobin different hand clenching frequencies, such as 0.5, 1, and 2 Hz.
(Hb) and oxyhemoglobin (HbO) concentration changes by Before the experiment, subjects practiced actual movements
shining near-infrared light into the head (with two or more of different hand clenching speed levels using a metronome;
wavelengths) and measuring the diffusively reflected light they were instructed to become familiar with the feeling of
changes that originate from physiological changes in the skin different speed levels. However, during the experiment pro-
and cortex [15–18]. Although fNIRS signals provide an cess, they were requested to perform different hand clenching
approach to investigating user intentions, an inherent time speed levels of motor imageries without actual movement.
delay of hemodynamic response exists. electromyography activity was monitored to exclude those
Most motor imagery-based paradigms currently use unqualified trials. The hand clenching force task refers to the
imagination of different limbs, such as the left and right different hand clenching forces of the right hand (e.g., 20%,
hands, feet, and tongue [19, 20]. The ability to produce 50%, and 80% of the maximum hand clenching force, MF).
multiple control commands, however, may be limited. The MF of the right hand was measured using an electrical
Although combining motor imageries with other mental tasks, dynamometer. Subjects were required to increase the hand
such as word association and mental arithmetic, is one way to clenching force to a target value in 2 s and then maintain the
increase the command number [21], motor parameter imagery force (figure 1). Before the experiment, subjects were per-
offers a more efficient approach to achieve this goal. formed substantial training until they could perform the
Jochumsen et al [22] detected ankle dorsiflexion movement movements appropriately.
intentions associated with different levels of force and speed Six right-handed neurologically healthy volunteers (three
using movement-related cortical potential (MRCP). This males and three females, average age: 26.8 ± 3.3 years)

2
J. Neural Eng. 12 (2015) 036004 X Yin et al

Figure 1. (a) The force transformation during hand clenching force


tasks. Before the experiment, participants perform the training of real
hand clenching. Participants are required to achieve their hand
clenching force to the target value in 2 s and then maintain the force
during the other period. During the experiment, subjects imagine to
achieve clenching without actual movement. (b) The experiment
paradigm used in the research.

participated in the experiment. All participants gave written


informed consent to join the experiment. Among these sub-
jects, subjects 1, 2, and 6 were trained with actual and ima-
gery movements for a total of three times before the
experiment, whereas subjects 3, 4, and 5 were only trained
one time before the experiment. The experiment was
approved by the Ethical Committee of the Shenyang Institute
of Automation, Chinese Academy of Sciences.
To acquire considerable task-relevant brain signals for
decoding motor imageries, the EEG and fNIRS signals were
recorded simultaneously. In consideration of the time lag in
the fNIRS response to cerebral activations [25], the time
duration of a single trial is longer than the time used for
traditional EEG paradigms. A single trial consists of four Figure 2. (a) The locations of EEG electrodes and fNIRS probes
parts, i.e., baseline, cue, task, and rest period [figure 1(b)]. used in the experiment. The red ones are light emitters and the blue
Owing to the inherent delay of hemodynamic response, the ones are light detectors. The locations between the two probe types
task duration was set to 10 s to ensure fNIRS signals reached are the measured channels. The emitter-detector distance is fixed at
30 mm. (b) The actual EEG and fNIRS channel locations in the
the maximum values. The rest period lasted from 10 s to 12 s experiment.
to eliminate the effect of periodic system error and make
fNIRS signals return to base value.

The EEG signals were acquired by Neuroscan Synamps2


2.2. Data acquisition
at a sampling frequency of 1000 Hz, with A1 as the reference
and Fpz as the ground. The electrode impedance was reduced
A total of 21 EEG electrodes and 24 fNIRS channels over the to 5 K ohms before the experiment. The electro-oculogram
primary motor area and the supplementary motor area were (EOG) was also recorded to ensure that no EOG artifact
used in this research [figure 2(a)]. The fNIRS probes con- existed during the motor imagery task period. Meanwhile, the
tained two types, i.e., the light emitters (the red ones) and the fNIRS signals were acquired by ETG-4000 (Hitachi Medical
light detectors (the blue ones). The locations between the Corporation, Japan) at a sampling frequency of 10 Hz. The
emitters and the detectors were set as the measured channels. illuminators emitted near-infrared light at two different
In our research, two 3 × 3 probe sets were used. The EEG wavelengths, i.e., 695 and 830 nm. The triggers were simul-
electrodes were arranged in accordance with the 10–20 taneously sent to Synamps2 and ETG-4000 through parallel
international system, and the fNIRS probe sets were arranged and serial ports. Although the received triggers of the two
in accordance with the C3 and C4 locations of the EEG signal types may present a difference of a few milliseconds,
electrodes. such a difference does not affect the following analysis.

3
J. Neural Eng. 12 (2015) 036004 X Yin et al

Every subject participated in three sessions of the 2.4. Feature extraction


experiment. Every session included 30 trials of the hand
clenching speed motor imagery task and 30 trials of the hand 2.4.1. EEG. In this study, the time-frequency-phase feature
clenching force motor imagery task. Given that the duration is proposed to improve the classification of different motor
of a single trial was longer than that of traditional EEG imageries. Hilbert transform and the complex wavelet
paradigms, the number of trials in one session was corre- convolution are two methods used to obtain the phase
spondingly smaller. information of a signal [11]. These two methods can obtain
similar results [31]. The Hilbert transform method is adopted
in this study.
2.3. Signal preprocessing
The Hilbert transform of a signal x(t) can be obtained by
2.3.1. EEG. In order to reduce the computational cost, the convoluting with the function h(t) = 1/πt using
EEG data were downsampled to 250 Hz, followed by a ∞ ∞
Chebyshve II low-pass filter with five orders at a cutoff y (t ) = P ∫−∞ x (τ ) h (t − τ )dτ = π1 P ∫−∞ tx−(τ )τ dτ, (3)
frequency of 125 Hz to eliminate signal distortion. The data
were then band-pass filtered with a band of 5 to 45 Hz. A where P is the Cauchy principal value. The analytic signal of
small Laplacian filter [26] was used to improve the spatial x(t) can be obtained using equation (2).
resolution of the EEG data. This is expressed by z (t ) = x (t ) + iy (t ) = A (t )eiθ (t ) , (4)
2 2
1 where i is the imaginary unit, A(t) = sqrt(x(t) + y(t) ) is the
Vj Lap = Vj − ∑ Vk , (1)
N k∈S instantaneous amplitude (IA), and θ(t) = arctany(t)/x(t) is the
j
instantaneous phase (IP). The value range of θ(t) is [−π π].
The instantaneous frequency (IF) can be obtained by w(t) = dθ
where Vj is the jth channel, Sj is the surrounding channel set
(t)/d(t). To achieve the correct IF, θ(t) must be unwrapped by
of Vj, N is the size of Sj, and Vk is the kth channel in Sj.
adding multiples of ±2π when absolute jumps of more than π
Previous studies have shown that mu rhythm and beta rhythm
occur between consecutive elements.
are effective for BCI control [27]. Thus, in this study, signals
In this study, four feature types were included, i.e.,
of 8 to 12 Hz and 18 to 25 Hz were extracted for
power, IA, IP, and IF, which were combined together to
classification.
construct the time-phase-frequency feature. The latter three
features can be obtained from Hilbert transform. The
2.3.2. fNIRS. The original fNIRS signals are optical intensity topographies of IP and IF between hand clenching force
signals of two wavelengths. Thus, the concentration changes of and speed imagery are shown in figure 3.
Hb and HbO can be calculated with these optical signals using To decrease the feature dimensions and improve the
the modified Beer–Lambert Law, as shown in equation (2), classification stability, the original features were averaged
where ελ1/λ2,Hb/HbO is the extinction coefficient of Hb/HbO using a 0.5 s moving window with a step width of 0.125 s.
under the corresponding wavelength, Iλ1/λ2(t1/t2) is the After testing four window length and step width combinations
light intensity at times t1 and t2, and DPF is the ratio of (0.5 s to 0.125 s, 0.5 s to 0.2 s, 1 s to 0.125 s, and 1 s to 0.2 s),
the actual path length of the optical photon to the illuminator- we found that the 0.5 s to 0.125 s combination yielded the
detector distance [28]. Values for the differential path best performance. The 0.5 s window length is reasonable in
length factors (DPF695 = 6.51, DPF830 = 5.86) and the consideration of the varied nature of EEG signals, and the
extinction coefficients (ε695, Hb = 1.9665, ε695,HbO = 0.3120, 0.125 s step width is enough for achieving fluent BCI device
ε830,Hb = 0.7804, ε830, HbO = 1.0507) are obtained from control. The averaged feature points between the time range
[29, 30]. of [−0.5 0.5] of all the channels are combined into a vector,
⎛ Iλ1 ( t1) ⎞ and the original size of each feature type is 8 × 21 = 168. To
⎜ log ⎟ eliminate the degradation of the classifier performance caused
⎜ Iλ1 ( t2 ) ⎟
⎜ ⎟ by feature value range variance and obtain a high classifica-
⎛ ΔcHb ⎞ ⎛ ελ1, Hb ελ1, HbO ⎞−1 ⎜ DPFλ1 d ⎟ tion accuracy, each feature vector was normalized to the range
ΔC = ⎜ ⎟=⎜ ⎟
ελ 2, HbO ⎠ ⎜ (2)
⎝ ΔcHbO ⎠ ⎝ ελ 2, Hb Iλ 2 ( t1) ⎟ [−1 1] using equation (5). The four normalized feature vectors
⎜ log ⎟ were then merged into a single vector to construct the time-
⎜ Iλ 2 ( t2 ) ⎟
⎜ DPF d ⎟ phase-frequency feature.
⎝ λ2 ⎠ ⎛ Feature − min(Feature)
Featurenorm = ⎜
The low-frequency drift caused by probe movements in ⎝ max(Feature) − min(Feature)
the concentration data was removed using a linear-detrend − 0.5) × 2, (5)
filter. The concentration data were then low-pass filtered
using a Chebyshev II filter with five orders, at a cutoff
frequency of 0.1 Hz to remove high-frequency artifacts, such 2.4.2. fNIRS. Three types of concentration change signals
as heart and breathing rates. After eliminating the physiolo- are currently used in fNIRS-based BCI applications, i.e., Hb,
gical noise, the data were downsampled to 1 Hz to decrease HbO, and total hemoglobin (HbT, i.e., HbT = Hb + HbO),
feature space dimensionality. along with two optical intensity signals. The signal pattern

4
J. Neural Eng. 12 (2015) 036004 X Yin et al

courses of the four preprocessed fNIRS concentration signals


activated by cognitive tasks are shown in figure 4.
The four concentration signals and two optical intensity
signals of 24 channels from the [0 12] s period were extracted
to construct the feature vectors. The original feature space of
each signal consisted of 12 × 24 = 288 values. The features
extracted from these six signal types were then normalized
using equation (5).

2.5. Feature optimization

The existence of redundant information in the original feature


space can significantly reduce the classification accuracy.
Therefore, feature optimization is essential in improving the
discriminative performance of a classifier. Feature extraction
and feature selection are two typically used feature optimi-
zation methods [34]. Although feature extraction projects the
original feature set to new features on the basis of transfor-
mations (e.g., principal component analysis [35]), feature
selection methods select the best subset of the original feature
set on the basis of some criteria. The disadvantage of the
feature extraction method is that the newly created feature
space is difficult to understand. Hence, the feature selection
method was chosen in our research.
Depending on whether the classifier is included in the
selection process, feature selection methods can be grouped
into ‘wrapper’ and ‘filter’ methods [36]. On the one hand, the
wrapper methods generally consider the classification accu-
Figure 3. (a) The topography of the IP of mu feature between hand racy of the classifier as the feature selection criterion, thus
clenching force and speed imageries. Upper: topography of hand
clenching force imagery. Lower: topography of hand clenching resulting in a high classification rate. However, its general-
speed imagery. (b) The topography of the IF of mu feature between ization capability is poor, and its computational burden is
hand clenching force and speed imageries. extensive. On the other hand, the filter method, based on joint
mutual information (JMI) criterion, has been chosen in this
study, because Brown et al [36] showed that this criterion
HbD, i.e., the difference between HbO and Hb
provides the best tradeoff between accuracy and stability.
concentrations, was also employed in this study [32]. HbO
In order to score the potential usefulness of a feature, the
and Hb concentrations are typically strongly negatively
JMI criterion uses the equation given by
correlated with each other under normal circumstances [33].
In this work, we propose that HbD may amplify the amplitude JJMI ( Xk ) = ∑ I ( Xk X j ; Y ), (6)
of concentration changes due to cognitive tasks. The time Xj ∈ S

Figure 4. The time course of the four preprocessed fNIRS concentration signals activated during hand clenching force tasks.

5
J. Neural Eng. 12 (2015) 036004 X Yin et al

Table 1. Decoding accuracies of different EEG feature types and their combinations.

Subject Power IA IP IF Power-IA-IP-IF


subj1 0.72 ± 0.13 0.72 ± 0.14 0.75 ± 0.07 0.81 ± 0.06 0.89 ± 0.07
subj2 0.73 ± 0.08 0.76 ± 0.07 0.78 ± 0.04 0.81 ± 0.02 0.86 ± 0.01
subj3 0.69 ± 0.05 0.69 ± 0.06 0.80 ± 0.02 0.80 ± 0.05 0.87 ± 0.06
subj4 0.62 ± 0.04 0.70 ± 0.08 0.83 ± 0.06 0.77 ± 0.02 0.88 ± 0.01
subj5 0.73 ± 0.03 0.73 ± 0.02 0.87 ± 0.09 0.82 ± 0.06 0.90 ± 0.07
subj6 0.73 ± 0.03 0.74 ± 0.07 0.82 ± 0.02 0.77 ± 0.06 0.88 ± 0.01
trained 0.73 ± 0.00 0.74 ± 0.01 0.78 ± 0.03 0.79 ± 0.02 0.88 ± 0.01
non-trained 0.68 ± 0.05 0.71 ± 0.02 0.83 ± 0.03 0.79 ± 0.02 0.88 ± 0.01
all 0.70 ± 0.04 0.72 ± 0.02 0.81 ± 0.04 0.79 ± 0.02 0.88 ± 0.01

Where Xk is the feature to evaluate, Xj is the feature that has ⎡ βT⎤ ⎡tT⎤
been selected already, S is the selected feature set, and Y is the ⎢ 1 ⎥ ⎢ 1 ⎥
β=⎢ ⋮ ⎥ and T = ⎢ ⋮ ⎥ .
feature label. This equation stands for the information ⎢ β T⎥ ⎢⎣ tN T ⎥⎦
between a joint random variable XkXj and the targets. The ⎣ N ⎦N × m N ×m
details of the algorithm can be found in [37].
When the input weight wi and the bias bi are given, the
2.6. Classification hidden layer output matrix H can be calculated. The output
weight β can be calculated using the equation given by
In this study, the extreme learning machines (ELMs) were
used to classify between hand clenching force and speed β = H †T, (9)
motor imageries of the right hand. ELMs are types of single-
hidden layer feedforward neural networks (SLFNs) [38], where H+ is the Moore–Penrose generalized inverse of matrix
which can be used for regression and multiclass classifica- H [41].
tions [39]. Unlike other feedforward neural networks that use Liang [42] showed that although the accuracy of ELMs is
gradient-based learning algorithms to tune all the network comparable with that of support vector machines, ELMs
parameters iteratively, ELMs use an analytical approach by require less computational cost and shorter training time.
choosing the input weights randomly and then determining
the output weights of SLFNs. The advantages of ELMs
include extremely fast learning speed, small training error, 3. Results
and good generalization performance. Huang et al [40] rig-
orously proved that the input weights and hidden layer biases
3.1. EEG
of SLFNs with infinitely differentiable activation functions
can be randomly assigned. The classification accuracies between hand clenching force
{
For a training set ℵ = (xi , ti ) xi ∈ R n , ti ∈ R m , i = and speed motor imageries of the right hand are shown in
1, … , N , standard SLFNs with activation function g (x ) and a table 1 and figure 5. When the power, IA, IP, and IF features
hidden node number N are mathematically modeled next are used alone, their decoding accuracies are 0.70 ± 0.04,
N N 0.72 ± 0.02, 0.81 ± 0.04, and 0.79 ± 0.02, respectively. The
∑βi gi ( x j ) = ∑βi g ( wi phase feature (IP feature) and its derivative feature (IF fea-
)
⋅ x j + bi = t j , j = 1, … , N ,
ture) outperform the power and amplitude features. When the
i=1 i=1
four features are used simultaneously, the classification
(7) accuracy can be increased to 0.88 ± 0.01. The CSP method
where wi is the input weight vector that connects the input performs a weighting of the electrodes to maximize the dif-
nodes and ith hidden node, β is the output weight vector that ference between two different motor tasks, and the channel
connects ith hidden node and the output nodes, and bi is the variance of the filtered signal is used for the classification
bias of ith hidden node. [43]. In this study, we find that the averaged classification
Equation (7) can be written in a compact format as accuracy using CSP is 0.73 ± 0.03, which is worse than that of
the time-phase-frequency feature. This result demonstrates
Hβ = T, (8) that using motor parameter imagery for BCI applications is
possible and the time-phase-frequency method outperforms
where the traditional CSP method.
When the power and IA features are used, the average
⎡ g ( w1 ⋅ x1 + b1) ⋯ g ( w1 ⋅ x1 + bN ) ⎤
⎢ ⎥ accuracy for the trained group is better than that for the non-
H=⎢ ⋮ ⋯ ⋮ ⎥ , trained group. However, when the IP and IF features are used,
⎢⎣ g ( w1 ⋅ xN + b1) ⋮ g ( wN ⋅ xN + bN )⎥⎦ the average accuracy for the non-trained group is not worse
N ×N
than that for the trained group. Therefore, the phase feature

6
J. Neural Eng. 12 (2015) 036004 X Yin et al

Figure 5. Decoding accuracies of different EEG feature types and their combinations. (a) Results for every subject; (b) Results for different
groups.

may provide significantly different information compared to The accuracy of the concentration-combined feature is higher
the amplitude feature. than that of the optical-combined feature by 0.03, which
implies that the concentration feature should be chosen
preferentially.
3.2. fNIRS

The decoding accuracies using four concentration fNIRS


3.3. EEG–fNIRS
features and two optical fNIRS features are shown in table 2
and figure 6. It can be seen that figure 6(a) shows that dif- To investigate the performance of the EEG–fNIRS merged
ferent subjects have different feature types. The HbD feature feature, the four normalized EEG features and the four nor-
can acquire the best accuracy compared with other features. malized fNIRS concentration features were combined into
For all subjects, the averaged accuracies of four concentration one feature vector, which was then optimized using the JMI
features (Hb, HbO, HbT, and HbD) are 0.73 ± 0.05, feature selection criterion. The accuracy of the EEG–fNIRS
0.73 ± 0.05, 0.70 ± 0.06, and 0.74 ± 0.05, respectively, indi- merged feature and its comparison with the results of sole
cating that the HbD feature can achieve a higher accuracy. EEG and fNIRS features are shown in table 3 and figure 7,
When the two optical features are used, the decoding respectively. Although the accuracy of the merged feature can
accuracies are 0.70 ± 0.05 and 0.70 ± 0.06, respectively, only be increased by 0.01 for the average of all the subjects,
which are lower than those of the four concentration features. the accuracy is increased by 0.03 for subject 5 and by 0.05 for

7
J. Neural Eng. 12 (2015) 036004
Table 2. Decoding accuracies of different fNIRS signal types and their combinations.

Subject Hb HbO HbT HbD Lam1 Lam2 Lam1-lam2 Hb-HbO-HbT Hb-HbO-HbT-HbD


subj1 0.76 ± 0.05 0.80 ± 0.09 0.79 ± 0.03 0.76 ± 0.01 0.77 ± 0.08 0.76 ± 0.01 0.79 ± 0.02 0.82 ± 0.06 0.80 ± 0.06
subj2 0.74 ± 0.08 0.77 ± 0.06 0.78 ± 0.02 0.78 ± 0.00 0.74 ± 0.06 0.76 ± 0.07 0.80 ± 0.06 0.77 ± 0.02 0.79 ± 0.04
subj3 0.64 ± 0.02 0.68 ± 0.02 0.63 ± 0.01 0.69 ± 0.01 0.62 ± 0.03 0.60 ± 0.02 0.67 ± 0.07 0.69 ± 0.01 0.69 ± 0.07
subj4 0.69 ± 0.08 0.68 ± 0.03 0.67 ± 0.04 0.67 ± 0.03 0.66 ± 0.08 0.68 ± 0.03 0.67 ± 0.04 0.67 ± 0.05 0.70 ± 0.05
subj5 0.75 ± 0.00 0.69 ± 0.07 0.68 ± 0.03 0.72 ± 0.02 0.72 ± 0.05 0.71 ± 0.06 0.75 ± 0.04 0.77 ± 0.04 0.76 ± 0.04
8

subj6 0.77 ± 0.05 0.79 ± 0.09 0.68 ± 0.06 0.79 ± 0.06 0.67 ± 0.02 0.67 ± 0.09 0.71 ± 0.05 0.77 ± 0.04 0.79 ± 0.03
trained 0.76 ± 0.01 0.78 ± 0.01 0.75 ± 0.05 0.78 ± 0.01 0.73 ± 0.04 0.73 ± 0.04 0.77 ± 0.04 0.79 ± 0.02 0.79 ± 0.00
non-trained 0.69 ± 0.05 0.68 ± 0.01 0.66 ± 0.02 0.69 ± 0.02 0.67 ± 0.04 0.66 ± 0.05 0.69 ± 0.04 0.71 ± 0.04 0.72 ± 0.03
all 0.73 ± 0.05 0.73 ± 0.05 0.70 ± 0.06 0.74 ± 0.05 0.70 ± 0.05 0.70 ± 0.06 0.73 ± 0.05 0.75 ± 0.05 0.76 ± 0.05

X Yin et al
J. Neural Eng. 12 (2015) 036004 X Yin et al

Figure 6. Decoding accuracies of different fNIRS signal types and their combinations. (a) Results for every subject; (b) Results for different
groups.

subject 6. Hence, the EEG and fNIRS features can supple- amplitude aspect, such as band power, ERD/ERS, and CSP.
ment each other and improve the classification of different In this study, IP feature and its derivative feature (IF) were
motor imagery tasks. compared with the amplitude feature and its square feature
(power feature). The results show that when used alone, the
phase feature outperforms the amplitude feature by approxi-
mately 10% for the average of all the subjects. When the
4. Discussion amplitude and phase features are used simultaneously, the
classification accuracy between hand clenching force and
4.1. Classification of sole EEG speed motor imageries can be improved to 88% for both
Amplitude and phase are two aspects of a signal. Most fea- trained and non-trained groups. The classification accuracy of
tures used in EEG-based BCI applications are focused on the time-phase-frequency also outperforms the results using CSP

9
J. Neural Eng. 12 (2015) 036004 X Yin et al

Table 3. Decoding accuracies of fNIRS, EEG, and fNIRS-EEG by 15%. The time-phase-frequency feature proposed in the
features. current study can also be extended to time-spatial-phase-fre-
Hb-HbO-HbT- quency feature by adopting the CSP method.
Hb-HbO- Power-IA- HbD-&-power-
Subject HbT-HbD IP-IF IA-IP-IF
4.2. Classification of sole fNIRS
subj1 0.80 ± 0.06 0.89 ± 0.07 0.89 ± 0.02
subj2 0.79 ± 0.04 0.86 ± 0.01 0.87 ± 0.02 fNIRS is a new measurement method that can be used for BCI
subj3 0.69 ± 0.07 0.87 ± 0.06 0.87 ± 0.03 applications. Both concentration features and optical features
subj4 0.70 ± 0.05 0.88 ± 0.01 0.88 ± 0.01 were used in current research. After comparing the two fea-
subj5 0.76 ± 0.04 0.90 ± 0.07 0.93 ± 0.03 ture types, the results demonstrate that the concentration
subj6 0.79 ± 0.03 0.88 ± 0.01 0.92 ± 0.03
signal outperforms the optical signal, implying that the con-
trained 0.79 ± 0.00 0.88 ± 0.01 0.89 ± 0.02
centration signal is more effective in reflecting brain activa-
non-trained 0.72 ± 0.03 0.88 ± 0.01 0.89 ± 0.03
all 0.76 ± 0.05 0.88 ± 0.01 0.89 ± 0.02 tions than optical signals. Moreover, compared with the Hb,
HbO, and HbT features, the HbD feature can obtain the best

Figure 7. Decoding accuracies of fNIRS, EEG, and fNIRS-EEG merged feature. (a) Results for every subject; (b) Results for different
groups.

10
J. Neural Eng. 12 (2015) 036004 X Yin et al

results when used alone. Finally, although the average accu- sub-classes, we only separated hand clenching force from
racy of the Hb-HbO-HbT-HbD feature combination outper- speed motor imagery. In future work, we will identify dif-
forms that of the Hb-HbO-HbT feature combination by only ferent levels of hand clenching force and speed motor
1%, the HbD feature provides new information for cerebral imageries.
activations. In conclusion, the paradigm of hand clenching force and
speed motor imageries proposed in this study is feasible in
increasing control command numbers for BCI applications.
4.3. Classification of EEG–fNIRS
Furthermore, the EEG–fNIRS merged feature can better
The results in this paper show that when the EEG–fNIRS improve classification accuracy compared with the single-
merged feature is used, the decoding accuracy can be signal type approach.
improved by 1% to 5%. The best accuracy using the merged
feature is 93% ± 3% for subject 5, which is high enough,
considering that only one hand is used in the experiment. The Acknowledgments
merged feature outperforms the sole EEG feature and the sole
fNIRS feature. Although the classifier-level merged method This work is supported by the National Natural Science
has been widely used in previous studies [24], the feature- Foundation (NNSF) of China under Grant Nos. 61203368,
level merged method is more fundamental in improving 81470084, and 61463024, and by the National High Tech-
classification performance. Furthermore, the optimized fea- nology Research and Development Program of China (863
tures offer cognitive neuroscience experts a convenient way Program) under Grant No. 2012AA02A605.
of explaining the neuromechanism behind the optimized
features.
EEG presents the neural electrical activity during brain References
activation, whereas fNIRS measures hemoglobin oxygenation
information. There are three reasons why the EEG–fNIRS
merged features can achieve better performance than sole [1] Wolpaw J R, Birbaumer N, Mcfarland D J, Pfurtscheller G and
Vaughan T M 2002 Brain-computer interfaces for
EEG and sole fNIRS. First, when EEG and fNIRS are used communication and control Clinical Neurophysiology 113
simultaneously, more task-relevant information content can 767–91
be enhanced about the motor imagery state of the subject. [2] Vidal J 1973 Toward direct brain-computer communication
Second, these two techniques can complement each other in Ann. Rev. Biophys. Bioeng. 2 157–80
presenting cortex activation during motor imagery. Finally, [3] Scherer R and Pfurtscheller G 2013 Thought-based interaction
with the physical world Trends Cogn. Sci. 17 490–2
feature optimization can also extract the most relevant fea- [4] Ortiz-Rosario A and Adeli H 2013 Brain-computer interface
tures, which can separate hand clenching force and speed technologies: from signal to action Rev. Neuroscience 24
motor imageries. 537–52
[5] Kubler A, Holz E and Botrel L 2013 Brain-computer
interfacing: science fiction has come true Brain 136 2001–4
4.4. Limitations of the study [6] Donoghue J P 2008 Bridging the brain to the world: a
perspective on neural interface systems Neuron 60 511–21
In our study, we used only a single-distance fNIRS approach, [7] De Massari D, Ruf C A, Furdea A, Matuz T,
and the hemodynamic responses caused by skin blood flow Van Der Heiden L, Halder S, Silvoni S and Birbaumer N
may be present [44–48]. Although a Chebyshev II infinite 2013 Brain communication in the locked-in state Brain 136
impulse response filter at a cutoff frequency of 0.1 Hz was 1989–2000
[8] Sun H Y, Xiang Y and Yang M D 2011 Neurological
used to reduce physiological noise, the systemic interference rehabilitation of stroke patients via motor imaginary-based
may inevitably be present in fNIRS measurements. It is brain-computer interface technology Neural Regen. Res. 6
possible that changes in respiration that cause changes of CO2 2198–202
values in the blood also affect the measured signals [49]. [9] Marshall D, Coyle D, Wilson S and Callaghan M 2013 Games,
However, our objective was to distinguish two motor ima- gameplay, and BCI: the state of the art IEEE T. Comput. Int.
Ai Games 5 82–99
geries and extract considerable useful patterns to improve [10] Bonnet L, Lotte F and Lecuyer A 2013 Two brains, one game:
accuracy, and not to understand the neural mechanisms of design and evaluation of a multiuser BCI video game based
functional brain activity. Our future work will thus examine a on motor imagery IEEE T. Comput. Int. Ai Games 5 185–98
two-detector approach to eliminating the systemic inter- [11] Lachaux J-P, Rodriguez E, Martinerie J and Varela F J 1999
ference and checking whether this approach can significantly Measuring phase synchrony in brain signals Human Brain
Mapping 8 194–208
improve classification accuracy. [12] Gysels E and Celka P 2004 Phase synchronization for the
In addition, the hand clenching force and speed motor recognition of mental tasks in a brain-computer interface
imageries in this study both come from the same right hand. IEEE T. Neur. Sys. Reh. 12 406–15
The results show that when the EEG–fNIRS feature is used, [13] Li J I E and Zhang L 2009 Phase interval value analysis for the
the classification of these two motor imageries reaches 89%. motor imagery task in BCI J.Circuit Sys. Comp. 18 1441–52
[14] Coyle S, Ward T, Markham C and Mcdarby G 2004 On the
The usage of motor parameter imageries in BCI applications suitability of near-infrared (NIR) systems for next-
is, therefore, feasible. Although the hand clenching force generation brain–computer interfaces Phys. Measure. 25
motor imagery and speed motor imagery both contain three 815–22

11
J. Neural Eng. 12 (2015) 036004 X Yin et al

[15] Jobsis F F 1977 Noninvasive, infrared monitoring of cerebral [33] Cui X, Bray S and Reiss A L 2010 Functional near infrared
and myocardial oxygen sufficiency and circulatory spectroscopy (NIRS) signal improvement based on negative
parameters Science 198 1264–7 correlation between oxygenated and deoxygenated
[16] Hoshi Y 2005 Functional near-infrared spectroscopy: potential hemoglobin dynamics NeuroImage 49 3039–46
and limitations in neuroimaging studies Int. Rev. Neurobiol. [34] Jain A K, Duin R P W and Mao J C 2000 Statistical pattern
66 237–66 recognition: a review IEEE T. Pattern Analysis Machine Int.
[17] Hoshi Y 2007 Functional near-infrared spectroscopy: current 22 4–37
status and future prospects J. Biomed. Opt. 12 062106 [35] Yu X, Chum P and Sim K B 2014 Analysis the effect of PCA
[18] Scholkmann F, Kleiser S, Metz A J, Zimmermann R, for feature reduction in non-stationary EEG based motor
Mata Pavia J, Wolf U and Wolf M 2014 A review on imagery of BCI system Optik 125 1498–502
continuous wave functional near-infrared spectroscopy and [36] Brown G, Pocock A, Zhao M-J and Luján M 2012 Conditional
imaging instrumentation and methodology Neuroimage 85 likelihood maximisation: a unifying framework for
6–27 information theoretic feature selection J. Machine Learn.
[19] Sano A and Bakardjian H 2009 Movement-related cortical Res. 13 27–66
evoked potentials using four-limb imagery Int. J. Neurosci. [37] Meyer P E, Schretter C and Bontempi G 2008 Information-
119 639–63 theoretic feature selection in microarray data using variable
[20] Hashimoto Y and Ushiba J 2013 EEG-based classification of complementarity IEEE J. Sel. Topics Signal Proces. 2
imaginary left and right foot movements using beta rebound 261–74
Clinical Neurophysiology 124 2153–60 [38] Huang G B, Zhu Q Y and Siew C K and Ieee 2004 Extreme
[21] Friedrich E V C, Scherer R and Neuper C 2013 Long-term learning machine: A new learning scheme of feedforward
evaluation of a 4-class imagery-based brain-computer neural networks IEEE Int. Joint Conf. Neural Networks
interface Clin. Neurophys. 124 916–27 (New York) (IEEE)
[22] Jochumsen M, Niazi I K, Mrachacz-Kersting N, Farina D and [39] Huang G-B, Zhou H, Ding X and Zhang R 2012 Extreme
Dremstrup K 2013 Detection and classification of learning machine for regression and multiclass classification
movement-related cortical potentials associated with task IEEE Transactions on Systems, Man, and Cybernetics—Part
force and speed J. Neural Eng. 10 056015 B: Cybernetics 42 513–29
[23] Yuan H, Perdoni C and He B 2010 Relationship between speed [40] Huang G B, Zhu Q Y and Siew C K 2006 Extreme learning
and EEG activity during imagined and executed hand machine: Theory and applications Neurocomputing 70
movements J. Neural Eng. 7 026001 489–501
[24] Fazli S, Mehnert J, Steinbrink J, Curio G, Villringer A, [41] Rao C R and Mitra S K 1972 Generalized inverse of a matrix
Muller K R and Blankertz B 2012 Enhanced performance by and its applications Proc. of the Sixth Berkeley Symp. on
a hybrid NIRS-EEG brain computer interface Neuroimage Mathematical Statistics and Probability Volume 1: Theory
59 519–29 of Statistics (Berkeley, CA) (University of California Press)
[25] Matthews F and Pearlmutter B A 2008 Hemodynamics for [42] Liang N Y, Saratchandran P, Huang G B and Sundararajan N
brain-computer interfaces IEEE Signal Proces. Mag. 25 2006 Classification of mental tasks from EEG signals using
87–94 extreme learning machine Int. J. Neural Sys. 16 29–38
[26] Mcfarland D J, Mccane L M, David S V and Wolpaw J R 1997 [43] Ramoser H, Muller-Gerking J and Pfurtscheller G 2000
Spatial filter selection for EEG-based communication Optimal spatial filtering of single trial EEG during imagined
Electroen. Clin. Neuro. 103 386–94 hand movement Reh. Eng., IEEE T. 8 441–6
[27] Mcfarland D J, Miner L A, Vaughan T M and Wolpaw J R [44] Erdoğan S B, Yücel M A and Akın A 2014 Analysis of task-
2000 Mu and beta rhythm topographies during motor evoked systemic interference in fNIRS measurements:
imagery and actual movements Brain Top. 12 177–86 insights from fMRI NeuroImage 87 490–504
[28] Delpy D T, Cope M, Van Der Zee P, Arridge S, Wray S and [45] Gagnon L, Yücel M A, Boas D A and Cooper R J 2013 Further
Wyatt J 1988 Estimation of optical pathlength through tissue improvement in reducing superficial contamination in NIRS
from direct time of flight measurement Phys. Med. Biol. 33 using double short separation measurements NeuroImage 85
1433–42 127–35
[29] Cope M 1991 The development of a near infrared spectroscopy [46] Kirilina E, Jelzow A, Heine A, Niessing M, Wabnitz H,
system and its application for non invasive monitoring of Brühl R, Ittermann B, Jacobs A M and Tachtsidis I 2012 The
cerebral blood and tissue oxygenation in the newborn infants physiological origin of task-evoked systemic artefacts in
PhD dissertation Department of Medical Physics and functional near infrared spectroscopy Neuroimage 61 70–81
Biology, University College London, UK [47] Tachtsidis I, Leung T S, Chopra A, Koh P H, Reid C B and
[30] Duncan A, Meek J H, Clemence M, Elwell C E, Tyszczuk L, Elwell C E 2009 False Positives in Functional Nearinfrared
Cope M and Delpy D T 1995 Optical pathlength Topography, in Oxygen Transport to Tissue XXX (New
measurements on adult head, calf and forearm and the head York: Springer) p 307–14
of the newborn infant using phase resolved optical [48] Takahashi T, Takikawa Y, Kawagoe R, Shibuya S,
spectroscopy Phys. Medicine Bio. 40 295–304 Iwano T and Kitazawa S 2011 Influence of skin blood flow
[31] Le Van Quyen M, Foucher J, Lachaux J, Rodriguez E, Lutz A, on near-infrared spectroscopy signals measured on the
Martinerie J and Varela F J 2001 Comparison of Hilbert forehead during a verbal fluency task Neuroimage 57
transform and wavelet methods for the analysis of neuronal 991–1002
synchrony J. Neuroscience Meth. 111 83–98 [49] Scholkmann F, Gerber U, Wolf M and Wolf U 2013 End-tidal
[32] Yoshino K and Kato T 2012 Vector-based phase classification CO2: an important parameter for a correct interpretation in
of initial dips during word listening using near-infrared functional brain studies using speech tasks Neuroimage 66
spectroscopy Neuroreport 23 947–51 71–9

12

You might also like