TABLE 3
Table 3. Subjects’ feedback to each paradigm.
Discussion
The present study mainly focused on the effect of chromatic stimulus on the performance of an ERP-based BCI and discussed several related problems stated as follows: (1) the influence on the offline error trials brought by the layout and the relationship between the layout and adjacency distraction, (2) the availability of the conclusion (Li et al., 2014) applied to the present study that better performance (including higher accuracy, higher amplitude, and shorter latency) occurred in a high-luminosity contrast, and (3) the observation of the ERP components’ waveforms in this work.
Performance
As for performance, classification accuracy and ITR were the main indexes to evaluate the performance of a BCI system. The online result (Table 2) depicted that the highest online averaged accuracy was obtained by R-P with 98.44%, higher than 92.71% by G-P, and 93.23% by B-P. In addition, significance was found between R-P and G-P both over online accuracy (p < 0.05) and ITR (p < 0.05), under the circumstance that all subjects were divided into three groups to experience the three paradigms in three kinds of order. Thus, the effects by the order of process were eliminated.To explain the result, some literature in psychology may help. It was found that longer-wavelength colors including red are considered as arousing or warm, whereas colors with a shorter wavelength like green and blue are associated with relaxing and cool (Nakshian, 1964). For one color as stimulus to be experienced lasting for 40 min at least in our experiment, the color of stimulus when flashing may exert some psychological hint to motivate or cool down the emotion of subjects to some degree. Some psychological experiments found that red can promote performance on some virtual target-shooting task (Sorokowski and Szmajke, 2011). They reported that the participants were able to hit red moving objects significantly better than blue and black objects, which was much relevant to our study in both stimulus color and the conclusion. On the side of biology, it was known that objects' information of color was described to be processed in visual area V4 of the human brain (Dubner and Zeki, 1971) and the cones in human's eyes have different light sensitivity to red, green, and blue light. This paper's result may give some evidence or reference to help related biological research.In related studies, the green/blue flicker paradigm achieved an 80.60% online classification accuracy (Takano et al., 2009). The paradigm that set a green familiar face as stimulus yielded an 86.1% online accuracy on average (Li et al., 2015). An SSVEP-BCI utilizing red, green, blue, and violet as stimuli showed that the violet one gained the highest accuracy of 94.38%, and the red one obtained 90.21% in wheelchair control application (Singla et al., 2013). Hence, the novel BCI with chromatic stimulus is consistent, efficient, and practicable, as judged by extracting consistent ERP wave features and outstanding mean accuracy over 90% online experiments for all 12 subjects.Layout of the StimulusIn this work, we applied a novel layout paradigm with chromatic stimulus flashing in blocks on the basis of SCP. The benefits of this design lie in two parts. One is the problem of double flash. Considering that eight blocks randomly flashed once in one trial, and the SOA of one flash is 400 ms, a single target cannot possibly flash twice in a time interval shorter than 800 ms. The other is adjacency distraction. As shown in the section Effects by the Layout, the position indeed influenced the error trials in offline sessions significantly, but the ratios it caused were 0.56% for the outer blocks and 0.98% for the inner blocks, thereby indicating a comparatively minor aspect in terms of the whole situation, especially after model modification.Color ContrastAs mentioned in the section Color Contrast Calculation, the color contrast ratio was 2.61:1 for R-P, 1.29:1 for G-P, and 3.66:1 for B-P with a white background. In previous literature (Nam et al., 2010; Li et al., 2014), all of the values of RGB channels remained equal, and the groups for contrast were limited to two. However, when the comparison groups of stimulus color increased to three in the present study, several previous results did not show similarity with the trend. In P300 waveform, no satisfactory significance was shown in the P300 amplitude of three paradigms within subjects at Pz, inconsistent with the trend in the literature. For online accuracy, a higher averaged accuracy was obtained by R-P, followed by B-P and G-P, as shown in Table 2; hence, G-P had the lowest color contrast ranked at the bottom, whereas the results of R-P and G-P cannot be satisfied by that observation. Moreover, the relationship between color contrast and accuracy is not linear.ERP ComponentVisual stimulus features such as color are processed in the ventral stream of visual pathways over the occipitotemporal areas of the brain (Corbetta et al., 1991; Merigan and Maunsell, 1993).P2 peak waveform features in the present study resulted in obtaining a longer latency in G-P at Oz. The oddball paradigm is one primary way to evoke P2, and its amplitude can be enhanced to the targets (Ferreira-Santos et al., 2012). However, in a visual search paradigm, more specific research has been performed on stimulus features (e.g., color, size, and orientation) to explore the mechanisms for feature detection in the brain (Luck and Hillyard, 1994). Thus, the findings in the present work are relatively supplemented in this area.N2, which is an endogenous component similar to P300, corresponds to visual attention or degree of attention. In the present study, the N2 latency from G-P was significantly longer than that of the two other paradigms within all subjects. This result was caused by a shorter latency shown in high color contrast, whereas a longer latency was shown in low color contrast (Li et al., 2014). Here, “green” obtained the lowest value in color contrast at the white background.Meanwhile, P300 and N4 failed to exhibit significance either in amplitude or in latency. As shown in Figure 5, the three grand averaged curves were relatively close to each other under the color shadows of P300 and N4 waveforms, thereby indicating that P300 and N4 were not sensitive to different stimulus colors in this work.ConclusionThe color of stimulus out of RGB could achieve the best performance in an ERP-based BCI by designing a novel layout in a single-character pattern. In detail, R-P yielded the highest online averaged accuracy and the fastest ITR among the three; G-P displayed a longer latency in the ERP waveforms of P2 and N2. Moreover, the eight blocks in the paradigm can be replaced with control commands or be applied to psychological attention estimation. Further investigation will be performed on the neural mechanism of our experimental results. Besides, further improvement may focus on the algorithm improvement, enhancement of ITR, and fatigue supervision (e.g., heart rate and body temperature).Ethics StatementThis work was approved by Shanghai Xuhui Central Hospital Committee, SOP-IEC-033-01.0-AF02. This study was carried out in accordance with the recommendations of name of guidelines, name of committee with written informed consent from all subjects. All subjects gave written informed consent in accordance with the Declaration of Helsinki. The protocol was approved by the name of committee.Author ContributionsMG designed the concept of the manuscript, designed the whole experiment, and collected the original data set. All authors contributed to manuscript revision and read and approved the submitted version.FundingThis work was supported by the National Key Research and Development Program 2017YFB13003002. This work was also supported in part by the National Natural Science Foundation of China under Grant Nos. 61573142, 61773164, and 91420302; the program of Introducing Talents of Discipline to Universities (the 111 Project) under grant B17017; and the Polish National Science Center (UMO-2016/20/W/NZG/00354) in search of the sources of brain's cognitive activity.Conflict of Interest StatementThe authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.References Alharbi, E., Rasheed, S., and Buhari, S. (2016). Single trial classification of evoked EEG signals due to RGB colors. Broad Res. Artif. Intell. Neurosci. 7, 29–41. Available online at: http://brain.edusoft.ro/index.php/brain/article/view/568/635Google Scholar Chen, L., Jin, J., Zhang, Y., Wang, X., and Cichocki, A. (2015). A survey of the dummy face and human face stimuli used in BCI paradigm. J. Neurosci. Methods 239, 18–27. doi: 10.1016/j.jneumeth.2014.10.002PubMed Abstract | CrossRef Full Text | Google Scholar Cheng, J., Jin, J., Daly, I., Zhang, Y., Wang, B., Wang, X., et al. (2018). Effect of a combination of flip and zooming stimuli on the performance of a visual brain-computer interface for spelling. Biomed. Eng. /Biomed. Tech. 64, 29–38. doi: 10.1515/bmt-2017-0082PubMed Abstract | CrossRef Full Text | Google Scholar Coles, M. G. H., and Rugg, M. D. (eds.). (1995). “Event-related brain potentials: an introduction,” in Electrophysiology of Mind: Event-Related Brain Potentials and Cognition, Oxford Psychology Series No. 25 (New York, NY: Oxford University Press), 1–26.Google Scholar Corbetta, M., Miezin, F. M., Dobmeyer, S., Shulman, G. L., and Petersen, S. E. (1991). Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography. J. Neurosci. 11, 2383–2402. doi: 10.1523/JNEUROSCI.11-08-02383.1991PubMed Abstract | CrossRef Full Text | Google Scholar Dubner, R., and Zeki, S. (1971). Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus in the monkey. Brain Res. 35, 528–532. doi: 10.1016/0006-8993(71)90494-XPubMed Abstract | CrossRef Full Text | Google Scholar Farwell, L. A., and Donchin, E. (1988). Talking off the top of your head: toward a mental prosthesis utilizing event-related brain potentials. Electroencephalogr. Clin. Neurophysiol. 70:510. doi: 10.1016/0013-4694(88)90149-6PubMed Abstract | CrossRef Full Text | Google Scholar Fazel-Rezai, R., Allison, B. Z., Guger, C., Sellers, E. W., Kleih, S. C., and Kübler, A. (2012). P300 brain computer interface: current challenges and emerging trends. Front. Neuroeng. 5:14. doi: 10.3389/fneng.2012.00014PubMed Abstract | CrossRef Full Text | Google Scholar Ferreira-Santos, F., Silveira, C., Almeida, P., Palha, A., Barbosa, F., and Marques-Teixeira, J. (2012). The auditory P200 is both increased and reduced in schizophrenia? A meta-analytic dissociation of the effect for standard and target stimuli in the oddball task. Clin. Neurophysiol. 123, 1300–1308. doi: 10.1016/j.clinph.2011.11.036PubMed Abstract | CrossRef Full Text | Google Scholar Freunberger, R., Klimesch, W., Doppelmayr, M., and Höller, Y. (2007). Visual P2 component is related to theta phase-locking. Neurosci. Lett. 426, 181–186. doi: 10.1016/j.neulet.2007.08.062PubMed Abstract | CrossRef Full Text | Google Scholar Furdea, A., Halder, S., Krusienski, D., Bross, D., Nijboer, F., Birbaumer, N., et al. (2009). An auditory oddball (P300) spelling system for brain–computer interfaces. Psychophysiology 46, 617–625. doi: 10.1111/j.1469-8986.2008.00783.xPubMed Abstract | CrossRef Full Text | Google Scholar Guger, C., Daban, S., Sellers, E., Holzner, C., Krausz, G., Carabalona, R., et al. (2009). How many people are able to control a P300-based brain–computer interface (BCI)? Neurosci. Lett. 462, 94–98. doi: 10.1016/j.neulet.2009.06.045PubMed Abstract | CrossRef Full Text | Google Scholar Guo, F., Hong, B., Gao, X., and Gao, S. (2008). A brain–computer interface using motion-onset visual evoked potential. J. Neural Eng. 5:477. doi: 10.1088/1741-2560/5/4/011PubMed Abstract | CrossRef Full Text | Google Scholar Hoffmann, U., Vesin, J. M., Ebrahimi, T., and Diserens, K. (2008). An efficient P300-based brain–computer interface for disabled subjects. J. Neurosci. Methods 167, 115–125. doi: 10.1016/j.jneumeth.2007.03.005PubMed Abstract | CrossRef Full Text | Google Scholar Hong, B., Guo, F., Liu, T., Gao, X., and Gao, S. (2009). N200-speller using motion-onset visual response. Clin. Neurophysiol. 120, 1658–1666. doi: 10.1016/j.clinph.2009.06.026PubMed Abstract | CrossRef Full Text | Google Scholar Hwang, H.-J., Kwon, K., and Im, C.-H. (2009). Neurofeedback-based motor imagery training for brain–computer interface (BCI). J. Neurosci. Methods 179, 150–156. doi: 10.1016/j.jneumeth.2009.01.015PubMed Abstract | CrossRef Full Text | Google Scholar Jiao, Y., Zhang, Y., Chen, X., Yin, E., Jin, J., Yu Wang, X., et al. (2018). Sparse group representation model for motor imagery EEG classification. IEEE J. Biomed. Health Inf. 23, 631–641. doi: 10.1109/JBHI.2018.2832538PubMed Abstract | CrossRef Full Text | Google Scholar Jiao, Y., Zhang, Y., Jin, J., and Wang, X. (2016). “Multilayer correlation maximization for frequency recognition in SSVEP brain-computer interface,” in Information Science and Technology (ICIST), 2016 Sixth International Conference on (IEEE), Dailan, 31–35. doi: 10.1109/ICIST.2016.7483381CrossRef Full Text | Google Scholar Jin, J., Allison, B. Z., Sellers, E. W., Brunner, C., Horki, P., Wang, X., et al. (2011). An adaptive P300-based control system. J. Neural Eng. 8:036006. doi: 10.1088/1741-2560/8/3/036006PubMed Abstract | CrossRef Full Text | Google Scholar Jin, J., Allison, B. Z., Zhang, Y., Wang, X., and Cichocki, A. (2014). An ERP-based BCI using an oddball paradigm with different faces and reduced errors in critical functions. Int. J. Neural Syst. 24:1450027. doi: 10.1142/S0129065714500270PubMed Abstract | CrossRef Full Text | Google Scholar Jin, J., Horki, P., Brunner, C., Wang, X., Neuper, C., and Pfurtscheller, G. (2010). A new P300 stimulus presentation pattern for EEG-based spelling systems. Biomed. Tech./Biomed. Eng. 55, 203–210. doi: 10.1515/bmt.2010.029PubMed Abstract | CrossRef Full Text | Google Scholar Jin, J., Sellers, E. W., Zhou, S., Zhang, Y., Wang, X., and Cichocki, A. (2015). A P300 brain–computer interface based on a modification of the mismatch negativity paradigm. Int. J. Neural Syst. 25, 157–584. doi: 10.1142/S0129065715500112PubMed Abstract | CrossRef Full Text | Google Scholar Kübler, A., Furdea, A., Halder, S., Hammer, E. M., Nijboer, F., and Kotchoubey, B. (2009). A brain–computer interface controlled auditory event-related potential (P300) spelling system for locked-in patients. Ann. N.Y. Acad. Sci. 1157, 90–100. doi: 10.1111/j.1749-6632.2008.04122.xPubMed Abstract | CrossRef Full Text | Google Scholar Li, Q., Liu, S., Li, J., and Bai, O. (2015). Use of a green familiar faces paradigm improves p300-speller brain–computer interface performance. PloS ONE 10:e0130325. doi: 10.1371/journal.pone.0130325PubMed Abstract | CrossRef Full Text | Google Scholar Li, Y., Bahn, S., Chang, S. N., and Lee, J. (2014). Effects of luminosity contrast and stimulus duration on user performance and preference in a P300-based brain–computer interface. Int. J. Hum. Comput. Interact. 30, 151–163. doi: 10.1080/10447318.2013.839903CrossRef Full Text | Google Scholar Li, Y., Pan, J., Long, J., Yu, T., Wang, F., Yu, Z., et al. (2016). Multimodal BCIs: target detection, multidimensional control, and awareness evaluation in patients with disorder of consciousness. Proc. IEEE 104, 332–352. doi: 10.1109/JPROC.2015.2469106CrossRef Full Text | Google Scholar Luck, S. J., and Hillyard, S. A. (1994). Electrophysiological correlates of feature analysis during visual search. Psychophysiology 31, 291–308. doi: 10.1111/j.1469-8986.1994.tb02218.xPubMed Abstract | CrossRef Full Text | Google Scholar Martens, S. M., Hill, N., Farquhar, J., and Schölkopf, B. (2009). Overlap and refractory effects in a brain–computer interface speller based on the visual P300 event-related potential. J. Neural Eng. 6:026003. doi: 10.1088/1741-2560/6/2/026003PubMed Abstract | CrossRef Full Text | Google Scholar Merigan, W. H., and Maunsell, J. H. (1993). How parallel are the primate visual pathways? Annu. Rev. Neurosci. 16, 369–402. doi: 10.1146/annurev.ne.16.030193.002101PubMed Abstract | CrossRef Full Text | Google Scholar Nakanishi, M., Wang, Y., Chen, X., Wang, Y.-T., Gao, X., and Jung, T.-P. (2018). Enhancing detection of SSVEPs for a high-speed brain speller using task-related component analysis. IEEE Trans. Biomed. Eng. 65, 104–112. doi: 10.1109/TBME.2017.2694818PubMed Abstract | CrossRef Full Text | Google Scholar Nakshian, J. S. (1964). The effects of red and green surroundings on behavior. J. Gen. Psychol. 70, 143–161. doi: 10.1080/00221309.1964.9920584PubMed Abstract | CrossRef Full Text | Google Scholar Nam, C. S., Li, Y., and Johnson, S. (2010). Evaluation of P300-based brain–computer interface in real-world contexts. Int. J. Hum. Comput. Interact. 26, 621–637. doi: 10.1080/10447311003781326CrossRef Full Text | Google Scholar Ortner, R., Allison, B. Z., Korisek, G., Gaggl, H., and Pfurtscheller, G. (2011). An SSVEP BCI to control a hand orthosis for persons with tetraplegia. IEEE Trans. Neural Syst. Rehabil. Eng. 19, 1–5. doi: 10.1109/TNSRE.2010.2076364PubMed Abstract | CrossRef Full Text | Google Scholar Pfurtscheller, G., and Neuper, C. (2001). Motor imagery and direct brain–computer communication. Proc. IEEE 89, 1123–1134. doi: 10.1109/5.939829CrossRef Full Text | Google Scholar Pfurtscheller, G., Solis-Escalante, T., Ortner, R., Linortner, P., and Muller-Putz, G. R. (2010). Self-paced operation of an SSVEP-Based orthosis with and without an imagery-based “brain switch:” a feasibility study towards a hybrid BCI. IEEE Trans. Neural Syst. Rehabil. Eng. 18, 409–414. doi: 10.1109/TNSRE.2010.2040837PubMed Abstract | CrossRef Full Text | Google Scholar Pires, G., Nunes, U., and Castelo-Branco, M. (2012). Comparison of a row-column speller vs. a novel lateral single-character speller: assessment of BCI for severe motor disabled patients. Clin. Neurophysiol. 123, 1168–1181. doi: 10.1016/j.clinph.2011.10.040PubMed Abstract | CrossRef Full Text | Google Scholar Rasheed, S., and Marini, D. (2015). Classification of EEG signals produced by RGB colour stimuli. J. Biomed. Eng. Med. Imaging 2:56. doi: 10.14738/jbemi.25.1566CrossRef Full Text | Google Scholar Salvaris, M., and Sepulveda, F. (2009). Visual modifications on the P300 speller BCI paradigm. J. Neural Eng. 6:046011. doi: 10.1088/1741-2560/6/4/046011PubMed Abstract | CrossRef Full Text | Google Scholar Sellers, E. W., Krusienski, D. J., Mcfarland, D. J., Vaughan, T. M., and Wolpaw, J. R. (2006). A P300 event-related potential brain–computer interface (BCI): the effects of matrix size and inter stimulus interval on performance. Biol. Psychol. 73, 242–252. doi: 10.1016/j.biopsycho.2006.04.007PubMed Abstract | CrossRef Full Text | Google Scholar Singla, R., Khosla, A., and Jha, R. (2013). Influence of stimuli color on steady-state visual evoked potentials based BCI wheelchair control. J. Biomed. Sci. Eng. 6. doi: 10.4236/jbise.2013.611131CrossRef Full Text | Google Scholar Sorokowski, P., and Szmajke, A. (2011). The influence of the” Red Win” effect in sports: a hypothesis of erroneous perception of opponents dressed in red-Preliminary test. Hum. Mov. 12, 367–373. doi: 10.2478/v10038-011-0043-5CrossRef Full Text | Google Scholar Sutton, S., Braren, M., Zubin, J., and John, E. (1965). Evoked-potential correlates of stimulus uncertainty. Science 150, 1187–1188. doi: 10.1126/science.150.3700.1187PubMed Abstract | CrossRef Full Text | Google Scholar Takano, K., Komatsu, T., Hata, N., Nakajima, Y., and Kansaku, K. (2009). Visual stimuli for the P300 brain–computer interface: a comparison of white/gray and green/blue flicker matrices. Clin. Neurophysiol. 120, 1562–1566. doi: 10.1016/j.clinph.2009.06.002PubMed Abstract | CrossRef Full Text | Google Scholar Townsend, G., Lapallo, B., Boulay, C., Krusienski, D., Frye, G., Hauser, C., et al. (2010). A novel P300-based brain–computer interface stimulus presentation paradigm: moving beyond rows and columns. Clin. Neurophysiol. 121, 1109–1120. doi: 10.1016/j.clinph.2010.01.030PubMed Abstract | CrossRef Full Text | Google Scholar Vidal, J. J. (1973). Toward direct brain–computer communication. Annu. Rev. Biophys. Bioeng. 2, 157–180. doi: 10.1146/annurev.bb.02.060173.001105PubMed Abstract | CrossRef Full Text | Google Scholar Vidal, J. J. (1977). Real-time detection of brain events in EEG. Proc. IEEE 65, 633–641. doi: 10.1109/PROC.1977.10542CrossRef Full Text | Google Scholar Wang, Y., Gao, S., and Gao, X. (2006). “Common spatial pattern method for channel selection in motor imagery based brain–computer interface,” in Engineering in Medicine and Biology Society, 2005. IEEE-EMBS 2005. 27th Annual International Conference of the (IEEE), Shanghai, 5392–5395.Google Scholar Wolpaw, J. R., Birbaumer, N., Heetderks, W. J., Mcfarland, D. J., Peckham, P. H., Schalk, G., et al. (2000). Brain–computer interface technology: a review of the first international meeting. IEEE Trans. Rehabil. Eng. 8:164. doi: 10.1109/TRE.2000.847807PubMed Abstract | CrossRef Full Text | Google Scholar Wolpaw, J. R., Birbaumer, N., Mcfarland, D. J., Pfurtscheller, G., and Vaughan, T. M. (2002). Brain–computer interfaces for communication and control. Clin. Neurophysiol. 113, 767–791. doi: 10.1016/S1388-2457(02)00057-3PubMed Abstract | CrossRef Full Text | Google Scholar Zhang, Y., Guo, D., Li, F., Yin, E., Zhang, Y., Li, P., et al. (2018). Correlated component analysis for enhancing the performance of SSVEP-based brain-computer interface. IEEE Trans. Neural Syst. Rehabil. Eng. 26, 948–956. doi: 10.1109/TNSRE.2018.2826541CrossRef Full Text | Google Scholar Zhang, Y., Zhao, Q., Jin, J., Wang, X., and Cichocki, A. (2012). A novel BCI based on ERP components sensitive to configural processing of human faces. J. Neural Eng. 9:026018. doi: 10.1088/1741-2560/9/2/026018PubMed Abstract | CrossRef Full Text | Google ScholarKeywords: brain–computer interface, ERP, color of stimulus, visual stimulus, single character paradigmCitation: Guo M, Jin J, Jiao Y, Wang X and Cichockia A (2019) Investigation of Visual Stimulus With Various Colors and the Layout for the Oddball Paradigm in Evoked Related Potential-Based Brain–Computer Interface. Front. Comput. Neurosci. 13:24. doi: 10.3389/fncom.2019.00024Received: 18 January 2019; Accepted: 01 April 2019;Published: 26 April 2019.Edited by: Rong Chen, University of Maryland, Baltimore, United StatesReviewed by: Daqing Guo, University of Electronic Science and Technology of China, ChinaJunfeng Sun, Shanghai Jiao Tong University, ChinaCopyright © 2019 Guo, Jin, Jiao, Wang and Cichockia. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.*Correspondence: Jing Jin, jinjingat@gmail.com