An Investigation on the Utility and Reliability of Electroencephalogram Phase Signal Upon Interpreting Cognitive Responses in the Brain: A Critical Discussion

Document Type : Original Articles

Author

Department of Computer Science and Engineering and Information Technology, School of Electrical and Computer Engineering, Shiraz University

Abstract

Within the neuroscience and computational neuroscience communities, applications such as evaluating different cognitive responses of the brain, brain-computer interface (BCI) systems and brain connectivity studies have increasingly been using EEG phase information during the past few decades. The utility of EEG phase can be directly linked to the neural propagation and synchronized firing of neuronal populations during different cognitive states of the brain. Nevertheless, it has previously been shown that phase of narrow-band (frequency specific) foreground EEG (desired) is prone to contain fake spikes and variations (unrelated to brain activity) in the presence of background spontaneous EEG and low SNRs of foreground EEG (the low-amplitude analytic signals or LAAS problem). Accordingly, extracting the instantaneous EEG phase sequence for further utilization upon interpreting the cognitive states of the brain using phase related quantities, such as instantaneous frequency, phase shift, phase resetting and phase locking value, is a very sensitive and rigorous process. In this study, a simple procedure is proposed to illustrate the effects of LAAS problem on the utility of EEG phase related quantities in aforementioned applications, also to investigate the reliability of interpretations of the brain’s cognitive states based on such quantities. Results show that, without a proper and effective solution strategy, such potential flaws lead to incorrect physiological and pathological interpretations.

Keywords

References

  1. Gray CM, Konig P, Engel AK, Singer W, et al. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature. 1989; 338(6213):334-337. doi: 10.1038/338334a0
  2. Marshall W. Statistical analysis of EEG phase shift events [PhD thesis]. Waterloo: University of Waterloo; 2014.
  3. Krusienski DJ, McFarland DJ, Wolpaw JR. Value of amplitude, phase, and coherence features for a sensorimotor rhythm-based brain-computer interface. Brain Research Bulletin. 2012; 87(1):130-134. doi: 10.1016/j.brainresbull.2011.09.019
  4. He W, Wei P, Zhou Y, Wang L. Combination of amplitude and phase features under a uniform framework with EMD in EEG-based brain-computer interface. Paper presented at: The Annual International Conference of the IEEE Engineering in Medicine and Biology Society. 2012 Aug 28-1; San Diego, USA.
  5. Townsend G, Feng Y. Using phase information to reveal the nature of event-related desynchronization. Biomedical Signal Processing and Control. 2008; 3(3):192-202. doi: 10.1016/j.bspc.2008.01.003
  6. Razavipour F, Sameni R. A study of event related potential frequency domain coherency using multichannel electroencephalogram subspace analysis. Journal of Neuroscience Methods. 2015; 249:22-28. doi: 10.1016/j.jneumeth.2015.03.037
  7. Picton TW, Dimitrijevic A, John MS, Van Roon P. The use of phase in the detection of auditory steady-state responses. Clinical Neurophysiology. 2001; 112(9):1698-1711. doi: 10.1016/s1388-2457(01)00608-3
  8. De Tommaso M, Marinazzo D, Guido M, Libro G, Stramaglia S, Nitti L, et al. Visually evoked phase synchronization changes of alpha rhythm in migraine: Correlations with clinical features. International Journal of Psychophysiology. 2005; 57(3):203-210. doi: 10.1016/j.ijpsycho.2005.02.002
  9. Sakkalis V. Review of advanced techniques for the estimation of brain connectivity measured with EEG/MEG. Computers in Biology and Medicine. 2011; 41(12):1110-1117. doi: 10.1016/j.compbiomed.2011.06.020
  10. Friston KJ. Functional and effective connectivity: A review. Brain Connectivity. 2011; 1(1):13-36. doi: 10.1089/brain.2011.0008
  11. Gomez-Herrero G. Brain connectivity analysis with EEG [PhD thesis]. Tampere: Tampere University of Technology; 2010.
  12. Sauseng P. Brain oscillations: Phase-locked EEG alpha controls perception. Current Biology. 2012; 22(9):R306-R308. doi: 10.1016/j.cub.2012.03.029
  13. Fell J, Axmacher N. The role of phase synchronization in memory processes. Nature reviews neuroscience. 2011; 12(2):105-118. doi: 10.1038/nrn2979
  14. Siegel M, Warden MR, Miller EK. Phase-dependent neuronal coding of objects in short-term memory. Proceedings of the National Academy of Sciences. 2009; 106(50):21341-21346. doi: 10.1073/pnas.0908193106
  15. Kaminski M, Blinowska KJ. A new method of the description of the information flow in the brain structures. Biological Cybernetics. 1991; 65(3):203-210. doi: 10.1007/bf00198091
  16. Kaminski M, Blinowska K, Szelenberger W. Topographic analysis of coherence and propagation of EEG activity during sleep and wakefulness. Electroencephalography and clinical Neurophysiology. 1997; 102(3):216-227. doi: 10.1016/s0013-4694(96)95721-5
  17. Thatcher RW, North DM, Biver CJ. Development of cortical connections as measured by EEG coherence and phase delays. Human Brain Mapping. 2008; 29(12):1400-1415. doi: 10.1002/hbm.20474
  18. Nunez PL, Srinivasan R. Electric fields of the brain: The neurophysics of EEG. 2nd edition. Oxford: Oxford University Press; 2006.
  19. Suzuki. Phase relationships of alpha rhythm in man. The Japanese Journal of Physiology. 1974; 24(6):569-586. doi: 10.2170/jjphysiol.24.569
  20. Chavez M, Le Van Quyen M, Navarro V, Baulac M, Martinerie J. Spatio-temporal dynamics prior to neocortical seizures: Amplitude versus phase couplings. IEEE Transactions on Biomedical Engineering. 2003; 50(5):571-583. doi: 10.1109/tbme.2003.810696
  21. Netoff TI, Schiff SJ. Decreased neuronal synchronization during experimental seizures. Journal of Neuroscience. 2002; 22(16):7297-7307. PMID: 12177225
  22. Stam C, Van Der Made Y, Pijnenburg Y, Scheltens P. EEG synchronization in mild cognitive impairment and Alzheimer’s disease. Acta Neurologica Scandinavica. 2003; 108(2):90-96. PMID: 12859284
  23. Stam CJ, van Walsum AMvC, Pijnenburg YA, Berendse HW, de Munck JC, Scheltens P, et al. Generalized synchronization of MEG recordings in Alzheimers disease: Evidence for involvement of the gamma band. Journal of Clinical Neurophysiology. 2002; 19(6):562-574. doi: 10.1097/00004691-200212000-00010
  24. Thatcher RW, North DM, Neubrander J, Biver CJ, Cutler S, DeFina P. Autism and EEG phase reset deficient GABA mediated inhibition in thalamo-cortical circuits. Developmental Neuropsychology. 2009; 34(6):780-800. doi: 10.1080/87565640903265178
  25. Jeanmonod D, Magnin M, Morel A, Siegemund M, Cancro A, Lanz M, et al. Thalamocortical dysrhythmia II. Clinical and surgical aspects. Thalamus & Related Systems. 2001; 1(03):245-254. doi: 10.1017/s1472928801000267
  26. Jeanmonod D, Schulman J, Ramirez R, Cancro R, Lanz M, Morel A, et al. Neuropsychiatric thalamocortical dysrhythmia: Surgical implications. Thalamus & Related Systems. 2003; 2(02):103-113. doi: 10.1017/s1472928803000104
  27. Rizzuto D, Madsen J, Bromfield E, Schulze-Bonhage A, Seelig D, Aschenbrenner-Scheibe R, et al. Reset of human neocortical oscillations during a working memory task. Proceedings of the national academy of Sciences. 2003; 100(13):7931-7936. doi: 10.1073/pnas.0732061100
  28. Tallon-Baudry C, Bertrand O, Fischer C. Oscillatory synchrony between human extrastriate areas during visual short-term memory maintenance. The Journal of Neuroscience. 2001; 21(20):177. PMID: 11588207
  29. Squire LR. Mechanisms of memory. Science. 1986; 232(4758):1612-1619. doi: PMID: 3086978
  30. Thatcher RW, North D, Biver C. Intelligence and EEG phase reset: A two compartmental model of phase shift and lock. NeuroImage. 2008; 42(4):1639-1653. doi: 10.1016/j.neuroimage.2008.06.009
  31. Sauseng P, Klimesch W, Gruber WR, Birbaumer N. Cross-frequency phase synchronization: A brain mechanism of memory matching and attention. Neuroimage. 2008; 40(1):308-317. doi: 10.1016/j.neuroimage.2007.11.032
  32. Cosmelli D, David O, Lachaux JP, Martinerie J, Garnero L, Renault B, et al. Waves of consciousness: Ongoing cortical patterns during binocular rivalry. Neuroimage. 2004; 23(1):128-140. doi: 10.1016/j.neuroimage.2004.05.008
  33. Varela F, Lachaux JP, Rodriguez E, Martinerie J. The brainweb: Phase synchronization and large-scale integration. Nature Reviews Neuroscience. 2001; 2(4):229-239. doi: 10.1038/35067550
  34. John ER. The neurophysics of consciousness. Brain Research Reviews. 2002; 39(1):1-28. doi: 10.1016/s0165-0173(02)00142-x
  35. John ER. From synchronous neuronal discharges to subjective awareness? The Boundaries of Consciousness: Neurobiology and Neuropathology. 2005; 150(1):143-593. doi: 10.1016/s0079-6123(05)50011-6
  36. Vaadia E, Haalman I, Abeles M, Bergman H, Prut Y, Slovin H, et al. Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature. 1995; 373(6514):515-518. doi: 10.1038/373515a0
  37. Sauseng P, Klimesch W. What does phase information of oscillatory brain activity tell us about cognitive processes? Neuroscience & Biobehavioral Reviews. 2008; 32(5):1001-1013. doi: 10.1016/j.neubiorev.2008.03.014
  38. Kahana MJ. The cognitive correlates of human brain oscillations. The Journal of Neuroscience. 2006; 26(6):1669-72. doi: 10.1523/jneurosci.3737-05c.200
  39. Sameni R, Seraj E. A robust statistical framework for instantaneous electroencephalogram phase and frequency analysis [Internet]. 2016 [Cited 2016 Aug 23]. Available from: https://hal.archives-ouvertes.fr/hal-01355465/document.
  40. Chavez M, Besserve M, Adam C, Martinerie J. Towards a proper estimation of phase synchronization from time series. Journal of Neuroscience Methods. 2006; 154(1-2):149-160. doi: 10.1016/j.jneumeth.2005.12.009
  41. Seraj E, Sameni R. Robust electroencephalogram phase estimation with applications in brain-computer interface systems; 2016. [Cited 2016 Oct 10]. Available from: https://hal.archives-ouvertes.fr/hal-01378726/
  42. Mormann F, Lehnertz K, David P, Elger CE. Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients. Physica D: Nonlinear Phenomena. 2000; 144(3):358369. doi: 10.1016/s0167-2789(00)00087-7
  43. Lachaux JP, Rodriguez E, Martinerie J, Varela FJ, et al. Measuring phase synchrony in brain signals. Human Brain Mapping. 1999; 8(4):194-208. doi: PMID: 10619414
  44. Le Van Quyen M, Foucher J, Lachaux JP, Rodriguez E, Lutz A, Martinerie J, et al. Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony. Journal of Neuroscience Methods. 2001; 111(2):83-98. doi: 10.1016/s0165-0270(01)00372-7
  45. Cohen L, Loughlin P, Vakman D. On an ambiguity in the definition of the amplitude and phase of a signal. Signal Processing. 1999; 79(3):301-307. doi: 10.1016/s0165-1684(99)00103-6
  46. Oliveira PM, Barroso V. Instantaneous frequency of multicomponent signals. IEEE Signal Processing Letters. 1999; 6(4):81-83. doi: 10.1109/97.752060
  47. Picinbono B. On instantaneous amplitude and phase of signals. IEEE Transactions on Signal Processing. 1997; 45(3):552-560. doi: 10.1109/78.558469
  48. Freeman WJ. Origin, structure, and role of background EEG activity. Part 2. Analytic phase. Clinical Neurophysiology. 2004; 115(9):2089-2107. doi: 10.1016/j.clinph.2004.02.028
  49. Sameni R. [The open-source electrophysiological toolbox (OSET) [Internet]. 2010 [Cited 2010 Jan 10]. Available from: https://www.researchgate.net/publication/235325036_The_Open-Source_Electrophysiological_Toolbox_OSET_version_21
  50. Seraj E. Cerebral Signal Phase Analysis Toolbox-User Guide. Computers in Biology and Medicine [Internet]. 2016 [Cited 2016 Oct 07]. Available from: https://www.sparrho.com/item/cerebral-signal-phase-analysis-toolbox-user-guide/9c7f46/
  51. Thatcher RW, North DM, Biver CJ. Self-organized criticality and the development of EEG phase reset. Human Brain Mapping. 2009; 30(2):553574. doi: 10.1002/hbm.20524
  52. Freeman WJ, Burke BC, Holmes MD. Aperiodic phase re-setting in scalp EEG of beta-gamma oscillations by state transitions at alpha-theta rates. Human Brain Mapping. 2003; 19(4):248-272. doi: 10.1002/hbm.10120
  53. Pikovsky A, Rosenblum M, Kurths J. Synchronization: A universal concept in nonlinear sciences. Cambridge Nonlinear Sciences Series 12. Cambridge: Cambridge University Press; 2003.
  54. Rosenblum MG, Pikovsky AS, Kurths J. Phase synchronization of chaotic oscillators. Physical Review Letters. 1996; 76(11):1804-7. doi: 10.1103/physrevlett.76.1804
  55. Mezeiova K, Palus M. Comparison of coherence and phase synchronization of the human sleep electroencephalogram. Clinical Neurophysiology. 2012; 123(9):1821-1830. doi: 10.1016/j.clinph.2012.01.016
  56. Carter G, Knapp C, Nuttall A. Estimation of the magnitude-squared coherence function via overlapped fast Fourier transform processing. IEEE transactions on audio and electroacoustics. 1973; 21(4):337-344. doi: 10.1109/tau.1973.1162496
  57. Bakardjian H, Tanaka T, Cichocki A. Optimization of SSVEP brain responses with application to eight-command brain-computer interface. Neuroscience Letters. 2010; 469(1):34-38. doi: 10.1016/j.neulet.2009.11.039
  58. Seraj E. Cerebral synchrony assessment: A general review on cerebral signals' synchronization estimation concepts and methods [Internet]. 2016 [Cited 2016 Dec 12]; Available from: https://arxiv.org/abs/1612.04295
Journal of Advanced Medical Sciences and Applied Technologies
Volume 2, Issue 4 - Serial Number 4
9
December 2016
Pages 299-312

Files

Share

How to cite

Statistics