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Blood-brain barrier permeability changes: nonlinear analysis of ECoG based on wavelet and machine learning approaches

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Abstract

The blood-brain barrier plays a decisive role in protecting the brain from toxins and pathogens. The ability to analyze the BBB opening (OBBB) is crucial for the treatment of many brain diseases, but it is very difficult to noninvasively monitor OBBB. In this paper we analyze the EEG series of healthy rats in free behaviour and after music-induced OBBB. The research is performed using two completely different methods based on wavelet analysis and machine learning approach. The wavelet-approach demonstrates quantitative changes in the oscillatory structure in EEG signals after music listening, namely, a decrease in the number of patterns to the frequency band \(\varDelta f [1; 2.5] \) Hz. Using methods of machine learning we analyze the number of fragments of EEG realizations recognized as OBBB. After the music impact the number of recognized OBBB is increased in about 50%. Both methods enable us to recognize OBBB and are in a good agreement with each other. The comparative analysis was carried out using F-measures and ROC-curves.

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References

  1. N. Abbott, Dynamics of cns barriers: evolution, differentiation, and modulation. Cell. Mol. Neurobiol. 25, 5–23 (2005)

    Article  Google Scholar 

  2. N. Abbott, A.A. Patabendige, D.E. Dolman, S. Yusof, D. Begley, Structure and function of the blood-brain barrier. Neurobiol. Dis. 37, 13–25 (2010)

    Article  Google Scholar 

  3. N. Abbott, L. Rönnbäck, L. Hansson, Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41–53 (2006)

    Article  Google Scholar 

  4. H. Adeli, Z. Zhou, N. Dadmeh, Analysis of EEG records in an epileptic patient using wavelet transform. J. Neurosci. Methods 123(1), 69–87 (2003). https://doi.org/10.1016/s0165-0270(02)00340-0

  5. U. Albus, Guide for the care and use of laboratory animals (8th edn). Lab. Anim. 46, 267–268 (2012)

    Article  Google Scholar 

  6. A. Aouinet, C. Adnane, Electrocardiogram denoised signal by discrete wavelet transform and continuous wavelet transform. Signal Process. Int. J. 8(1), 1 (2014)

    Google Scholar 

  7. V. Bajaj, R. Pachori, Automatic classification of sleep stages based on the time-frequency image of eeg signals. Comput. Methods Programs Biomed. 112(3), 320–328 (2013)

    Article  Google Scholar 

  8. P. Cavalier, D. O’Hagan, Maximum wavelet coefficient points for potential field analysis and inversion. In: International conference on engineering geophysics, Al Ain, United Arab Emirates, 9-12 October 2017, pp. 128–131. Society of Exploration Geophysicists (2017)

  9. Y. Chassidim, R. Veksler, S. Lublinsky, G. Pell, A. Friedman, I. Shelef, Quantitative imaging assessment of blood-brain barrier permeability in humans. Fluids Barriers CNS 10(1), 9 (2013)

    Article  Google Scholar 

  10. F. Chollet et al. Keras. GitHub (2015). https://github.com/fchollet/keras

  11. C. Davatzikos, K. Ruparel, Y. Fan, D. Shen, M. Acharyya, J. Loughead, R. Gur, D. Langleben, Classifying spatial patterns of brain activity with machine learning methods: application to lie detection. NeuroImage 28(3), 663–668 (2005) https://doi.org/10.1016/j.neuroimage.2005.08.009. http://www.sciencedirect.com/science/article/pii/S1053811905005914

  12. E.C. Djamal, R.D. Putra, Brain-computer interface of focus and motor imagery using wavelet and recurrent neural networks. TELKOMNIKA Telecommun. Comput. Electron. Control 18(4), 2748–2756 (2020)

    Google Scholar 

  13. I. Elbeshlawi, M.S. AbdelBaki, Safety of gadolinium administration in children. Pediatr. Neurol. 86, 27–32 (2018)

    Article  Google Scholar 

  14. B. Everitt, The Cambridge dictionary of statistics (Cambridge University Press, Cambridge, 1998)

    MATH  Google Scholar 

  15. T. Fawcett, An introduction to roc analysis. Pattern Recogn. Lett. 27, 861–874 (2006)

    Article  ADS  Google Scholar 

  16. Q. Feng, M. Zhang, Y. Zhang, N. Jiang, J. Zhang, Multi-scale representation of sleep electroencephalogram events for healthy adult using wavelet transformation. J. Med. Imaging Health Inf. 7(5), 928–933 (2017)

    Article  Google Scholar 

  17. E. Fernandez-Blanco, D. Rivero, A. Pazos, Eeg signal processing with separable convolutional neural network for automatic scoring of sleeping stage. Neurocomputing 410, 220–228 (2020)

    Article  Google Scholar 

  18. V. Grubov, V. Musatov, V. Maksimenko, A. Pisarchik, A. Runnova, A. Hramov, Development of intelligent system for classification of multiple human brain states corresponding to different real and imaginary movements. Cybern. Phys. 6, 103–107 (2017)

    Google Scholar 

  19. V. Grubov, A. Runnova, M. Zhuravlev, V. Maksimenko, S. Pchelintseva, A. Pisarchik, Perception of multistable images: Eeg studies. Cybern. Phys. 6, 108–113 (2017)

    Google Scholar 

  20. A. Hassan, S. Bashar, M. Bhuiyan, On the classification of sleep states by means of statistical and spectral features from single channel electroencephalogram. In: International conference on advances in computing, communications and informatics (ICACCI), pp. 2238–2243 (2015)

  21. A. Hassan, M. Bhuiyan, Automated identification of sleep states from EEG signals by means of ensemble empirical mode decomposition and random under sampling boosting. Comput. Methods Prog. Biomed. 140, 201–210 (2017). https://doi.org/10.1016/j.cmpb.2016.12.015

  22. I.T. Hettiarachchi, T.T. Nguyen, S. Nahavandi, Motor imagery data classification for bci application using wavelet packet feature extraction. In: International Conference on Neural Information Processing, pp. 519–526. Springer (2014)

  23. A.K. Heye, R.D. Culling, M.C. Valdés Hernández, M.J. Thrippleton, J.M. Wardlaw, Assessment of blood–brain barrier disruption using dynamic contrast-enhanced MRI: a systematic review. NeuroImage Clin 6, 262–274 (2014)

  24. A.E. Hramov, A.A. Koronovskii, V.A. Makarov, A.N. Pavlov, E. Sitnikova, Wavelets in neuroscience (Springer, New York, 2015)

    Book  MATH  Google Scholar 

  25. A.E. Hramov, V.A. Maksimenko, S.V. Pchelintseva, A.E. Runnova, V.V. Grubov, V.Y. Musatov, M.O. Zhuravlev, A.A. Koronovskii, A.N. Pisarchik, Classifying the perceptual interpretations of a bistable image using eeg and artificial neural networks. Front. Neurosci. 11, 674 (2017)

    Article  Google Scholar 

  26. Y.L. Hsu, Y.T. Yang, J.S. Wang, C.Y. Hsu, Automatic sleep stage recurrent neural classifier using energy features of eeg signals. Neurocomputing 104, 105–114 (2013)

    Article  Google Scholar 

  27. M. Kaller, J. An, Contrast agent toxicity (StatPearls Publishing, Treasure Island, 2020)

    Google Scholar 

  28. S.K.Khare, V. Bajaj, S. Siuly, G. Sinha, Classification of schizophrenia patients through empirical wavelettransformation using electroencephalogram signals. in Modelling and Analysis of Active Biopotential Signals in Healthcare, (IOP publishing, 2020), pp. 1-1–1-26. https://doi.org/10.1088/978-0-7503-3279-8ch1

  29. J.P. Lachaux et al., Estimating the time-course of coherence between single-trial brain signals: an introduction to wavelet coherence. Neurophysiol. Clin. 32(3), 157–174 (2002)

    Article  Google Scholar 

  30. V.A. Maksimenko, A.E. Runnova, N.S. Frolov, V.V. Makarov, V. Nedaivozov, A.A. Koronovskii, A. Pisarchik, A.E. Hramov, Multiscale neural connectivity during human sensory processing in the brain. Phys. Rev. E 97(5), 052405 (2018)

  31. V.A. Maksimenko, A.E. Runnova, M.O. Zhuravlev, P. Protasov, R. Kulanin, M.V. Khramova, A.N. Pisarchik, A.E. Hramov, Human personality reflects spatio-temporal and time-frequency eeg structure. PloS one 13(9), e0197642 (2018)

  32. L. Montefusco, Wavelets (Elsevier Science, Amsterdam, 2014)

    Google Scholar 

  33. T. Nguyen, A. Khosravi, D. Creighton, S. Nahavandi, Eeg signal classification for bci applications by wavelets and interval type-2 fuzzy logic systems. Expert Syst. Appl. 42(9), 4370–4380 (2015)

    Article  Google Scholar 

  34. A. Ovchinnikov, A. Hramov, A. Luttjehann, A. Koronovskii, G. van Luijtelaar, Method for diagnostics of characteristic patterns of observable time series and its real-time experimental implementation for neurophysiological signals. Tech. Phys. 56(1), 1–7 (2011)

    Article  Google Scholar 

  35. R. Palaniappan, D.P. Mandic, Biometrics from brain electrical activity: A machine learning approach. IEEE Trans. Pattern Anal. Mach. Intell. 29(4), 738–742 (2007)

    Article  Google Scholar 

  36. W. Pan, W. Banks, A. Kastin, Blood-brain barrier permeability to ebiratide and tnf in acute spinal cord injury. Exp. Neurol. 146, 367–373 (1997)

    Article  Google Scholar 

  37. W. Pan, Y. Ding, Y. Yu, H. Ohtaki, T. Nakamachi, A. Kastin, Stroke upregulates tnf alpha transport across the blood-brain barrier. Exp. Neurol. 198, 222–233 (2006)

    Article  Google Scholar 

  38. W. Pan, A. Kastin, R. Bell, R. Olson, Upregulation of tumor necrosis factor a transport across the blood- brain barrier after acute compressive spinal cord injury. J. Neurosci. 19, 3649–3655 (1999)

    Article  Google Scholar 

  39. W. Pan, A. Kastin, L. Gera, J. Stewart, Bradykinin antagonist decreases early disruption of the blood-spinal cord barrier after spinal cord injury in mice. Neurosci. Lett. 307, 25–28 (2001)

    Article  Google Scholar 

  40. A. Pavlov, A. Dubrovsky, A. Koronovskii Jr., O. Pavlova, O. Semyachkina-Glushkovskaya, J. Kurths, Extended detrended fluctuation analysis of sound-induced changes in brain electrical activity. Chaos Soliton Fract. 139, 109989 (2020)

  41. M.A. Perazella, Gadolinium-contrast toxicity in patients with kidney disease: nephrotoxicity and nephrogenic systemic fibrosis. Curr. Drug. Saf. 3, 67–75 (2008)

    Article  Google Scholar 

  42. D.M.W. Powers, Evaluation: From precision, recall and f-factor to roc, informedness, markedness & correlation. J. Mach. Learn. Technol. 2(1), 37–63 (2011)

    MathSciNet  Google Scholar 

  43. M. Rogosnitzky, S. Branch, Gadolinium-based contrast agent toxicity: a review of known and proposed mechanisms. Biometals 29(365–376) (2016)

  44. M. Ronzhina, O. Janousek, J. Kolarova, M. Novakova, P. Honzik, I. Provaznik, Sleep scoring using artificial neural networks. Sleep Med. Rev. 16, 251–263 (2012)

    Article  Google Scholar 

  45. G. Rosenberg, Neurological diseases in relation to the blood-brain barrier. J. Cereb. Blood Flow Metab. 32, 1139–1151 (2012)

    Article  Google Scholar 

  46. A.E. Runnova, M.O. Zhuravlev, A.N. Pysarchik, M.V. Khramova, V.V. Grubov, The study of cognitive processes in the brain eeg during the perception of bistable images using wavelet skeleton. In: Dynamics and Fluctuations in Biomedical Photonics XIV, vol. 10063, p. 1006319. International Society for Optics and Photonics (2017)

  47. O. Semyachkina-Glushkovskaya, A. Abdurashitov, A. Dubrovsky, D. Bragin, O. Bragina, N. Shushunova, G. Maslyakova, N. Navolokin, A. Bucharskaya, V. Tuchind et al., Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood-brain barrier: mechanisms of brain clearing. J. Biomed. Opt. 22(12), 121719 (2017)

  48. O. Semyachkina-Glushkovskaya, A. Esmat, D. Bragin, O. Bragina, A.A. Shirokov, N. Navolokin, Y. Yang, A. Abdurashitov, A. Khorovodov, A. Terskov, M. Klimova, A. Mamedova, I. Fedosov, V. Tuchin, J. Kurths, Phenomenon of music-induced opening of the blood-brain barrier in healthy mice. bioRxiv p. 2020.10.03.324699 (2020). https://doi.org/10.1101/2020.10.03.324699. https://app.dimensions.ai/details/publication/pub.1131448754 and https://www.biorxiv.org/content/biorxiv/early/2020/10/05/2020.10.03.324699.full.pdf

  49. O. Semyachkina-Glushkovskaya, A. Esmat, D. Bragin, O. Bragina, A.A. Shirokov, N. Navolokin, Y. Yang, A. Abdurashitov, A. Khorovodov, A. Terskov, M. Klimova, A. Mamedova, I. Fedosov, V. Tuchin, J. Kurths, Phenomenon of music-induced opening of the blood-brain barrier in healthy mice. Proc. Roy. Soc. B Biol. Sci. 287(1941), 20202337 (2020). https://doi.org/10.1098/rspb.2020.2337. https://royalsocietypublishing.org/doi/abs/10.1098/rspb.2020.2337

  50. A. Subasi, Eeg signal classification using wavelet feature extraction and a mixture of expert mode. Expert Syst. Appl. 32, 1084–1093 (2007)

    Article  Google Scholar 

  51. Z. yao Tian, L. Qian, L. Fang, X. hua Peng, X. hu Zhu, M. Wu, W. zhi Wang, W. han Zhang, B. qi Zhu, M. Wan, X. Hu, J. Shao, Frequency-specific changes of resting brain activity in parkinson’s disease: a machine learning approach. Neuroscience 436, 170–183 (2020). https://doi.org/10.1016/j.neuroscience.2020.01.049. http://www.sciencedirect.com/science/article/pii/S0306452220300798

  52. R. Tripathy, S. Ghosh, P. Gajbhiye, U. Acharya, Development of automated sleep stage classification system using multivariate projection-based fixed boundary empirical wavelet transform and entropy features extracted from multichannel eeg signals. Entropy 22(1141) (2020)

  53. A. Tzallas, M. Tsipouras, D. Fotiadis, Epileptic seizure detection in EEGs using time-frequency analysis. IEEE Trans. Inf. Technol. Biomed. 13(5), 703–710 (2009)

  54. M. Unser, A. Aldroubi, A review of wavelets in biomedical applications. Proc. IEEE 84(4), 626–638 (1996)

    Article  Google Scholar 

  55. C.J. Van Rijsbergen, Information Retrieval (University of Glasgow, Information Retrieval Group, 1979)

  56. J. Wei, T. Chen, C. Li, G. Liu, J. Qiu, D. Wei, Eyes-open and eyes-closed resting states with opposite brain activity in sensorimotor and occipital regions: Multidimensional evidences from machine learning perspective. Front. Human Neurosci. 12, 422 (2018) https://doi.org/10.3389/fnhum.2018.00422. https://www.frontiersin.org/article/10.3389/fnhum.2018.00422

  57. S. Yang, C. Gu, E.T. Mandeville, Y. Dong, E. Esposito, Y. Zhang, G. Yang, Y. Shen, X. Fu, E.H. Lo et al., Anesthesia and surgery impair blood-brain barrier and cognitive function in mice. Front. Immunol. 8, 902 (2017)

    Article  ADS  Google Scholar 

  58. G. Zhu, Y. Li, P. Wen, Analysis and classification of sleep stages based on difference visibility graphs from a single-channel eeg signal. IEEE J. Biomed. Health Inf. 18(6), 1813–1821 (2014)

    Article  Google Scholar 

  59. E. Zinchenko, N. Navolokin, A. Shirokov, B. Khlebtsov, A. Dubrovsky, E. Saranceva, A. Abdurashitov, A. Khorovodov, A. Terskov, A. Mamedova et al., Pilot study of transcranial photobiomodulation of lymphatic clearance of beta-amyloid from the mouse brain: breakthrough strategies for non-pharmacologic therapy of alzheimer’s disease. Biomed. Opt. Exp. 10(8), 4003–4017 (2019)

    Article  Google Scholar 

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Acknowledgements

This work has been supported by the RF Government Grant No. 075-15-2019-1885 in part of the biological interpretation and machine learning approach. In the part of the development of numeric method of data analysis this work has been supported by the Council for Grants of the President of the Russian Federation for the State Support of Young Russian Scientists (Project No. MD-645.2020.9). The biological experiment has been partially supported by Russian Science Foundation Grant No. 18-75-10033.

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Semenova, N., Segreev, K., Slepnev, A. et al. Blood-brain barrier permeability changes: nonlinear analysis of ECoG based on wavelet and machine learning approaches. Eur. Phys. J. Plus 136, 736 (2021). https://doi.org/10.1140/epjp/s13360-021-01715-2

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