Source-Space Brain Functional Connectivity Features in Electroencephalogram-Based Driver Fatigue Classification
Abstract
:1. Introduction
2. Methods
2.1. General Structure
2.2. EEG Recordings and Pre-Processing
2.3. Feature Extraction: Source-Space FC Analysis
2.3.1. Source Localization
2.3.2. Parcellation of Source Vertices to ROIs
2.3.3. FC Estimation
2.3.4. Other Feature Extractors
2.4. Classification Alert vs. Fatigue
2.4.1. Feature Selection
2.4.2. Classification Algorithm
3. Results
3.1. Feature Selection
3.2. Effect of Fatigue on Critical Connections
3.3. Classification Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Thomas, M.J.W. Fatigue and Driving: An International Review. Appleton Inst. 2021. Available online: https://www.aaa.asn.au/wp-content/uploads/2021/10/Fatigue-Driving-Literature-Review-FINAL.pdf (accessed on 9 January 2023).
- Craig, A.; Tran, Y.; Wijesuriya, N.; Nguyen, H. Regional brain wave activity changes associated with fatigue. Psychophysiology 2012, 49, 574–582. [Google Scholar] [CrossRef] [PubMed]
- Chai, R.; Naik, G.R.; Nguyen, T.N.; Ling, S.H.; Tran, Y.; Craig, A.; Nguyen, H.T. Driver Fatigue Classification With Independent Component by Entropy Rate Bound Minimization Analysis in an EEG-Based System. IEEE J. Biomed. Health Inform. 2017, 21, 715–724. [Google Scholar] [CrossRef]
- Hu, S.; Zheng, G. Driver drowsiness detection with eyelid related parameters by Support Vector Machine. Expert Syst. Appl. 2009, 36, 7651–7658. [Google Scholar] [CrossRef]
- Tran, Y.; Wijesuriya, N.; Tarvainen, M.; Karjalainen, P.; Craig, A. The relationship between spectral changes in heart rate variability and fatigue. J. Psychophysiol. 2009, 23, 143–151. [Google Scholar] [CrossRef]
- Tran, Y.; Craig, A.; Craig, R.; Chai, R.; Nguyen, H. The influence of mental fatigue on brain activity: Evidence from a systematic review with meta-analyses. Psychophysiology 2020, 57, e13554. [Google Scholar] [CrossRef] [PubMed]
- Bose, R.; Wang, H.; Dragomir, A.; Thakor, N.V.; Bezerianos, A.; Li, J. Regression-Based Continuous Driving Fatigue Estimation: Toward Practical Implementation. IEEE Trans. Cogn. Dev. Syst. 2020, 12, 323–331. [Google Scholar] [CrossRef] [Green Version]
- Gurudath, N.; Riley, H.B. Drowsy Driving Detection by EEG Analysis Using Wavelet Transform and K-means Clustering. Procedia Comput. Sci. 2014, 34, 400–409. [Google Scholar] [CrossRef] [Green Version]
- Welch, P. The use of fast Fourier transform for the estimation of power spectra: A method based on time averaging over short, modified periodograms. IEEE Trans. Audio Electroacoust. 1967, 15, 70–73. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.-M.; Huang, Z.; Xia, Y. An adaptive multi-taper spectral estimation for stationary processes. Mech. Syst. Signal Process. 2023, 183, 109629. [Google Scholar] [CrossRef]
- Wang, H.; Liu, X.; Li, J.; Xu, T.; Bezerianos, A.; Sun, Y.; Wan, F. Driving Fatigue Recognition With Functional Connectivity Based on Phase Synchronization. IEEE Trans. Cogn. Dev. Syst. 2021, 13, 668–678. [Google Scholar] [CrossRef]
- Dimitrakopoulos, G.N.; Kakkos, I.; Vrahatis, A.G.; Sgarbas, K.; Li, J.; Sun, Y.; Bezerianos, A. Driving Mental Fatigue Classification Based on Brain Functional Connectivity. In Engineering Applications of Neural Networks, Proceedings of the 18th International Conference, EANN 2017, Athens, Greece, 25–27 August 2017; Boracchi, G., Iliadis, L., Jayne, C., Likas, A., Eds.; Springer International Publishing: Cham, Switzerland, 2017; pp. 465–474. [Google Scholar]
- Harvy, J.; Thakor, N.; Bezerianos, A.; Li, J. Between-Frequency Topographical and Dynamic High-Order Functional Connectivity for Driving Drowsiness Assessment. IEEE Trans. Neural Syst. Rehabil. Eng. 2019, 27, 358–367. [Google Scholar] [CrossRef] [PubMed]
- Bastos, A.M.; Schoffelen, J.-M. A Tutorial Review of Functional Connectivity Analysis Methods and Their Interpretational Pitfalls. Front. Syst. Neurosci. 2016, 9, 175. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanchez Bornot, J.M.; Wong-Lin, K.; Ahmad, A.L.; Prasad, G. Robust EEG/MEG Based Functional Connectivity with the Envelope of the Imaginary Coherence: Sensor Space Analysis. Brain Topogr. 2018, 31, 895–916. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Park, H.-J.; Friston, K.J. Structural and Functional Brain Networks: From Connections to Cognition. Science 2013, 342, 1238411. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stam, C.J.; Jones, B.F.; Manshanden, I.; van Cappellen van Walsum, A.M.; Montez, T.; Verbunt, J.P.A.; de Munck, J.C.; van Dijk, B.W.; Berendse, H.W.; Scheltens, P. Magnetoencephalographic evaluation of resting-state functional connectivity in Alzheimer’s disease. NeuroImage 2006, 32, 1335–1344. [Google Scholar] [CrossRef]
- Keeser, D.; Karch, S.; Davis, J.R.; Surmeli, T.; Engelbregt, H.; Länger, A.; Chrobok, A.; Loy, F.; Minton, B.; Thatcher, R.; et al. Changes of resting-state EEG and functional connectivity in the sensor and source space of patients with major depression. Klin. Neurophysiol. 2013, 44, P142. [Google Scholar] [CrossRef] [Green Version]
- van den Broek, S.P.; Reinders, F.; Donderwinkel, M.; Peters, M.J. Volume conduction effects in EEG and MEG. Electroencephalogr. Clin. Neurophysiol. 1998, 106, 522–534. [Google Scholar] [CrossRef]
- Schoffelen, J.-M.; Gross, J. Source connectivity analysis with MEG and EEG. Hum. Brain Mapp. 2009, 30, 1857–1865. [Google Scholar] [CrossRef]
- Xie, W.; Toll, R.T.; Nelson, C.A. EEG functional connectivity analysis in the source space. Dev. Cogn. Neurosci. 2022, 56, 101119. [Google Scholar] [CrossRef]
- Knyazeva, M.G.; Carmeli, C.; Khadivi, A.; Ghika, J.; Meuli, R.; Frackowiak, R.S. Evolution of source EEG synchronization in early Alzheimer’s disease. Neurobiol. Aging 2013, 34, 694–705. [Google Scholar] [CrossRef]
- Li, W.; Li, Y.; Zhu, W.; Chen, X. Changes in brain functional network connectivity after stroke. Neural Regen. Res. 2014, 9, 51–60. [Google Scholar] [CrossRef] [PubMed]
- Craig, A.; Tran, Y.; Wijesuriya, N.; Boord, P. A controlled investigation into the psychological determinants of fatigue. Biol. Psychol. 2006, 72, 78–87. [Google Scholar] [CrossRef] [PubMed]
- Bear, M.F. Neuroscience: Exploring the Brain, 4th ed.; Wolters Kluwer: Philadelphia, PA, USA, 2016. [Google Scholar]
- Shahid, A.; Wilkinson, K.; Marcu, S.; Shapiro, C. Stanford Sleepiness Scale (SSS). In STOP, THAT and One Hundred Other Sleep Scales; Springer Science & Business Media: Berlin, Germany, 2011; pp. 369–370. [Google Scholar]
- Sharbrough, F.C.G.E. American Electroencephalographic Society Guidelines for Standard Electrode Position Nomenclature. J. Clin. Neurophysiol. 1991, 8, 200–202. [Google Scholar]
- Gramfort, A.; Luessi, M.; Larson, E.; Engemann, D.; Strohmeier, D.; Brodbeck, C.; Goj, R.; Jas, M.; Brooks, T.; Parkkonen, L.; et al. MEG and EEG data analysis with MNE-Python. Front. Neurosci. 2013, 7, 267. [Google Scholar] [CrossRef] [Green Version]
- Fuchs, M.; Drenckhahn, R.; Wischmann, H.A.; Wagner, M. An improved boundary element method for realistic volume-conductor modeling. IEEE Trans. Biomed. Eng. 1998, 45, 980–997. [Google Scholar] [CrossRef]
- Vatta, F.; Meneghini, F.; Esposito, F.; Mininel, S.; Di Salle, F. Realistic and spherical head modeling for EEG forward problem solution: A comparative cortex-based analysis. Comput. Intell. Neurosci. 2010, 2010, 972060. [Google Scholar] [CrossRef]
- Hämäläinen, M.; Hari, R.; Ilmoniemi, R.J.; Knuutila, J.; Lounasmaa, O.V. Magnetoencephalography—theory, instrumentation, and applications to noninvasive studies of the working human brain. Rev. Mod. Phys. 1993, 65, 413–497. [Google Scholar] [CrossRef] [Green Version]
- Pascual-Marqui, R.D. Standardized low-resolution brain electromagnetic tomography (sLORETA): Technical details. Methods Find. Exp. Clin. Pharmacol. 2002, 24 (Suppl. D), 5–12. [Google Scholar]
- Dale, A.M.; Liu, A.K.; Fischl, B.R.; Buckner, R.L.; Belliveau, J.W.; Lewine, J.D.; Halgren, E. Dynamic statistical parametric mapping: Combining fMRI and MEG for high-resolution imaging of cortical activity. Neuron 2000, 26, 55–67. [Google Scholar] [CrossRef] [Green Version]
- Grech, R.; Cassar, T.; Muscat, J.; Camilleri, K.P.; Fabri, S.G.; Zervakis, M.; Xanthopoulos, P.; Sakkalis, V.; Vanrumste, B. Review on solving the inverse problem in EEG source analysis. J. NeuroEngineering Rehabil. 2008, 5, 25. [Google Scholar] [CrossRef] [Green Version]
- Vogt, B.A.; Berger, G.R.; Derbyshire, S.W. Structural and functional dichotomy of human midcingulate cortex. Eur. J. Neurosci. 2003, 18, 3134–3144. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vogt, B.A.; Vogt, L.; Laureys, S. Cytology and functionally correlated circuits of human posterior cingulate areas. Neuroimage 2006, 29, 452–466. [Google Scholar] [CrossRef] [Green Version]
- Bastos, A.M.; Vezoli, J.; Fries, P. Communication through coherence with inter-areal delays. Curr. Opin. Neurobiol. 2015, 31, 173–180. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Preti, M.G.; Bolton, T.A.W.; Van De Ville, D. The dynamic functional connectome: State-of-the-art and perspectives. NeuroImage 2017, 160, 41–54. [Google Scholar] [CrossRef] [PubMed]
- Rizkallah, J.; Annen, J.; Modolo, J.; Gosseries, O.; Benquet, P.; Mortaheb, S.; Amoud, H.; Cassol, H.; Mheich, A.; Thibaut, A.; et al. Decreased integration of EEG source-space networks in disorders of consciousness. NeuroImage Clin. 2019, 23, 101841. [Google Scholar] [CrossRef] [PubMed]
- Ying, X. An Overview of Overfitting and its Solutions. J. Phys. Conf. Ser. 2019, 1168, 022022. [Google Scholar] [CrossRef]
- Guyon, I.; Weston, J.; Barnhill, S.; Vapnik, V. Gene Selection for Cancer Classification using Support Vector Machines. Mach. Learn. 2002, 46, 389–422. [Google Scholar] [CrossRef]
- Hearst, M.A.; Dumais, S.T.; Osuna, E.; Platt, J.; Scholkopf, B. Support vector machines. IEEE Intell. Syst. Appl. 1998, 13, 18–28. [Google Scholar] [CrossRef] [Green Version]
- Viitaniemi, V.; Sjöberg, M.; Koskela, M.; Ishikawa, S.; Laaksonen, J. Chapter 12—Advances in visual concept detection: Ten years of TRECVID. In Advances in Independent Component Analysis and Learning Machines; Bingham, E., Kaski, S., Laaksonen, J., Lampinen, J., Eds.; Academic Press: Cambridge, MA, USA, 2015; pp. 249–278. [Google Scholar]
- Zhang, Y.; Wang, H.; Mao, J.; Xu, Z.-D.; Zhang, Y.-F. Probabilistic Framework with Bayesian Optimization for Predicting Typhoon-Induced Dynamic Responses of a Long-Span Bridge. J. Struct. Eng. 2021, 147, 04020297. [Google Scholar] [CrossRef]
- Bergstra, J.; Bengio, Y. Random Search for Hyper-Parameter Optimization. J. Mach. Learn. Res. 2012, 13, 281–305. [Google Scholar]
- Kakkos, I.; Dimitrakopoulos, G.N.; Gao, L.; Zhang, Y.; Qi, P.; Matsopoulos, G.K.; Thakor, N.; Bezerianos, A.; Sun, Y. Mental Workload Drives Different Reorganizations of Functional Cortical Connectivity Between 2D and 3D Simulated Flight Experiments. IEEE Trans. Neural. Syst. Rehabil. Eng. 2019, 27, 1704–1713. [Google Scholar] [CrossRef] [PubMed]
- Golland, P.; Liang, F.; Mukherjee, S.; Panchenko, D. Permutation Tests for Classification. In Learning Theory, Proceedings of the 18th Annual Conference on Learning Theory, COLT 2005, Bertinoro, Italy, 27–30 June 2005; Auer, P., Meir, R., Eds.; Springer: Berlin/Heidelberg, Germany, 2005; pp. 501–515. [Google Scholar]
- Perera, D.; Wang, Y.K.; Lin, C.T.; Nguyen, H.; Chai, R. Improving EEG-Based Driver Distraction Classification Using Brain Connectivity Estimators. Sensors 2022, 22, 6230. [Google Scholar] [CrossRef]
- Hag, A.; Handayani, D.; Pillai, T.; Mantoro, T.; Kit, M.H.; Al-Shargie, F. EEG Mental Stress Assessment Using Hybrid Multi-Domain Feature Sets of Functional Connectivity Network and Time-Frequency Features. Sensors 2021, 21, 6300. [Google Scholar] [CrossRef] [PubMed]
- van den Heuvel, M.P.; Sporns, O. Network hubs in the human brain. Trends Cogn. Sci. 2013, 17, 683–696. [Google Scholar] [CrossRef] [PubMed]
- Cao, T.; Wan, F.; Wong, C.M.; da Cruz, J.N.; Hu, Y. Objective evaluation of fatigue by EEG spectral analysis in steady-state visual evoked potential-based brain-computer interfaces. Biomed. Eng. Online 2014, 13, 28. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ahmadi, A.; Bazregarzadeh, H.; Kazemi, K. Automated detection of driver fatigue from electroencephalography through wavelet-based connectivity. Biocybern. Biomed. Eng. 2021, 41, 316–332. [Google Scholar] [CrossRef]
- Zhao, C.; Zhao, M.; Liu, J.; Zheng, C. Electroencephalogram and electrocardiograph assessment of mental fatigue in a driving simulator. Accid. Anal. Prev. 2012, 45, 83–90. [Google Scholar] [CrossRef] [PubMed]
- Clayton, M.S.; Yeung, N.; Cohen Kadosh, R. The roles of cortical oscillations in sustained attention. Trends Cogn. Sci. 2015, 19, 188–195. [Google Scholar] [CrossRef]
- Ishii, A.; Tanaka, M.; Watanabe, Y. The Neural Mechanisms Underlying the Decision to Rest in the Presence of Fatigue: A Magnetoencephalography Study. PLoS ONE 2014, 9, e109740. [Google Scholar] [CrossRef]
- Kong, W.; Zhou, Z.; Jiang, B.; Babiloni, F.; Borghini, G. Assessment of driving fatigue based on intra/inter-region phase synchronization. Neurocomputing 2017, 219, 474–482. [Google Scholar] [CrossRef]
EEG Band | Average Results of 1000 Classification Iterations | |||
---|---|---|---|---|
Sens | Spec | Acc | p-Value | |
Delta (0.5–4 Hz) | 88% | 88% | 88% | <0.001 |
Theta (4–7 Hz) | 90% | 91% | 90% | <0.001 |
Alpha (8–12 Hz) | 88% | 67% | 77% | <0.001 |
Beta (13–30 Hz) | 94% | 93% | 93% | <0.001 |
Gamma (32–45 Hz) | 83% | 92% | 88% | <0.001 |
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Nguyen, K.H.; Ebbatson, M.; Tran, Y.; Craig, A.; Nguyen, H.; Chai, R. Source-Space Brain Functional Connectivity Features in Electroencephalogram-Based Driver Fatigue Classification. Sensors 2023, 23, 2383. https://doi.org/10.3390/s23052383
Nguyen KH, Ebbatson M, Tran Y, Craig A, Nguyen H, Chai R. Source-Space Brain Functional Connectivity Features in Electroencephalogram-Based Driver Fatigue Classification. Sensors. 2023; 23(5):2383. https://doi.org/10.3390/s23052383
Chicago/Turabian StyleNguyen, Khanh Ha, Matthew Ebbatson, Yvonne Tran, Ashley Craig, Hung Nguyen, and Rifai Chai. 2023. "Source-Space Brain Functional Connectivity Features in Electroencephalogram-Based Driver Fatigue Classification" Sensors 23, no. 5: 2383. https://doi.org/10.3390/s23052383