Abstract
A new chaos–wavelet approach is presented for electroencephalogram (EEG)-based diagnosis of Alzheimer’s disease (AD) employing a recently developed concept in graph theory, visibility graph (VG). The approach is based on the research ideology that nonlinear features may not reveal differences between AD and control group in the band-limited EEG, but may represent noticeable differences in certain sub-bands. Hence, complexity of EEGs is computed using the VGs of EEGs and EEG sub-bands produced by wavelet decomposition. Two methods are employed for computation of complexity of the VGs: one based on the power of scale-freeness of a graph structure and the other based on the maximum eigenvalue of the adjacency matrix of a graph. Analysis of variation is used for feature selection. Two classifiers are applied to the selected features to distinguish AD and control EEGs: a Radial Basis Function Neural Network (RBFNN) and a two-stage classifier consisting of Principal Component Analysis (PCA) and the RBFNN. After comprehensive statistical studies, effective classification features and mathematical markers were discovered. Finally, using the discovered features and a two-stage classifier (PCA-RBFNN), a high diagnostic accuracy of 97.7% was obtained.
Similar content being viewed by others
References
Adeli H, Zhou Z, Dadmehr N (2003) Analysis of EEG records in an epileptic patient using wavelet transform. J Neurosci Methods 123(1):69–87
Adeli H, Ghosh-Dastidar S, Dadmehr N (2005a) Alzheimer’s disease: models of computation and analysis of EEGs. Clin EEG Neurosci 36(3):131–140
Adeli H, Ghosh-Dastidar S, Dadmehr N (2005b) Alzheimer’s disease and models of computation: imaging, classification, and neural models. J Alzheimer’s Dis 7(3):187–199
Adeli H, Ghosh-Dastidar S, Dadmehr N (2007) A wavelet–chaos methodology for analysis of EEGs and EEG subbands to detect seizure and epilepsy. IEEE Trans Biomed Eng 54(2):205–211
Adeli H, Ghosh-Dastidar S, Dadmehr N (2008) A spatio-temporal wavelet–chaos methodology for EEG-based diagnosis of Alzheimer’s disease. Neurosci Lett 444(2):190–194
Adler G, Brassen S, Jajcevic A (2003) EEG coherence in Alzheimer’s dementia. J Neural Transm 110(9):1051–1058
Ahmadlou M, Adeli H (2010) Wavelet-synchronization methodology: a new approach for EEG-based diagnosis of ADHD. Clin EEG Neurosci 41(1):1–10
Anand P, Siva Prasad BVN, Venkateswarlu C (2009) Modeling and optimization of a pharmaceutical formulation system using radial basis function network. Int J Neural Syst 19(2):127–136
Barber R, McKeith IG, Ballard C, Gholkar A, O’Brien JT (2001) A comparison of medial and lateral temporal lobe atrophy in dementia with Lewy bodies and Alzheimer’s disease: magnetic resonance imaging volumetric study. Dement Geriatr Cogn Disord 12(3):198–205
Besthorn C, Sattel H, Geiger-Kabisch C, Zerfass R, Förstl H (1995) Parameters of EEG dimensional complexity in Alzheimer’s disease. Electroencephalogr Clin Neurophysiol 95(2):84–89
Besthorn C, Zerfass R, Geiger-Kabisch C, Sattel H, Daniel S, Schreiter-Gasser U, Forstl H (1997) Discrimination of Alzheimer’s disease and normal aging by EEG data. Electroencephalogr Clin Neurophysiol 103(2):241–248
Bouwman FH, Schoonenboom NSM, Verwey NA, Elk EJ, Kok A, Blankenstein MA, Scheltens P, Flier WM (2009) CSF biomarker levels in early and late onset Alzheimer’s disease. Neurobiol Aging 30(12):1895–1901
Burton EJ, Barber R, Mukaetova-Ladinska EB, Robson J, Perry RH, Jaros E, Kalaria RN, O’Brien JT (2009) Medial temporal lobe atrophy on MRI differentiates Alzheimer’s disease from dementia with Lewy bodies and vascular cognitive impairment: a prospective study with pathological verification of diagnosis. Brain 132(1):195–203
Deursen JA, Vuurman EFPM, Verhey FRJ, Kranen-Mastenbroek VHJM, Riedel WJ (2008) Increased EEG gamma band activity in Alzheimer’s disease and mild cognitive impairment. J Neural Transm 115(9):1301–1311
Deursen JA, Vuurman EFPM, Kranen-Mastenbroek VHJM, Verhey FRJ, Riedel WJ (2009) 40-Hz steady state response in Alzheimer’s disease and mild cognitive impairment. Neurobiol Aging. doi:10.1016/j.neurobiolaging.2009.01.002
Dierks T, Jelic V, Julin P, Maurer K, Wahlund LO, Almkvist O, Strik WK, Winblad B (1997) EEG-microstates in mild memory impairment and Alzheimer’s disease: possible association with disturbed information processing. J Neural Transm 104(4–5):483–495
Fjell AM, Westlye LT, Amlien I, Espeseth T, Reinvang I, Raz N, Agartz I, Salat DH, Greve DN, Fischl B, Dale AM, Walhovd KB (2009) High consistency of regional cortical thinning in aging across multiple samples. Cereb Cortex 19(9):2001–2012
Fjell AM, Walhovd KB, Fennema-Notestine C, McEvoy LK, Hagler DJ, Holland D, Blennow K, Brewer JB, Dale AM (2010) Brain atrophy in healthy aging is related to CSF levels of Aβ1-42. Cerebral Cortex. doi:10.1093/cercor/bhp279
Geula C, Mesulam MM (1996) Systematic regional variations in the loss of cortical cholinergic fibers in Alzheimer’s disease. Cereb Cortex 6(2):165–177
Ghosh-Dastidar S, Adeli H, Dadmehr N (2008) Principal component analysis-enhanced cosine radial basis function neural network for robust epilepsy and seizure detection. IEEE Trans Biomed Eng 55(2):512–518
Giannitrapani D, Collins J, Vassiliadis D (1991) The EEG spectra of Alzheimer’s disease. Int J Psychophysiol 10(3):259–269
Gomez C, Mediavilla A, Hornero R, Abasolo D, Fernandez A (2009) Use of the Higuchi’s fractal dimension for the analysis of MEG recordings from Alzheimer’s disease patients. Med Eng Phys 31(3):306–313
Hampel H, Teipel SJ, Alexander GE, Pogarell O, Rapoport SI, Möller HJ (2002) In vivo imaging of region and cell type specific neocortical neurodegeneration in Alzheimer’s disease. J Neural Transm 109(5–6):837–855
He Z, You X, Zhou L, Cheung Y, Tang YY (2010) Writer identification using fractal dimension of wavelet subbands in Gabor domain. Integr Comput Aided Eng 17(2):157–165
Head D, Snyder AZ, Girton LE, Morris JC, Buckner RL (2005) Frontal-hippocampal double dissociation between normal aging and Alzheimer’s disease. Cereb Cortex 15(6):732–739
Hiele K, Vein AA, Welle A, Grond J, Westendorp RGJ, Bollen ELEM, Buchem MA, Dijk JG, Middelkoop HAM (2007) EEG and MRI correlates of mild cognitive impairment and Alzheimer’s disease. Neurobiol Aging 28(9):1322–1329
Higuchi T (1988) Approach to an irregular time series on the basis of the fractal theory. Physica D Nonlinear Phenom 31(2):277–283
Jackson CE, Snyder PJ (2008) Electroencephalography and event-related potentials as biomarkers of mild cognitive impairment and mild Alzheimer’s disease. Alzheimer’s Dementia 4(1–1):137–143
Jelles B, van Birgelen JH, Slaets JPJ, Hekster REM, Jonkman EJ, Stam CJ (1999) Decrease of non-linear structure in the EEG of Alzheimer patients compared to healthy controls. Clin Neurophysiol 110(7):1159–1167
Jeong J, Chae JH, Kim SY, Han SH (2001) Nonlinear dynamic analysis of the EEG in patients with Alzheimer’s disease and vascular dementia. J Clin Neurophysiol 18(1):58–67
Jones BF, Barnes J, Uylings HB, Fox NC, Frost C, Witter MP, Scheltens P (2006) Differential regional atrophy of the cingulate gyrus in Alzheimer disease: a volumetric MRI study. Cereb Cortex 16(12):1701–1708
Junfei Q, Honggui H (2010) A repair algorithm for radial basis function neural network with application to chemical oxygen demand modeling. Int J Neural Syst 20(1):63–74
Karim A, Adeli H (2003) Radial basis function neural network for work zone capacity and queue estimation. J Transp Eng 129(5):494–503
Kim J, Wilhelm T (2008) What is a complex graph? Physica A Stat Mech Appl 387(11):2637–2652
Kogan EA, Korczyn AD, Virchovsky RG, Klimovizky SS, Treves TA, Neufeld MY (2001) EEG changes during long-term treatment with donepezil in Alzheimer’s disease patients. J Neural Transm 108(10):1167–1173
Kramer MA, Chang FL, Cohen ME, Hudson D, Szeri AJ (2007) Synchronization measures of the scalp EEG can discriminate healthy from Alzheimer’s subjects. Int J Neural Syst 17(2):61–69
Kuczynski B, Targan E, Madison C, Weiner M, Zhang Y, Reed B, Chui HC, Jagust W (2010) White matter integrity and cortical metabolic associations in aging and dementia. Alzheimer’s Dementia 6(1):54–62
Lacasa L, Luque B, Ballesteros F, Luque J, Nuno JC (2008) From time series to complex networks: the visibility graph. Proc Natl Acad Sci USA 105(13):4972–4975
Lacasa L, Luque B, Luque J, Nuno JC (2009) The visibility graph: a new method for estimating the Hurst exponent of fractional Brownian motion. Europhys Lett 86(3):30001–30004
Lee H, Cichocki A, Choi S (2007) Nonnegative tensor factorization for continuous EEG classification. Int J Neural Syst 17(4):305–317
Lerch JP, Pruessner JC, Zijdenbos A, Hampel H, Teipel SJ, Evans AC (2005) Focal decline of cortical thickness in Alzheimer’s disease identified by computational neuroanatomy. Cereb Cortex 15(7):995–1001
Lipovetsky S (2009) PCA and SVD with nonnegative loadings. Pattern Recogn 42(1):68–76
Lopez-Rubio E, Ortiz-de-Lazcano-Lobato JM (2009) Dynamic competitive probabilistic principal components analysis. Int J Neural Syst 19(2):91–103
Meyer JS, Huang J, Chowdhury MH (2007) MRI confirms mild cognitive impairments prodromal for Alzheimer’s, vascular and Parkinson–Lewy body dementias. J Neurol Sci 257(1–2):97–104
Osipova D, Pekkonen E, Ahveninen J (2006) Enhanced magnetic auditory steady-state response in early Alzheimer’s disease. Clin Neurophysiol 117(9):1990–1995
Osterhage H, Mormann F, Wagner T, Lehnertz K (2007) Measuring the directionality of coupling: phase versus state space dynamics and application to EEG time series. Int J Neural Syst 17(3):139–148
Pedrycz W, Rai R, Zurada J (2008) Experience-consistent modeling for radial basis function neural networks. Int J Neural Syst 18(4):279–292
Pritchard WS, Duke DW, Coburn KL (1991) Altered EEG dynamical responsivity associated with normal aging and probable Alzheimer’s disease. Dementia 2(2):102–105
Rossello JL, Canals V, Morro A, Verd J (2009) Chaos-based mixed signal implementation of spiking neurons. Int J Neural Syst 19(6):465–471
Savitha R, Suresh S, Sundararajan N (2009) A fully complex-valued radial basis function network and its learning algorithm. Int J Neural Syst 19(4):253–267
Stebbins GT, Murphy CM (2009) Diffusion tensor imaging in Alzheimer’s disease and mild cognitive impairment. Behav Neurol 21(1):39–49
Stephen JM, Montano R, Donahue CH, Adair JC, Knoefel J, Qualls C, Hart B, Ranken D, Aine CJ (2010) Somatosensory responses in normal aging, mild cognitive impairment, and Alzheimer’s disease. J Neural Transm 117(2):217–225
Thomas C, Berg I, Rupp A, Seidl U, Schroder J, Roesch-Ely D, Kreisel SH, Mundt C, Weisbrod M (2010) P50 gating deficit in Alzheimer dementia correlates to frontal neuropsychological function. Neurobiol Aging 31(3):416–424
Thompson PM, Moussai J, Zohoori S, Goldkorn A, Khan AA, Mega MS, Small GW, Cummings JL, Toga AW (1998) Cortical variability and asymmetry in normal aging and Alzheimer’s disease. Cereb Cortex 8(6):492–509
Thompson PM, Mega MS, Woods RP, Zoumalan CI, Lindshield CJ, Blanton RE, Moussai J, Holmes CJ, Cummings JL, Toga AW (2001) Cortical change in Alzheimer’s disease detected with a disease-specific population-based brain atlas. Cereb Cortex 11(1):1–16
Whitwell JL, Weigand SD, Shiung MM, Boeve BF, Ferman TJ, Smith GE, Knopman DS, Petersen RC, Benarroch EE, Josephs KA, Jack CR Jr (2007) Focal atrophy in dementia with Lewy bodies on MRI: a distinct pattern from Alzheimer’s disease. Brain 130(3):708–719
Woyshville MJ, Calabrese JR (1994) Quantification of occipital EEG changes in Alzheimer’s disease utilizing a new metric: the fractal dimension. Biol Psychiatry 35(6):381–387
Wu Q, Ben-Arie J (2008) View invariant head recognition by hybrid PCA based reconstruction. Integr Comput Aided Eng 15(2)97–108
Wu D, Warwick K, Ma Z, Gasson MN, Burgess JG, Pan S, Aziz TZ (2010) Prediction of Parkinson’s disease tremor onset using radial basis function neural network based on particle swarm optimization. Int J Neural Syst 20(2):109–116
Acknowledgments
The authors would like to thank Dr. Dennis Duke of Florida State University and Dr. Kerry Coburn of Mercer University for providing EEG data for this research project.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ahmadlou, M., Adeli, H. & Adeli, A. New diagnostic EEG markers of the Alzheimer’s disease using visibility graph. J Neural Transm 117, 1099–1109 (2010). https://doi.org/10.1007/s00702-010-0450-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00702-010-0450-3