Abstract
Mental stress has been identified as one of the major contributing factors that leads to various diseases such as heart attack, depression, and stroke. To avoid this, stress quantification is important for clinical intervention and disease prevention. This study aims to investigate the feasibility of exploiting electroencephalography (EEG) signals to discriminate between different stress levels. We propose a new assessment protocol whereby the stress level is represented by the complexity of mental arithmetic (MA) task for example, at three levels of difficulty, and the stressors are time pressure and negative feedback. Using 18-male subjects, the experimental results showed that there were significant differences in EEG response between the control and stress conditions at different levels of MA task with p values < 0.001. Furthermore, we found a significant reduction in alpha rhythm power from one stress level to another level, p values < 0.05. In comparison, results from self-reporting questionnaire NASA-TLX approach showed no significant differences between stress levels. In addition, we developed a discriminant analysis method based on multiclass support vector machine (SVM) with error-correcting output code (ECOC). Different stress levels were detected with an average classification accuracy of 94.79%. The lateral index (LI) results further showed dominant right prefrontal cortex (PFC) to mental stress (reduced alpha rhythm). The study demonstrated the feasibility of using EEG in classifying multilevel mental stress and reported alpha rhythm power at right prefrontal cortex as a suitable index.
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Al-shargie F, Tang T, Badruddin N, Kiguchi M (2016) Mental stress quantification using EEG signals. In: Ibrahim F, Usman J, Mohtar M, Ahmad M (eds) International Conference for Innovation in Biomedical Engineering and Life Sciences. IFMBE Proceedings, vol 56. Springer, Singapore, pp 15–19
Alonso J, Romero S, Ballester M, Antonijoan R, Mañanas M (2015) Stress assessment based on EEG univariate features and functional connectivity measures. Physiol Meas 36:1351
Arnsten AF (2009) Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10:410–422
Bagwath Persad L (2011) Energy drinks and the neurophysiological impact of caffeine. Front Neurosci 5:116
Berka C, Levendowski DJ, Cvetinovic MM, Petrovic MM, Davis G, Lumicao MN, Zivkovic VT, Popovic MV, Olmstead R (2004) Real-time analysis of EEG indexes of alertness, cognition, and memory acquired with a wireless EEG headset. Int J Hum Comput Interact 17:151–170
Bosch JA, Brand HS, Ligtenberg TJ, Bermond B, Hoogstraten J, Amerongen AVN (1996) Psychological stress as a determinant of protein levels and salivary-induced aggregation of Streptococcus gordonii in human whole saliva. Psychosom Med 58:374–382
Bosch JA, de Geus EJ, Veerman EC, Hoogstraten J, Amerongen AVN (2003) Innate secretory immunity in response to laboratory stressors that evoke distinct patterns of cardiac autonomic activity. Psychosom Med 65:245–258
Brouwer A-M, Hogervorst MA, Holewijn M, van Erp JB (2014) Evidence for effects of task difficulty but not learning on neurophysiological variables associated with effort. Int J Psychophysiol 93:242–252
Brouwer A-M, Hogervorst MA, Van Erp JB, Heffelaar T, Zimmerman PH, Oostenveld R (2012) Estimating workload using EEG spectral power and ERPs in the n-back task. J Neural Eng 9:045008
Chanel G, Ansari-Asl K, Pun T (2007) Valence-arousal evaluation using physiological signals in an emotion recall paradigm. In: Systems, man and cybernetics. ISIC. IEEE, pp 2662–2667
Chanel G, Kierkels JJ, Soleymani M, Pun T (2009) Short-term emotion assessment in a recall paradigm. Int J Hum Comput Stud 67:607–627
Chanel G, Kronegg J, Grandjean D, Pun T (2006) Emotion assessment: arousal evaluation using EEG’s and peripheral physiological signals. In: Gunsel B, Jain AK, Tekalp AM, Sankur B (eds) Multimedia content representation, classification and security. MRCS 2006. Lecture Notes in Computer Science, vol 4105. Springer, Berlin, Heidelberg, pp 530–537
Chapin TJ, Russell-Chapin LA (2013) Neurotherapy and neurofeedback: brain-based treatment for psychological and behavioral problems. Routledge, pp 95–105. https://doi.org/10.4324/9780203072523
Choi Y, Kim M, Chun C (2015) Measurement of occupants’ stress based on electroencephalograms (EEG) in twelve combined environments. Build Environ 88:65–72
Cohen S, Janicki-Deverts D, Miller GE (2007) Psychological stress and disease. JAMA Intern Med 298:1685–1687
Curran T (1999) The electrophysiology of incidental and intentional retrieval: erp old/ new effects in lexical decision and recognition memory. Neuropsychologia 37:771–785
Dedovic K, Renwick R, Mahani NK, Engert V, Lupien SJ, Pruessner JC (2005) The Montreal Imaging Stress Task: using functional imaging to investigate the effects of perceiving and processing psychosocial stress in the human brain. J Psychiatry Neurosci 30:319
Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21
Dietterich TG, Bakiri G (1995) Solving multiclass learning problems via error-correcting output codes. J Artif Intell Res 2:263–286
Doi H, Nishitani S, Shinohara K (2013) NIRS as a tool for assaying emotional function in the prefrontal cortex. Front Hum Neurosci 7:770. https://doi.org/10.3389/fnhum.2013.00770
Edwards W (2010) Motor learning and control: from theory to practice. Cengage Learning
Engert V, Vogel S, Efanov SI, Duchesne A, Corbo V, Ali N, Pruessner JC (2011) Investigation into the cross-correlation of salivary cortisol and alpha-amylase responses to psychological stress. Psychoneuroendocrinology 36:1294–1302
Eysenck HJ (2012) A model for personality. Springer Science and Business Media 1:17–20
Fawcett T (2006) An introduction to ROC analysis. Pattern Recogn Lett 27:861–874
Ferree TC, Luu P, Russell GS, Tucker DM (2001) Scalp electrode impedance, infection risk, and EEG data quality. Clin Neurophysiol 112:536–544
Fink A, Grabner R, Neuper C, Neubauer A (2005) EEG alpha band dissociation with increasing task demands. Cogn Brain Res 24:252–259
Gärtner M, Grimm S, Bajbouj M (2015) Frontal midline theta oscillations during mental arithmetic: effects of stress. Front Behav Neurosci 9. https://doi.org/10.3389/fnbeh.2015.00096
Gärtner M, Rohde-Liebenau L, Grimm S, Bajbouj M (2014) Working memory-related frontal theta activity is decreased under acute stress. Psychoneuroendocrinology 43:105–113
Gordis EB, Granger DA, Susman EJ, Trickett PK (2006) Asymmetry between salivary cortisol and α-amylase reactivity to stress: relation to aggressive behavior in adolescents. Psychoneuroendocrinology 31:976–987
Granger DA, Kivlighan KT, El-Sheikh M, Gordis EB, Stroud LR (2007) Salivary α-amylase in biobehavioral research. Ann N Y Acad Sci 1098:122–144
Gray JR, Burgess GC, Schaefer A, Yarkoni T, Larsen RJ, Braver TS (2005) Affective personality differences in neural processing efficiency confirmed using fMRI. Cog Affect Behav Neurosci 5:182–190
Grillon C, Duncko R, Covington MF, Kopperman L, Kling MA (2007) Acute stress potentiates anxiety in humans. Biol Psychiatry 62:1183–1186
Hanrahan K, McCarthy AM, Kleiber C, Lutgendorf S, Tsalikian E (2006) Strategies for salivary cortisol collection and analysis in research with children. Appl Nurs Res 19:95–101
Hari R, Salmelin R (2012) Magnetoencephalography: from SQUIDs to neuroscience: neuroimage 20th anniversary special edition. NeuroImage 61:386–396
Harmony T, Fernández T, Silva J, Bernal J, Díaz-Comas L, Reyes A, Marosi E, Rodríguez M, Rodríguez M (1996) EEG delta activity: an indicator of attention to internal processing during performance of mental tasks. Int J Psychophysiol 24:161–171
Harrison AH, Connolly JF (2013) Finding a way in: a review and practical evaluation of fMRI and EEG for detection and assessment in disorders of consciousness. Neurosci Biobehav Rev 37:1403–1419
Hart SG, Staveland LE (1988) Development of NASA-TLX (Task Load Index): results of empirical and theoretical research. Adv Psychol 52:139–183
Hellhammer DH, Wüst S, Kudielka BM (2009) Salivary cortisol as a biomarker in stress research. Psychoneuroendocrinology 34:163–171
Herman JP, Ostrander MM, Mueller NK, Figueiredo H (2005) Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuro-Psychopharmacol Biol Psychiatry 29:1201–1213
Hill RW, Castro E (2009) Healing young brains: the neurofeedback solution. Hampton Roads Publishing, Charlottesville
Hogervorst MA, Brouwer A-M, van Erp JB (2015) Combining and comparing EEG, peripheral physiology and eye-related measures for the assessment of mental workload. Front Neurosci 8:322
Hombergh P, Künzi B, Elwyn G, Doremalen J, Akkermans R, Grol R, Wensing M (2009) High workload and job stress are associated with lower practice performance in general practice: an observational study in 239 general practices in the Netherlands. BMC Health Serv Res 9:118. https://doi.org/10.1186/1472-6963-9-118
Hoshi Y, Tamura M (1993) Detection of dynamic changes in cerebral oxygenation coupled to neuronal function during mental work in man. Neurosci Lett 150:5–8
Hosseini SA, Khalilzadeh MA (2010) Emotional stress recognition system using EEG and psychophysiological signals: using new labelling process of EEG signals in emotional stress state. In: 2010 International Conference on Biomedical Engineering and Computer Science (ICBECS), Wuhan, China, pp 1–6
Hwang MI (1994) Decision making under time pressure: a model for information systems research. Inf Manag 27:197–203
Ishikawa W, Sato M, Fukuda Y, Matsumoto T, Takemura N, Sakatani K (2014) Correlation between asymmetry of spontaneous oscillation of hemodynamic changes in the prefrontal cortex and anxiety levels: a near-infrared spectroscopy study. J Biomed Opt 19:027005. https://doi.org/10.1117/1.JBO.19.2.027005
Ishino K, Hagiwara M (2003) A feeling estimation system using a simple electroencephalograph. In: Systems, man and cybernetics. IEEE, pp 4204–4209
Joëls M, Karst H, Alfarez D, Heine VM, Qin Y, Ev R, Verkuyl M, Lucassen PJ, Krugers HJ (2004) Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress Int J Biol Stress 7:221–231
Jun G, Smitha K (2016) EEG based stress level identification. In: IEEE proc. systems, man, and cybernetics (SMC), pp 003270–003274
Kappenman ES, Luck SJ (2010) The effects of electrode impedance on data quality and statistical significance in ERP recordings. Psychophysiology 47:888–904
Khosrowabadi R, Quek C, Ang KK, Tung SW, Heijnen MA (2011) Brain-computer interface for classifying EEG correlates of chronic mental stress. In: Neural networks (IJCNN). IEEE, pp 757–762
Khushaba RN, Kodagoda S, Lal S, Dissanayake G (2011) Driver drowsiness classification using fuzzy wavelet-packet-based feature-extraction algorithm. IEEE Trans Biomed Eng 58:121–131
Kirschbaum C, Hellhammer DH (1994) Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 19:313–333
Koibuchi E, Suzuki Y (2014) Exercise upregulates salivary amylase in humans (review). Exp Ther Med 7:773–777
Lewis RS, Weekes NY, Wang TH (2007) The effect of a naturalistic stressor on frontal EEG asymmetry, stress, and health. Biol Psychol 75:239–247
Lin C-T, Lin K-L, Ko L-W, Liang S-F, Kuo B-C, Chung I-F (2008) Nonparametric single-trial EEG feature extraction and classification of driver’s cognitive responses. EURASIP J Adv Signal Process 2008:1–10
Liu T-K, Chen Y-P, Hou Z-Y, Wang C-C, Chou J-H (2014) Noninvasive evaluation of mental stress using by a refined rough set technique based on biomedical signals. Artf Intell Med 61:97–103
Lotte F, Congedo M, Lécuyer A, Lamarche F, Arnaldi B (2007) A review of classification algorithms for EEG-based brain–computer interfaces. J Neural Eng 4:R1
Masuda M, Holmes TH (1967) The social readjustment rating scale: a cross-cultural study of Japanese and Americans. J Psychosom Res 11:227–237
McEwen BS (2005) Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 54:20–23
McEwen BS (2008) Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol 583:174–185
Michel CM, Murray MM (2012) Towards the utilization of EEG as a brain imaging tool. NeuroImage 61:371–385
Michels N, Sioen I, Braet C, Huybrechts I, Vanaelst B, Wolters M, De Henauw S (2013) Relation between salivary cortisol as stress biomarker and dietary pattern in children. Psychoneuroendocrinology 38:1512–1520
Nater UM, La Marca R, Florin L, Moses A, Langhans W, Koller MM, Ehlert U (2006) Stress-induced changes in human salivary alpha-amylase activity—associations with adrenergic activity. Psychoneuroendocrinology 31:49–58
Noto Y, Sato T, Kudo M, Kurata K, Hirota K (2005) The relationship between salivary biomarkers and state-trait anxiety inventory score under mental arithmetic stress: a pilot study. Anesth Analg 101:1873–1876
Ossewaarde L, Qin S, Van Marle HJ, van Wingen GA, Fernández G, Hermans EJ (2011) Stress-induced reduction in reward-related prefrontal cortex function. NeuroImage 55:345–352
Peng H, Hu B, Zheng F, Fan D, Zhao W, Chen X, Yang Y, Cai Q (2013) A method of identifying chronic stress by EEG. Pers Ubiquit Comput 17:1341–1347
Pruessner JC, Dedovic K, Pruessner M, Lord C, Buss C, Collins L, Dagher A, Lupien SJ (2010) Stress regulation in the central nervous system: evidence from structural and functional neuroimaging studies in human populations-2008 Curt Richter Award Winner. Psychoneuroendocrinology 35:179–191
Puterman E, O’Donovan A, Adler NE, Tomiyama AJ, Kemeny M, Wolkowitz OM, Epel E (2011) Physical activity moderates stressor-induced rumination on cortisol reactivity. Psychosom Med 73:604
Qin S, Hermans EJ, van Marle HJ, Luo J, Fernández G (2009) Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biol Psychiatry 66:25–32
Rahnuma KS, Wahab A, Kamaruddin N, Majid H (2011) EEG analysis for understanding stress based on affective model basis function. In: 2011 I.E. International Symposium on Consumer Electronics (ISCE), pp 592–597. https://doi.org/10.1109/ISCE.2011.5973899
Reinhardt T, Schmahl C, Wüst S, Bohus M (2012) Salivary cortisol, heart rate, electrodermal activity and subjective stress responses to the Mannheim Multicomponent Stress Test (MMST). Psychiatry Res 198:106–111
Robles TF, Shetty V, Zigler CM, Glover DA, Elashoff D, Murphy D, Yamaguchi M (2011) The feasibility of ambulatory biosensor measurement of salivary alpha amylase: relationships with self-reported and naturalistic psychological stress. Biol Psychol 86:50–56
Ryu K, Myung R (2005) Evaluation of mental workload with a combined measure based on physiological indices during a dual task of tracking and mental arithmetic. Int J Ind Ergonom 35:991–1009
Saidatul A, Paulraj MP, Yaacob S, Yusnita MA (2011) Analysis of EEG signals during relaxation and mental stress condition using AR modeling techniques. In: 2011 I.E. International Conference on Control system, computing and engineering (ICCSCE), pp 477–481. https://doi.org/10.1109/ICCSCE.2011.6190573
Selye H (1965) The stress syndrome. Am J Nurs 65:97–99
Seo S-H, Lee J-T (2010) Stress and EEG. INTECH Open Access Publisher
Sharma N, Gedeon T (2013) Modeling stress recognition in typical virtual environments. In: 2013 International Conference on Pervasive Computing Technologies for Healthcare (PervasiveHealth), Venice, Italy, pp 17–24
Skosnik PD, Chatterton RT, Swisher T, Park S (2000) Modulation of attentional inhibition by norepinephrine and cortisol after psychological stress. Int J Psychophysiol 36:59–68
Steptoe A, Kivimäki M (2012) Stress and cardiovascular disease. Nat Rev Cardiol 9:360–370
Takizawa R, Nishimura Y, Yamasue H, Kasai K (2014) Anxiety and performance: the disparate roles of prefrontal subregions under maintained psychological stress. Cereb Cortex 24:1858–1866
Thompson M, Thompson L (2007) Neurofeedback for stress management. Princs Pract Stress Manag 3:249–287
Tong Y (2010) Time lag dependent multimodal processing of concurrent fMRI and near-infrared spectroscopy (NIRS) data suggests a global circulatory origin for low-frequency oscillation signals in human brain. NeuroImage 53:553–564
Tran Y, Thuraisingham R, Wijesuriya N, Nguyen H, Craig A (2007) Detecting neural changes during stress and fatigue effectively: a comparison of spectral analysis and sample entropy. In: IEEE/EMBS Conference on Neural Engineering, pp 350–353. https://doi.org/10.1109/CNE.2007.369682
Uylings H, Van Eden C, De Bruin J, Feenstra M, Pennartz C (2000) The integration of stress by the hypothalamus, amygdala and prefrontal cortex: balance between the autonomic nervous system and the neuroendocrine system. Prog Brain Res 126:117–132
van der Werff SJ, van den Berg SM, Pannekoek JN, Elzinga BM, Van Der Wee NJ (2013) Neuroimaging resilience to stress: a review. Front Behav Neurosci 7:32. https://doi.org/10.3389/fnbeh.2013.00039
Vapnik VN, Vapnik V (1998) Statistical learning theory vol 1 Wiley New York
Wang J, Rao H, Wetmore GS, Furlan PM, Korczykowski M, Dinges DF, Detre JA (2005) Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. Proc Natl Acad Sci U S A 102:17804–17809
Yamaguchi M, Kanemori T, Kanemaru M, Takai N, Mizuno Y, Yoshida H (2004) Performance evaluation of salivary amylase activity monitor. Biosens Bioelectron 20:491–497
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This research is funded by the Ministry of Education, Malaysia under Higher Institution Centre of Excellence (HiCOE) scheme.
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Al-shargie, F., Tang, T.B., Badruddin, N. et al. Towards multilevel mental stress assessment using SVM with ECOC: an EEG approach. Med Biol Eng Comput 56, 125–136 (2018). https://doi.org/10.1007/s11517-017-1733-8
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DOI: https://doi.org/10.1007/s11517-017-1733-8