Comparison of the influence of stimuli color on Steady-State Visual Evoked Potentials
Tello, Richard Junior Manuel Godinez; Müller, Sandra Mara Torres; Ferreira, André; Bastos, Teodiano Freire
http://dx.doi.org/10.1590/2446-4740.0739
Res. Biomed. Eng., vol.31, n3, p.218-231, 2015
Downloads: 2
Views: 835
Abstract
Introduction: The main idea of a traditional Steady State Visually Evoked Potentials (SSVEP)-BCI is the activation of commands through gaze control. For this purpose, the retina of the eye is excited by a stimulus at a certain frequency. Several studies have shown effects related to different kind of stimuli, frequencies, window lengths, techniques of feature extraction and even classification. So far, none of the previous studies has performed a comparison of performance of stimuli colors through LED technology. This study addresses precisely this important aspect and would be a great contribution to the topic of SSVEP-BCIs. Additionally, the performance of different colors at different frequencies and the visual comfort were evaluated in each case. Methods: LEDs of four different colors (red, green, blue and yellow) flickering at four distinct frequencies (8, 11, 13 and 15 Hz) were used. Twenty subjects were distributed in two groups performing different protocols. Multivariate Synchronization Index (MSI) was the technique adopted as feature extractor. Results: The accuracy was gradually enhanced with the increase of the time window. From our observations, the red color provides, in most frequencies, both highest rates of accuracy and Information Transfer Rate (ITR) for detection of SSVEP. Conclusion: Although the red color has presented higher ITR, this color was turned in the less comfortable one and can even elicit epileptic responses according to the literature. For this reason, the green color is suggested as the best choice according to the proposed rules. In addition, this color has shown to be safe and accurate for an SSVEP-BCI.
Keywords
Brain Computer Interface, color, EEG, LED, SSVEP.
References
Bieger J, Garcia-Molina G, Zhu D. Effects of stimulation properties in Steady-State Visual Evoked Potential based Brain-Computer Interfaces. In: Proceedings of 32nd Annual International Conference of the IEEE Engineering in Medicine and Biology Society; 2010 Aug 31-Sep 04; Buenos Aires, Argentina. Engineering in Medicine and Biology Society; 2010. p. 3345-8.
Bieger J, Garcia-Molina G. Light stimulation properties to influence brain activity: a brain-computer interface application [internet]. Philips Research; 2010 Oct [cited 2015 Feb 26]; 7-9. Available from: http://repository.tudelft.nl/view/philips/uuid%3A617bbd89-8ab8-49da-9fc8-f6c7803724c9/.
Buechner VL, Maier MA, Lichtenfeld S, Schwarz S. Red - take a closer look. PLoS One. 2014; 9(9):e108111. http://dx.doi.org/10.1371/journal.pone.0108111. PMid:25254380.
Cao T, Wan F, Peng UM, Pui-In M, Mang IV, Yong H. Flashing color on the performance of SSVEP-based Brain-Computer Interfaces. In: International Conference of the IEEE EMBS; 2012; San Diego, CA. IEEE; 2012. p. 1819-22. http://dx.doi.org/10.1109/EMBC.2012.6346304.
Carmeli C, Knyazeva MG, Innocenti GM, De Feo O. Assessment of EEG synchronization based on state-space analysis. NeuroImage. 2005; 25(2):339-54. http://dx.doi.org/10.1016/j.neuroimage.2004.11.049. PMid:15784413.
Chellappa SL, Steiner R, Blattner P, Oelhafen P, Götz T, Cajochen C. Non-visual effects of light on melatonin, alertness and cognitive performance: can blue-enriched light keep us alert? PLoS One. 2011; 6(1):e16429. http://dx.doi.org/10.1371/journal.pone.0016429. PMid:21298068.
Di Russo F, Pitzalis S, Aprile T, Spitoni G, Patria F, Stella A, Spinelli D, Hillyard SA. Spatiotemporal analysis of the cortical sources of the steady-state visual evoked potential. Human Brain Mapping. 2007; 28(4):323-34. http://dx.doi.org/10.1002/hbm.20276. PMid:16779799.
Drew P, Sayres R, Watanabe K, Shimojo S. Pupillary response to chromatic flicker. Experimental Brain Research. 2001; 136(2):256-62. http://dx.doi.org/10.1007/s002210000605. PMid:11206288.
Ebersole JS, Pedley TA. Current practice of clinical electroencephalography. 3rd ed. Philadelphia: Lippincott Williams & Wilkins; 2002.
Elliot AJ. Color and psychological functioning: a review of theoretical and empirical work. Frontiers in Psychology. 2015; 6(368):368. http://dx.doi.org/10.3389/fpsyg.2015.00368. PMid:25883578.
Elliot AJ, Fairchild MD, Franklin A. Handbook of color psychology. Cambridge: Cambridge University Press; 2014.
Fisher RS, Harding G, Erba G, Barkley GL, Wilkins A. Photic- and pattern-induced seizures: a review for the epilepsy foundation of America working group. Epilepsia. 2005; 46(9):1426-41. http://dx.doi.org/10.1111/j.1528-1167.2005.31405.x. PMid:16146439.
Gregory R. Eye and brain the psychology of seeing. Princeton: Princeton University Press; 1997.
Herrmann CS. Human EEG responses to 1-100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena. Experimental Brain Research. 2001; 137(3-4):346-53. http://dx.doi.org/10.1007/s002210100682. PMid:11355381.
Kelly SP, Lalor EC, Finucane C, McDarby G, Reilly RB. Visual spatial attention control in an independent brain-computer interface. IEEE Transactions on Biomedical Engineering. 2005a; 52(9):1588-96. http://dx.doi.org/10.1109/TBME.2005.851510. PMid:16189972.
Kelly SP, Lalor EC, Reilly RB, Foxe JJ. Independent Brain Computer Interface control using visual spatial attention-dependent modulations of parieto-occipital alpha. In: Proceedings of the 2nd International IEEE EMBS Conference on Neural Engineering; 2005; Arlington, VA. IEEE; 2005b. p. 667-70. http://dx.doi.org/10.1109/CNE.2005.1419713.
Krolak-Salmon P, Hénaff MA, Tallon-Baudry C, Yvert B, Guénot M, Vighetto A, Mauguière F, Bertrand O. Human lateral geniculate nucleus and visual cortex respond to screen flicker. Annals of Neurology. 2003; 53(1):73-80. http://dx.doi.org/10.1002/ana.10403. PMid:12509850.
Lindsey DT, Brown AM, Reijnen E, Rich AN, Kuzmova YI, Wolfe JM. Color channels, not color appearance or color categories, guide visual search for desaturated color targets. Psychological Science. 2010; 21(9):1208-14. http://dx.doi.org/10.1177/0956797610379861. PMid:20713637.
McFarland DJ, McCane LM, David SV, Wolpaw JR. Spatial filter selection for EEG-based communication. Electroencephalography and Clinical Neurophysiology. 1997; 103(3):386-94. http://dx.doi.org/10.1016/S0013-4694(97)00022-2. PMid:9305287.
Mehta R, Zhu RJ. Blue or red? Exploring the effect of color on cognitive task performances. Science. 2009; 323(5918):1226-9. http://dx.doi.org/10.1126/science.1169144. PMid:19197022.
Moller AC, Elliot AJ, Maier MA. Basic hue-meaning associations. Emotion. 2009; 9(6):898-902. http://dx.doi.org/10.1037/a0017811. PMid:20001133.
Morgan ST, Hansen JC, Hillyard SA. Selective attention to stimulus location modulates the steady-state visual evoked potential. Proceedings of the National Academy of Sciences of the United States of America. 1996; 93(10):4770-4. http://dx.doi.org/10.1073/pnas.93.10.4770. PMid:8643478.
Pastor MA, Artieda J, Arbizu J, Valencia M, Masdeu JC. Human cerebral activation during steady-state visual-evoked responses. The Journal of Neuroscience. 2003; 23(37):11621-7. PMid:14684864.
Pomerleau VJ, Fortier-Gauthier U, Corriveau I, Dell’Acqua R, Jolicœur P. Colour-specific differences in attentional deployment for equiluminant pop-out colours: evidence from lateralised potentials. International Journal of Psychophysiology. 2014; 91(3):194-205. http://dx.doi.org/10.1016/j.ijpsycho.2013.10.016. PMid:24188915.
Regan D. An effect of stimulus colour on average steady-state potentials evoked in man. Nature. 1966; 210(5040):1056-7. http://dx.doi.org/10.1038/2101056a0. PMid:5914904.
Rubboli G, Parra J, Seri S, Takahashi T, Thomas P. EEG diagnostic procedures and special investigations in the assessment of photosensitivity. Epilepsia. 2004; 45(1 Suppl 1):35-9. http://dx.doi.org/10.1111/j.0013-9580.2004.451002.x. PMid:14706044.
Sammer G, Blecker C, Gebhardt H, Kirsch P, Stark R, Vaitl D. Acquisition of typical EEG waveforms during fMRI: SSVEP, LRP, and frontal theta. NeuroImage. 2005; 24(4):1012-24. http://dx.doi.org/10.1016/j.neuroimage.2004.10.026. PMid:15670678.
Tello RJMG, Muller SMT, Bastos TF Fo, Ferreira A. A comparison of techniques and technologies for SSVEP classification. In: IEEE-ISSNIP Biosignals and Biorobotics Conference: Biosignals and Robotics for Better and Safer Living (BRC); 2014; Salvador. IEEE; 2014a. p. 1-6. http://dx.doi.org/10.1109/BRC.2014.6880956.
Tello RJMG, Muller SMT, Bastos TF Fo, Ferreira A. Comparison of new techniques based on EMD for control of a SSVEP-BCI. In: IEEE 23rd International Symposium on Industrial Electronics (ISIE); 2014; Istanbul. IEEE; 2014b. p. 992-7. http://dx.doi.org/10.1109/ISIE.2014.6864747.
Tello RJMG, Muller SMT, Bastos TF Fo, Ferreira A. Comparison between wire and wireless EEG acquisition systems based on SSVEP in an independent-BCI. In: 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC’14). 2014c. p. 22-25. http://dx.doi.org/10.1109/EMBC.2014.6943519.
Tello RG, Pant JK, Müller SM, Krishnan S, Bastos TF Fo. An evaluation of performance for an independent SSVEP-BCI based on compressive sensing system. In: Jaffray DA. World Congress on Medical Physics and Biomedical Engineering; 2015 June 7-12; Toronto, Canada. Springer International Publishing; 2015. p. 982-5. (IFMBE Proceedings, 51). http://dx.doi.org/10.1007/978-3-319-19387-8_239.
Vialatte FB, Maurice M, Dauwels J, Cichocki A. Steady-state visually evoked potentials: focus on essential paradigms and future perspectives. Progress in Neurobiology. 2010; 90(4):418-38. http://dx.doi.org/10.1016/j.pneurobio.2009.11.005. PMid:19963032.
Wang Y, Wang R, Gao X, Hong B, Gao S. A practical VEP based brain-computer interface. IEEE Transactions on Neural Systems and Rehabilitation Engineering. 2006; 14(2):234-40. http://dx.doi.org/10.1109/TNSRE.2006.875576.
Wu Z, Lai Y, Xia Y, Wu D, Yao D. Stimulator selection in SSVEP-based BCI. Medical Engineering & Physics. 2008; 30(8):1079-88. http://dx.doi.org/10.1016/j.medengphy.2008.01.004. PMid:18316226.
Zhang Y, Wang R, Hong B, Gao X, Gao S. Source estimation of contrast-related perception based on frequency-tagged binocular rivalry. In: EMBS '06. 28th Annual International Conference of Engineering in Medicine and Biology Society; 2006; New York, NY. IEEE; 2006. p. 1177-80. http://dx.doi.org/10.1109/IEMBS.2006.260094.
Zhang Y, Xu P, Cheng K, Yao D. Multivariate synchronization index for frequency recognition of SSVEP-based brain-computer interface. Journal of Neuroscience Methods. 2014; 221(1):32-40. http://dx.doi.org/10.1016/j.jneumeth.2013.07.018. PMid:23928153.
Bieger J, Garcia-Molina G. Light stimulation properties to influence brain activity: a brain-computer interface application [internet]. Philips Research; 2010 Oct [cited 2015 Feb 26]; 7-9. Available from: http://repository.tudelft.nl/view/philips/uuid%3A617bbd89-8ab8-49da-9fc8-f6c7803724c9/.
Buechner VL, Maier MA, Lichtenfeld S, Schwarz S. Red - take a closer look. PLoS One. 2014; 9(9):e108111. http://dx.doi.org/10.1371/journal.pone.0108111. PMid:25254380.
Cao T, Wan F, Peng UM, Pui-In M, Mang IV, Yong H. Flashing color on the performance of SSVEP-based Brain-Computer Interfaces. In: International Conference of the IEEE EMBS; 2012; San Diego, CA. IEEE; 2012. p. 1819-22. http://dx.doi.org/10.1109/EMBC.2012.6346304.
Carmeli C, Knyazeva MG, Innocenti GM, De Feo O. Assessment of EEG synchronization based on state-space analysis. NeuroImage. 2005; 25(2):339-54. http://dx.doi.org/10.1016/j.neuroimage.2004.11.049. PMid:15784413.
Chellappa SL, Steiner R, Blattner P, Oelhafen P, Götz T, Cajochen C. Non-visual effects of light on melatonin, alertness and cognitive performance: can blue-enriched light keep us alert? PLoS One. 2011; 6(1):e16429. http://dx.doi.org/10.1371/journal.pone.0016429. PMid:21298068.
Di Russo F, Pitzalis S, Aprile T, Spitoni G, Patria F, Stella A, Spinelli D, Hillyard SA. Spatiotemporal analysis of the cortical sources of the steady-state visual evoked potential. Human Brain Mapping. 2007; 28(4):323-34. http://dx.doi.org/10.1002/hbm.20276. PMid:16779799.
Drew P, Sayres R, Watanabe K, Shimojo S. Pupillary response to chromatic flicker. Experimental Brain Research. 2001; 136(2):256-62. http://dx.doi.org/10.1007/s002210000605. PMid:11206288.
Ebersole JS, Pedley TA. Current practice of clinical electroencephalography. 3rd ed. Philadelphia: Lippincott Williams & Wilkins; 2002.
Elliot AJ. Color and psychological functioning: a review of theoretical and empirical work. Frontiers in Psychology. 2015; 6(368):368. http://dx.doi.org/10.3389/fpsyg.2015.00368. PMid:25883578.
Elliot AJ, Fairchild MD, Franklin A. Handbook of color psychology. Cambridge: Cambridge University Press; 2014.
Fisher RS, Harding G, Erba G, Barkley GL, Wilkins A. Photic- and pattern-induced seizures: a review for the epilepsy foundation of America working group. Epilepsia. 2005; 46(9):1426-41. http://dx.doi.org/10.1111/j.1528-1167.2005.31405.x. PMid:16146439.
Gregory R. Eye and brain the psychology of seeing. Princeton: Princeton University Press; 1997.
Herrmann CS. Human EEG responses to 1-100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena. Experimental Brain Research. 2001; 137(3-4):346-53. http://dx.doi.org/10.1007/s002210100682. PMid:11355381.
Kelly SP, Lalor EC, Finucane C, McDarby G, Reilly RB. Visual spatial attention control in an independent brain-computer interface. IEEE Transactions on Biomedical Engineering. 2005a; 52(9):1588-96. http://dx.doi.org/10.1109/TBME.2005.851510. PMid:16189972.
Kelly SP, Lalor EC, Reilly RB, Foxe JJ. Independent Brain Computer Interface control using visual spatial attention-dependent modulations of parieto-occipital alpha. In: Proceedings of the 2nd International IEEE EMBS Conference on Neural Engineering; 2005; Arlington, VA. IEEE; 2005b. p. 667-70. http://dx.doi.org/10.1109/CNE.2005.1419713.
Krolak-Salmon P, Hénaff MA, Tallon-Baudry C, Yvert B, Guénot M, Vighetto A, Mauguière F, Bertrand O. Human lateral geniculate nucleus and visual cortex respond to screen flicker. Annals of Neurology. 2003; 53(1):73-80. http://dx.doi.org/10.1002/ana.10403. PMid:12509850.
Lindsey DT, Brown AM, Reijnen E, Rich AN, Kuzmova YI, Wolfe JM. Color channels, not color appearance or color categories, guide visual search for desaturated color targets. Psychological Science. 2010; 21(9):1208-14. http://dx.doi.org/10.1177/0956797610379861. PMid:20713637.
McFarland DJ, McCane LM, David SV, Wolpaw JR. Spatial filter selection for EEG-based communication. Electroencephalography and Clinical Neurophysiology. 1997; 103(3):386-94. http://dx.doi.org/10.1016/S0013-4694(97)00022-2. PMid:9305287.
Mehta R, Zhu RJ. Blue or red? Exploring the effect of color on cognitive task performances. Science. 2009; 323(5918):1226-9. http://dx.doi.org/10.1126/science.1169144. PMid:19197022.
Moller AC, Elliot AJ, Maier MA. Basic hue-meaning associations. Emotion. 2009; 9(6):898-902. http://dx.doi.org/10.1037/a0017811. PMid:20001133.
Morgan ST, Hansen JC, Hillyard SA. Selective attention to stimulus location modulates the steady-state visual evoked potential. Proceedings of the National Academy of Sciences of the United States of America. 1996; 93(10):4770-4. http://dx.doi.org/10.1073/pnas.93.10.4770. PMid:8643478.
Pastor MA, Artieda J, Arbizu J, Valencia M, Masdeu JC. Human cerebral activation during steady-state visual-evoked responses. The Journal of Neuroscience. 2003; 23(37):11621-7. PMid:14684864.
Pomerleau VJ, Fortier-Gauthier U, Corriveau I, Dell’Acqua R, Jolicœur P. Colour-specific differences in attentional deployment for equiluminant pop-out colours: evidence from lateralised potentials. International Journal of Psychophysiology. 2014; 91(3):194-205. http://dx.doi.org/10.1016/j.ijpsycho.2013.10.016. PMid:24188915.
Regan D. An effect of stimulus colour on average steady-state potentials evoked in man. Nature. 1966; 210(5040):1056-7. http://dx.doi.org/10.1038/2101056a0. PMid:5914904.
Rubboli G, Parra J, Seri S, Takahashi T, Thomas P. EEG diagnostic procedures and special investigations in the assessment of photosensitivity. Epilepsia. 2004; 45(1 Suppl 1):35-9. http://dx.doi.org/10.1111/j.0013-9580.2004.451002.x. PMid:14706044.
Sammer G, Blecker C, Gebhardt H, Kirsch P, Stark R, Vaitl D. Acquisition of typical EEG waveforms during fMRI: SSVEP, LRP, and frontal theta. NeuroImage. 2005; 24(4):1012-24. http://dx.doi.org/10.1016/j.neuroimage.2004.10.026. PMid:15670678.
Tello RJMG, Muller SMT, Bastos TF Fo, Ferreira A. A comparison of techniques and technologies for SSVEP classification. In: IEEE-ISSNIP Biosignals and Biorobotics Conference: Biosignals and Robotics for Better and Safer Living (BRC); 2014; Salvador. IEEE; 2014a. p. 1-6. http://dx.doi.org/10.1109/BRC.2014.6880956.
Tello RJMG, Muller SMT, Bastos TF Fo, Ferreira A. Comparison of new techniques based on EMD for control of a SSVEP-BCI. In: IEEE 23rd International Symposium on Industrial Electronics (ISIE); 2014; Istanbul. IEEE; 2014b. p. 992-7. http://dx.doi.org/10.1109/ISIE.2014.6864747.
Tello RJMG, Muller SMT, Bastos TF Fo, Ferreira A. Comparison between wire and wireless EEG acquisition systems based on SSVEP in an independent-BCI. In: 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC’14). 2014c. p. 22-25. http://dx.doi.org/10.1109/EMBC.2014.6943519.
Tello RG, Pant JK, Müller SM, Krishnan S, Bastos TF Fo. An evaluation of performance for an independent SSVEP-BCI based on compressive sensing system. In: Jaffray DA. World Congress on Medical Physics and Biomedical Engineering; 2015 June 7-12; Toronto, Canada. Springer International Publishing; 2015. p. 982-5. (IFMBE Proceedings, 51). http://dx.doi.org/10.1007/978-3-319-19387-8_239.
Vialatte FB, Maurice M, Dauwels J, Cichocki A. Steady-state visually evoked potentials: focus on essential paradigms and future perspectives. Progress in Neurobiology. 2010; 90(4):418-38. http://dx.doi.org/10.1016/j.pneurobio.2009.11.005. PMid:19963032.
Wang Y, Wang R, Gao X, Hong B, Gao S. A practical VEP based brain-computer interface. IEEE Transactions on Neural Systems and Rehabilitation Engineering. 2006; 14(2):234-40. http://dx.doi.org/10.1109/TNSRE.2006.875576.
Wu Z, Lai Y, Xia Y, Wu D, Yao D. Stimulator selection in SSVEP-based BCI. Medical Engineering & Physics. 2008; 30(8):1079-88. http://dx.doi.org/10.1016/j.medengphy.2008.01.004. PMid:18316226.
Zhang Y, Wang R, Hong B, Gao X, Gao S. Source estimation of contrast-related perception based on frequency-tagged binocular rivalry. In: EMBS '06. 28th Annual International Conference of Engineering in Medicine and Biology Society; 2006; New York, NY. IEEE; 2006. p. 1177-80. http://dx.doi.org/10.1109/IEMBS.2006.260094.
Zhang Y, Xu P, Cheng K, Yao D. Multivariate synchronization index for frequency recognition of SSVEP-based brain-computer interface. Journal of Neuroscience Methods. 2014; 221(1):32-40. http://dx.doi.org/10.1016/j.jneumeth.2013.07.018. PMid:23928153.
Facebook
Google+
Twitter
LinkedIn
Mendeley
StumbleUpon
CiteULike
Reddit
Email