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Biomedical Signal Processing and Control 7 (2012) 104–111

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Biomedical Signal Processing and Control


journal homepage: www.elsevier.com/locate/bspc

LASSO based stimulus frequency recognition model for SSVEP BCIs


Yu Zhang, Jing Jin, Xiangyun Qing, Bei Wang, Xingyu Wang ∗
Key Laboratory of Advanced Control and Optimization for Chemical Processes, Ministry of Education, School of Information Science and Engineering,
East China University of Science and Technology, Shanghai 200237, PR China

a r t i c l e i n f o a b s t r a c t

Article history: Steady-state visual evoked potential (SSVEP) has been increasingly used for the study of brain–computer
Received 31 August 2010 interface (BCI). How to recognize SSVEP with shorter time and lower error rate is one of the key points
Received in revised form 5 January 2011 to develop a more efficient SSVEP-based BCI. To achieve this goal, we make use of the sparsity constraint
Accepted 7 February 2011
of the least absolute shrinkage and selection operator (LASSO) for the extraction of more discriminative
Available online 5 March 2011
features of SSVEP, and then we propose a LASSO model using the linear regression between electroen-
cephalogram (EEG) recordings and the standard square-wave signals of different frequencies to recognize
Keywords:
SSVEP without the training stage. In this study, we verified the proposed LASSO model offline with the EEG
Brain–computer interfaces (BCIs)
Electroencephalogram (EEG)
data of nine healthy subjects in contrast to canonical correlation analysis (CCA). In the experiment, when a
Least absolute shrinkage and selection shorter time window was used, we found that the LASSO model yielded better performance in extracting
operator (LASSO) robust and detectable features of SSVEP, and the information transfer rate obtained by the LASSO model
Steady-state visual evoked potential was significantly higher than that of the CCA. Our proposed method can assist to reduce the recording
(SSVEP) time without sacrificing the classification accuracy and is promising for a high-speed SSVEP-based BCI.
Time window (TW) © 2011 Elsevier Ltd. All rights reserved.

1. Introduction is estimated typically by the fast Fourier transform (FFT) from the
EEG signal within a time window (TW) [9–12]. The frequency cor-
Steady-state visual evoked potential (SSVEP) may be elicited responding to the peak of PSD is considered as the target stimulus
over occipital scalp areas with the same frequency as the stim- frequency. When using the PSDA, the length of TW required in
ulus and may often include its harmonics when a subject pays SSVEP-based BCIs is typically more than 3 s [13–15], and such dura-
attention to a repetitively flickering stimulus [1,2]. In recent years, tion may limit the real-time speed of SSVEP-based BCIs. Wu et al.
SSVEP-based brain–computer interfaces (BCIs) have been increas- [16] proposed the stability coefficient (SC) method to recognize
ingly studied and have demonstrated strength including a higher SSVEP, and the SC was shown to be better than the PSDA in using
information transfer rate (ITR) and less training to both the system a shorter TW with the cost of training data to form the SC model.
and the user than other BCIs (e.g. P300-based BCIs, event-related Lin et al. [5] used canonical correlation analysis (CCA) to recog-
desynchronization/synchronization (ERD/ERS)-based BCIs) [3–6]. nize SSVEP. Bin et al. [3] developed an online SSVEP-based BCI
SSVEP-based BCIs typically depend on external visual stimuli in system by the CCA with 2 s TW. The CCA can improve the speed
the form of an array of light sources, where each light source flick- of a SSVEP-based BCI in contrast to the PSDA. Indeed, a high-speed
ers with a distinct frequency [1,2,4,7]. The outstanding property SSVEP-based BCI does require a shorter TW, and hence this study is
of SSVEP is that the frequency components of the target stimu- devoted to achieving this goal through developing an algorithm to
lus focused by a subject significantly present in the EEG spectrum, extract more discriminative features from EEG recordings within a
and hence the target stimulus can be inferred by classifying the shorter TW (i.e. using fewer samples).
frequency components of recorded EEG [2,8,10]. When fewer samples are available, the sparse signal processing
In order to obtain faster speed of a SSVEP-based BCI, one option plays an important role [17]. Sparsity analysis has been proved to be
is to recognize the target stimulus frequency accurately within very useful in blind signal reconstruction [18–20], image and signal
shorter time, and then in this case, a better algorithm to recog- detection [21,22]. Recently, the robustness of sparsity constraint
nize frequencies of EEG signal should be provided. The traditional has been exhibited to occlusion and corruption in face recognition
frequency recognition method in SSVEP-based BCIs is power spec- [23,24]. As a popular model selection and shrinkage estimation
tral density analysis (PSDA) and the power spectral density (PSD) method, least absolute shrinkage and selection operator (LASSO)
proposed by Tibshirani [25] can provide an analytical solution and a
low-variance estimate with high interpretability for a linear regres-
∗ Corresponding author. Tel.: +86 021 64253386; fax: +86 021 64253386. sion due to its sparsity constraint [26,27]. In this study, we attempt
E-mail address: xywang@ecust.edu.cn (X. Wang). to make use of the sparsity constraint of the LASSO to extract more

1746-8094/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.bspc.2011.02.002
Y. Zhang et al. / Biomedical Signal Processing and Control 7 (2012) 104–111 105

Fig. 1. Experimental images and layout. The colors of the four flickering squares in the second row are red in the experiment.

discriminative features of SSVEP from a shorter TW. We propose a 2.4. EEG recordings
LASSO model using the linear regression between EEG recordings
and the standard square-wave signals of different frequencies to EEG signals were recorded at 250 Hz sampling rate from three
recognize SSVEP without the training stage. To validate the pro- channels O1, Oz, O2 which were placed on the standard posi-
posed LASSO model, the CCA is used for comparison with the EEG tions of the 10–20 international system and each channel was
data collected from nine healthy subjects, and information trans- amplified by A Nuamps (NuAmp, Neuroscan, Inc.) amplifier with
fer rate (ITR) [28–30] is calculated to evaluate the communication a sensitivity of 100 ␮V. The average of two mastoid electrodes (A1,
performance. A2) was used as reference and the ground electrode was placed
on the forehead. The EEG signals were bandpass filtered between
2. Experiments 5 and 35 Hz.

2.1. Subjects 3. Methods

Nine healthy right-handed volunteers (S1–S9, aged from 21 to 3.1. SSVEP frequency recognition model based on LASSO estimate
28 years, seven males and two females) participated in our exper-
iment. All of them had normal or corrected to normal vision and 3.1.1. LASSO estimate
no experience with a SSVEP-based BCI. The subjects were seated Consider a standard linear regression model for the observations
in a comfortable chair 50 cm from a standard 17 inch CRT moni- of the response y ∈ Rn [26,31]:
tor (85 Hz refresh rate, 1024 × 768 screen resolution) in a shielded
y = Xˇ + ε, (1)
room.
where y is a n × 1 vector, X = (x1 , x2 , . . ., xp ) denotes a n × p design
2.2. Stimulation unit and experimental layout matrix, and ε represents a noise vector with the zero mean and
constant variance. As introduced in [25], the LASSO estimate is then
The command icons, stimuli and the layout used in this study given by:
are presented in Fig. 1. The first row in Fig. 1 shows four command     
ˆ = arg min
ˇ y − Xˇ2 + ˇ , (2)
icons (‘Volume ON’, ‘Volume +’, ‘Volume −’, ‘Volume OFF’). The fre- 2 1
ˇ
quencies of the four flickering squares in the second row were ‘f1 :
6.1 Hz, f2 : 7.1 Hz, f3 : 8.5 Hz, f4 : 10.6 Hz’ corresponding to the four where || · ||1 , || · ||2 denote the l1 -norm and l2 -norm respectively.
commands, respectively. These four commands could be used to  is a penalty parameter which encourages a sparse solution ˇ ˆ
adjust the volume of a device. (i.e. it has many entries equal to zero). The optimization problem
depicted by Eq. (2) can be solved by quadratic programming [32].
2.3. Experimental schedule

Each subject completed six runs with 10 min rest after each run.
Each run consisted of four parts, and one part was for one of the
four command icons. In each part, a cued target icon was presented
in the middle of the blank screen for 1 s, and then the four squares
appeared and flickered simultaneously. The subject was required
to focus on the flickering square corresponding to the cued target
icon for 4 s. Hence, 24 (i.e. 6 × 4) segments of 4 s EEG data were
acquired from each subject. Fig. 2 shows the timing of each part. Fig. 2. The timing of each part.
106 Y. Zhang et al. / Biomedical Signal Processing and Control 7 (2012) 104–111

The LASSO estimate usually offers an analytical solution and a low- between a and b, by solving the following optimization problem:
variance estimate with high interpretability for a linear regression
E[aT b] E[W Ta ABT W b ]
[26,27]. max (a, b) = =
W a ,W b
E[aT a]E[bT b] E[W Ta AAT W a ]E[W Tb BBT W b ]
3.1.2. Frequency components recognition model (6)
To construct the SSVEP recognition model, we assume that X
is a standard signal set consisting of four symmetric square-wave
signals which correspond to the four stimulus frequencies respec- The maximum of  is the maximum canonical correlation. Lin
tively. The symmetric square-wave signal can be decomposed into et al. [5] used the CCA to recognize stimulus frequency in SSVEP
the Fourier series of its harmonics [3,5]: BCI for the first time. They reported that the CCA was better than
⎛ ⎞T the PSDA using multiple channels. Also, an online SSVEP BCI based
sin(2(fi )t) on the CCA was developed by Bin et al. [3]. As introduced in
⎜ cos(2(fi )t) ⎟ [3,5], A contains multi-channel (O1, Oz, O2) EEG signals, and Bi = Si
⎜ ⎟ 1 2 n
Si = ⎜ ⎟ , (i = 1, 2, 3, 4). Then, the canonical correlation coefficient i reflect-
..
⎜ . ⎟ t= , ,..., , (3)
F F F ing the correlation between the ith stimulus frequency fi and the
⎝ sin(2(Kf )t) ⎠
i EEG signals was computed through Eq. (6). The fundamental fre-
cos(2(Kfi )t) quency and second harmonic were still used for the CCA. In order
where Si (i = 1, 2, 3, 4) are the four symmetric square-wave sig- to be consistent with the work of Lin et al. [5], only the maxi-
nals, fi (i = 1, 2, 3, 4) denotes ith stimulus frequency (fundamental mum correlation coefficient was used as the classification basis.
frequency), K is the number of harmonics, F is the sampling rate, Then, the target stimulus frequency ftarget could be recognized
n represents the number of sampling points and the superscript by Eq. (7).
T denotes the transpose transform. In this study, the fundamental ftarget = max(1 , 2 , 3 , 4 ) (7)
frequency and second harmonic components are used to analyze fi
the SSVEP, hence N equals to 2. Then, X = [S 1 , S 2 , S 3 , S 4 ]n×16 . Sup-
pose the vector y derived from the LASSO estimate contains the EEG 3.3. Information transfer evaluation
data within a TW at one channel. In this study, the length of a TW
was set to be from 0.5 to 4 s with the interval of 0.5 s. The LASSO In this study, information transfer rate (ITR) [28–30] was
estimator ˇ ˆ between the EEG signal y and the standard signal set adopted to evaluate the communication speed of our BCI. If N pos-
X can be computed from Eq. (2) by the quadratic programming sible choices exist in one trial, if each choice is of the identical
[32]. Here, ˇ ˆ = [ˇ1,1 , ˇ1,2 , ˇ1,3 , ˇ1,4 , . . . , ˇ4,1 , ˇ4,2 , ˇ4,3 , ˇ4,4 ]T in probability to be selected by the user, if the probability (P) that
which the entries ˇi,1 , ˇi,2 , ˇi,3 , and ˇi,4 (i = 1, 2, 3, 4) imply the the desired selection will indeed be chosen always keeps invariant,
contribution degree (CD) of the ith stimulus frequency fi and its and if each of the other (i.e. undesired) choices has the same prob-
harmonic to the EEG signal. Since ˇ ˆ is sparse to some extent (i.e. ability of selection, the bit rate or bits/trial (Br) can be computed
ˆ as:
most entries in ˇ equal to zero), the CDs of different stimulus fre- 1−P 
quencies in the standard signal set X to the EEG signal y can be Br = log2 N + P × log2 P + (1 − P) × log2 (8)
classified. N−1
The synthetical measurement for the CDs of different stimulus Then, the ITR (bits/min) is equal to Br multiplied by the selection
frequencies at used channels is defined as: speed (i.e. trials per minute).
M 2K k
k=1 j=1
|ˇi,j |
CDi = (4) 4. Results
M
in which M is the number of used channels which are O1, Oz 4.1. Classification accuracy
and O2 here, K represents the number of harmonics (K = 2) and
CDi denotes the contribution degree of ith square-wave signal Fig. 4 describes the classification accuracy of the LASSO model
Si (i.e. ith stimulus frequency fi ) to the EEG signals at the three and the CCA for all subjects. From the averaged accuracy, there was
channels. The maximal CDi implies the dominant frequency com- no evident difference between accuracies of the two methods when
ponent in the EEG signals. Thus, the target stimulus frequency ftarget the length of TW was more than 2.5 s. However, the classification
can be recognized by Eq. (5). The detailed explanation of LASSO accuracy of the LASSO model was obviously higher than that of the
model for recognizing SSVEP frequency components is illustrated CCA when the length of TW was less than 2.5 s. That is, the LASSO
in Fig. 3. model is better than the CCA for SSVEP frequency recognition in
using a short TW less than 2.5 s.
ftarget = max(CD1 , CD2 , CD3 , CD4 ) (5)
fi The Bonferroni corrected t-test was used to analyze the perfor-
mance of LASSO model and CCA. Table 1 exhibits the p value of the
3.2. Comparison method classification accuracy differences between each two TW lengths
for each method. For the LASSO model, the classification accuracies
In our study, we also implemented canonical correlation analy- were not significantly different (see Table 1). For the CCA, when the
sis (CCA) and compared the results with that of our proposed LASSO TW lengths were less than 2 s, the classification accuracies were
model. CCA is a well-known multivariable method developed by significantly different from each other. This result means that the
Hotelling [33] in statistics. CCA extends ordinary correlation to two LASSO model was more robust than the CCA when using a shorter
sets of variables [34] and is widely used in several fields, such as TW less than 2 s.
functional magnetic resonance imaging (fMRI) [35], and climate
research [36]. Consider two multidimensional random variables A, 4.2. Information transfer rate
B and their linear combinations a = AT Wa and b = BT Wb respectively.
A canonical correlation coefficient  is then computed through find- The highest information transfer rate (ITR) with the corre-
ing the weight vectors Wa and Wb which maximize the correlation sponding classification accuracy and TW duration was also used
Y. Zhang et al. / Biomedical Signal Processing and Control 7 (2012) 104–111 107

i
Fig. 3. Explanation of the LASSO model for recognizing SSVEP frequency components. yi denotes the EEG signals with t seconds length of time window from ith channel. ˇ ˆ is
the LASSO estimator corresponding to yi . CDi denotes the contribution degree of ith square-wave signal (i.e. ith stimulus frequency fi ) to the EEG signals from three channels
(O1, Oz, O2).

Fig. 4. Classification accuracy obtained by the LASSO model and the CCA, across different time window (TW) lengths, for all nine subjects and the averaged accuracy.

to evaluate the performance of the LASSO model and the CCA (see 4.3. Classification features
Table 2). The corresponding classification accuracy difference was
not significant between the LASSO model and the CCA (p = 0.64) Fig. 5 displays the features of different target frequencies
while the highest ITR of the LASSO model was significantly higher obtained by the LASSO model (contribution degree, CD) and the CCA
than that of the CCA (p < 0.05). The corresponding TW length of (maximum correlation coefficient, CC). Here, the features extracted
the LASSO model was significantly shorter than that of the CCA from 1 s TW were used to analyze the performance of the two
(p < 0.05). In other words, the LASSO model could improve the speed methods. For most subjects, CD was higher than CC for the target
of BCI system without sacrificing classification accuracy in contrast frequency and CD was lower than CC for the non-target frequency.
to the CCA. This implies that the LASSO model produces more detectable fea-

Table 1
The p value among different TW lengths.

0.5 s vs. 1 s 1 s vs. 1.5 s 1.5 s vs. 2 s 2 s vs. 2.5 s 2.5 s vs. 3 s 3 s vs. 3.5 s 3.5 s vs. 4 s

LASSO p = 0.086 p = 0.15 p = 0.81 p = 1.0 p = 0.28 p = 0.51 p = 0.59


CCA p < 0.01 p < 0.01 p < 0.05 p = 0.13 p < 0.05 p = 0.16 p = 0.20
108 Y. Zhang et al. / Biomedical Signal Processing and Control 7 (2012) 104–111

Fig. 5. Classification features of different four target frequencies (f1 –f4 ). The black bar is the contribution degree (CD) of different stimulus frequencies in the LASSO model,
and the white bar is the maximum correlation coefficient (CC) of different stimulus frequencies in the CCA. The abscissa 1, 2, 3, 4 correspond to the stimulus frequencies f1 ,
f2 , f3 , f4 respectively. The features are extracted from 1 s TW, averaged over six runs and then normalized to [0,1].
Y. Zhang et al. / Biomedical Signal Processing and Control 7 (2012) 104–111 109

Fig. 6. Time–frequency representation of SSVEP (f1 –f4 ) through complex Morlet wavelet transform from the bandpass filtered (5–35 Hz) EEG signal on channel Oz and
averaged over six runs.
110 Y. Zhang et al. / Biomedical Signal Processing and Control 7 (2012) 104–111

Table 2 SSVEP frequency components are vulnerable to the interference


The highest information transfer rate (ITR) (bits/min) with the corresponding clas-
from non-related EEG or noises within a short TW. Thus, the CCA
sification accuracies (Acc) and time window length (TW).
may extract incorrect features from a short TW (e.g. less than 2 s)
Subject LASSO CCA since its recognition strategy is only based on the maximum of the
TW Acc ITR TW Acc ITR canonical correlation coefficient; (2) It has been reported that spar-
sity constraint can handle the signal corruption [20,37] and image
S1 1 1.0 60.0 1 0.96 50.5
S2 0.5 0.75 31.7 1.5 0.88 30.2 occlusion [24,38,39], such as noises, missing data and outliers. In
S3 3.5 0.71 8.90 3 0.71 10.0 our study, the sparsity constraint of the LASSO encouraged a sparse
S4 1.5 0.75 19.0 3 0.71 10.0 LASSO estimator that helped the LASSO mode robustly recognize
S5 1 0.96 50.5 1 0.83 32.6 the dominant frequency component in EEG signals. Hence, the tar-
S6 0.5 0.88 50.3 2.5 0.92 24.9
S7 0.5 0.88 50.3 1.5 0.88 30.2
get and non-target stimulus frequencies could be classified more
S8 0.5 0.80 38.4 0.5 0.60 15.8 accurately.
S9 0.5 0.83 43.4 2 0.92 29.1
Average 1.1 ± 1.0 0.84 ± 0.1 39.2 ± 16.6 1.8 ± 0.9 0.82 ± 0.12 25.9 ± 12.8
6. Conclusions

tures than that obtained from the CCA. The target frequency f2 of In this study, the proposed LASSO based linear regression model
S5, the target frequencies f2 and f4 of S6, and the target frequen- can recognize the stimulus frequency of SSVEP-based BCI in shorter
cies f2 and f3 of S8 were classified incorrectly by the CCA due to time without sacrificing the classification accuracy in contrast to
the indiscriminate features. However, the LASSO model extracted the CCA. This frequency recognition model can be further used in
more robust and distinct features making the target frequencies online SSVEP-based BCIs. Our future work will focus on designing
classified accurately. For S3, the target frequency could not be clas- an online BCI system based on this frequency recognition model
sified correctly neither by the LASSO model nor by the CCA. This is and testing its real-time performance in real world settings.
because that this subject was not able to focus on the flicker stim-
ulus, hence the evoked SSVEP might be too weak (see Fig. 6). It Acknowledgments
has been reported that SSVEP-based BCI was inapplicable for some
subjects due to their low attention to the stimulus or weak SSVEP The authors would like to thank the editor and anonymous ref-
response [1,4,12]. Fig. 6 depicts the time–frequency representa- erees for their valuable comments. They would also like to thank
tion of SSVEP at channel Oz by complex Morlet wavelet transform. Dr. F.Y. Cong (University of Jyväskylä, Finland) and Dr. B.Z. Alli-
While the SSVEP frequency spectrums can be observed for most son (Graz University of Technology, Austria) for their advice and
subjects, they are still disturbed by some non-related frequency English checking. This study is supported by Nation Nature Science
spectrums resulting from spontaneous EEG or other noises to vary- Foundation of China 61074113, Shanghai Leading Academic Disci-
ing extent. pline Project B504, and Fundamental Research Funds for the Central
Universities WH0914028.
5. Discussion
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