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Neural Networks

journal homepage: www.elsevier.com/locate/neunet

reproduces analytical results best?

Arlex Oscar Marín García a,1 , Markus Franziskus Müller a,b,∗,1 , Kaspar Schindler c ,

Christian Rummel d

a

Facultad de Ciencias, Universidad Autónoma del Estado de Morelos, 62209 Cuernavaca, Morelos, Mexico

b

Centro Internacional de Ciencias, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico

c

Department of Neurology, Inselspital, Bern University Hospital, University Bern, Switzerland

d

Support Center for Advanced Neuroimaging (SCAN), Institute of Diagnostic and Interventional Neuroradiology, University Hospital, Inselspital,

University of Bern, Switzerland

Article history: The analysis of short segments of noise-contaminated, multivariate real world data constitutes a

Received 14 June 2012 challenge. In this paper we compare several techniques of analysis, which are supposed to correctly

Received in revised form 26 March 2013 extract the amount of genuine cross-correlations from a multivariate data set. In order to test for the

Accepted 13 May 2013

quality of their performance we derive time series from a linear test model, which allows the analytical

derivation of genuine correlations. We compare the numerical estimates of the four measures with the

Keywords:

analytical results for different correlation pattern. In the bivariate case all but one measure performs

Genuine correlations

Random correlations

similarly well. However, in the multivariate case measures based on the eigenvalues of the equal-time

Multivariate analysis cross-correlation matrix do not extract exclusively information about the amount of genuine correlations,

EEG but they rather reflect the spatial organization of the correlation pattern. This may lead to failures

Epilepsy when interpreting the numerical results as illustrated by an application to three electroencephalographic

recordings of three patients suffering from pharmacoresistent epilepsy.

© 2013 Elsevier Ltd. All rights reserved.

1. Introduction Bouchaud, & Potters, 1999; Müller, Baier, Galka, Stephani, & Muhle,

2005; Müller, Baier, Rummel, & Schindler, 2008; Müller et al., 2006;

Often, the precise mathematical definition of measures used Plerou et al., 2002; Plerou, Gopikrishnan, Rosenow, Nunes Amaral,

for data analysis contains integrals over infinite ranges (like & Stanley, 1999; Rummel, Müller, Baier, Amor, & Schindler, 2010).

the Fourier transform, Correlation coefficient, Hilbert transform, Due to the finite size of the data window, the estimate of

etc.) or limits to zero and/or infinity (e.g. Correlation dimension, the cross-correlation of two completely independent time series

Lyapunov exponent, etc.) (see for example Kantz & Schreiber, (e.g. independent Gaussian white noise) is generally non-zero. For

2004). In application to real world data, which are non-stationary the same reason, it is at first also not clear how close the numerical

and recorded with finite sampling rate, such requirements cannot estimate approximates the correct value in the case when genuine

be met. This lack of mathematical precision influences the quality correlations are present. Even worse, as the amount of random

of the numerical estimates. In the case of cross-correlations the correlations depends on the relation of the period of the slowest

sampling theorem proves that coarse graining of the data is not dominant frequency component of the signal and the length of the

relevant, provided that the highest frequency component of the data segment (Rummel et al., 2010), it may change drastically over

signal is smaller than the Nyquist frequency (a property which time (Müller et al., 2011, 2008). This undesired effect questions the

often is not checked for). However, replacing the integral over cross-correlation coefficient as an appropriate technique for the

infinite range with a sum over a finite data segment may cause analysis of real world data.

a serious side effect called ‘‘random correlations’’ (Laloux, Cizeau, At this place the question arises why not to simply use an-

other bivariate measure instead of the cross-correlation coeffi-

cient, which additionally to the above mentioned problem only

∗ Corresponding author at: Facultad de Ciencias, Universidad Autónoma del detects linear interrelationships between two signals. Therefore,

Estado de Morelos, 62209 Cuernavaca, Morelos, Mexico. Tel.: +52 777 3297020; fax: any nonlinear interrelation, which might be expected between sig-

+52 777 3297040. nals measured in real word complex systems, remains unobserved

E-mail address: muellerm@buzon.uaem.mx (M.F. Müller). by definition. However, for two reasons we concentrate on the

1 These authors have contributed equally to this work. numerically robust and computationally cheap cross-correlation

0893-6080/$ – see front matter © 2013 Elsevier Ltd. All rights reserved.

http://dx.doi.org/10.1016/j.neunet.2013.05.009

A.O. Marín García et al. / Neural Networks 46 (2013) 154–164 155

coefficient. At first, also for other measures deficiencies appear of the analysis of the model data. We selected several examples of

once the precise mathematical definition is translated into an al- different correlation pattern that demonstrate the pros and cons of

gorithm of a numerical estimate. Usually integrals over infinite each of the measures. Finally, we present an analysis of intracranial

ranges are then converted to finite sums, or limits to infinity or zero electroencephalographic recordings of epilepsy patients in order to

cannot be respected due to the finite amount of coarse-grained illustrate how the pitfalls of some measures may lead to erroneous

data. Secondly, it turns out that the cross-correlation coefficient conclusions drawn from the numerical analysis of real world data

performs equally well, or even better than sophisticated non- with unknown correlation pattern.

linear measures for the detection of the (linear or nonlinear)

coupling between nonlinear or even chaotic dynamical units 2. Methods and concepts

(Ansari-Asl, Senhadji, Bellanger, & Wendling, 2006; Kreuz et al.,

2007). In these studies measures for phase synchronization based 2.1. Correlation measures

on the Hilbert transform or wavelets, information theoretical mea-

sures like mutual information or measures based on phase space The equal-time correlation matrix Ĉ is real, symmetric and pos-

reconstruction have been included. Finally, in Mormann et al. itive definite, i.e. its eigenvalues are positive real numbers: 0 ≤

(2005) 30 different measures are tested for their ability to discrimi- λ1 ≤ λ2 ≤ · · · ≤ λM ≤ M. The range of the eigenvalues is limited

nate a possible pre-seizure from an interictal state by analyzing in- due to the trace condition Tr(Ĉ ) = i=1 λi = M. Cru-

M M

i=1 Cii =

tracranial electroencephalographic recordings. The authors found cial for characterizing cross-correlations is how the corresponding

that ‘‘A remarkable aspect of our results is that both among the uni- eigenvalues of the cross-correlation matrix are distributed (Baier,

variate and the bivariate approaches linear measures performed Müller, Stephani, & Muhle, 2007; Müller et al., 2005, 2006; Plerou

equally good or even better than non-linear measures’’. The au- et al., 2002). Therefore, the eigenvalues are central for designing a

thors of Ansari-Asl et al. (2006) recommend explicitly the appli- certain class of correlation measures.

cation of linear bivariate measures as a ‘‘first attempt’’. For these We aim to compare the equal-time cross-correlation matrix de-

reasons we concentrate on linear cross-correlations in this study. rived from the real world data with the equivalent matrix derived

During the last decade numerous studies have been dedicated from surrogates, which shares the same univariate properties as

to solve the problem of random correlations and several methods the original data but does not contain any genuine zero-lag cross-

have been developed to extract the genuine correlation structure correlations between the data channels. Hence, such data repre-

of a multivariate data set. One class of methods is based on the sents the null hypothesis of zero genuine correlations with the

techniques known from Random Matrix Theory (RMT) (Laloux same amount of random correlations as the original data. For the

et al., 1999; Müller et al., 2005, 2006; Plerou et al., 2002, 1999). At present null hypothesis of zero genuine correlations the surrogates

the core of these methods lays the distribution of eigenvalues and are generated in an iterative process where Fourier phases are ran-

eigenvectors of the equal-time cross-correlation matrix, which is domized while conserving the power spectrum as well as the am-

compared to those of well-defined random matrix ensembles, as plitude distribution of the signals (Schreiber & Schmitz, 2000).

e.g. the Wishart ensemble or the Gaussian Orthogonal Ensemble. Alternatively this kind of surrogate data can be approximated to

That part of the spectrum, which coincides with the random a high degree by randomly shifting the data channels relatively to

matrix prediction, is considered as random; while it is believed each other and wrapping the extra values around to the beginning

that significant deviations from the random matrix prediction are of the data set (Netoff & Schiff, 2002). In the present paper we used

generated by genuine interrelations. Hence, ensembles of random the technique of Fourier phase randomization, i.e. Iterative Am-

interrelation matrices represent the null hypothesis of absence of plitude Adjusted Fourier Transform based surrogates (IAAFT), al-

genuine cross-correlations. These techniques have often been used though shift surrogates deliver qualitatively similar results as we

to analyze stock data (optimization of portfolios by using certain have tested for.

variants of Principal Component Analysis). We define data segments of length L data points, which are

For a second group of methods the null hypothesis is repre- divided in at least NT non-overlapping windows of size T sampling

sented by appropriate surrogate data (Carmeli, Knyazeva, Inno- points. Each of these windows is used to estimate the equal-time

centi, & de Feo, 2005; Cui, Liu, Wan, & Li, 2010; Müller et al., 2011, cross-correlation matrix. Then, for each of the data segments L

2008; Rummel et al., 2010). Some techniques are based on compar- we generate NL surrogates and proceed with them in the same

ing the eigenvalues of the equal-time cross-correlation matrix de- way. Hence, we get an ensemble of correlation matrices, which

rived from the original data and from surrogates. Other approaches uniquely reflect random correlations. We diagonalize each of these

assess the distribution of the matrix elements itself and permit matrices; the eigenvalues are then used to define two different

not only to estimate the amount of genuine correlations but they correlation measures, which are supposed to reflect the ‘‘amount

provide in addition detailed information about the topology of the of genuine cross-correlation’’ of an empirical, multivariate data set

spatial correlation pattern. No thresholds or external parameters (Cui et al., 2010; Müller et al., 2011, 2008; Rummel et al., 2010).

have to been fixed such that methods of this group are fully data We define the amount of genuine cross-correlation as the

driven. Originally they have been designed for analyzing EEG data, average over all zero-lag cross-correlation coefficients of a M-

although a clustering algorithm derived within the same frame- dimensional multivariate data set under the supposition of in-

work (Rummel, 2008; Rummel, Baier, & Müller, 2007; Rummel finitely long, stationary time series recorded with infinite temporal

et al., 2010; Rummel, Müller, & Schindler, 2008) might be a use- resolution. In this case, the integral over an infinite range (the cor-

ful tool also for the analysis of financial data (Münnix et al., 2012). relation integral) can be evaluated precisely for each pair of time

In the present study we will focus solely on this group. series and no spurious contributions occur. Hence, the amount of

The paper is organized as follows. In the next section, we first genuine cross-correlations GCS can be defined as:

review the definitions of the correlation measures and define the M

2 ⌢

term ‘‘amount of genuine cross-correlation’’. Then we discuss the GCS = C ij (1)

model used for the derivation of artificial recordings and present M (M − 1) i>j

as an analytical result a formula, which quantifies the amount of

where

genuine cross-correlations as a function of the coupling strength. ∞

We close the method section with a description of EEG-recordings ⌢

and patients involved in this study. Then we present the results C ij = X̃i (t )X̃j (t )dt (2)

−∞

156 A.O. Marín García et al. / Neural Networks 46 (2013) 154–164

instead of the estimate over a finite data segment of length T and statistically equivalent to those derived from the surrogates.

finite sampling rate: Hence, CCS = 0, because all Si are equal to zero. In the case

of maximal correlations (all signals are identical), all λ̃oi = 0

T

1 for i = 1, . . . , M − 1 and λ̃oM = M. In this case, numerator and

Cij = X̃i (tk )X̃j (tk ). (3)

T k=1 denominator of formula (3) have the same value and CCS = 1

(c) CCS-Matrix (Rummel et al., 2010):

The tilde in Eqs. (2) and (3) indicates that the time series X̃i and The previous concept has been generalized in order to define

X̃j are normalized to zero mean and unit variance (within the data the CCS-Matrix, of which each entry is a bivariate estimate of

window of T data points in case of Eq. (3)). the genuine cross-correlations between

two

data channels. Let

µoij = med Cijo and µsij = med Cijs the medians of the

The definition of the correlation measures considered in this

study is: absolute values of the entries of the correlation matrices de-

rived from theoriginal data and the surrogates respectively and

(a) Synchronization Index SI (Carmeli et al., 2005; Cui et al., 2010): νijo = med Cijo . Then the definition of the CCS-matrix reads:

In order to account for the amount of random correlations,

the average eigenvalues derived from the original data λ̄oi o µoij − µsij

are divided by the corresponding ones estimated from the CCSij = sign νij Sij . (7)

1 − µsij

surrogates λ̄si . Then normalized quantities may be defined as:

In the last formula, the denominator assures proper normal-

λ̄oi /λ̄si ization of the matrix elements, the pre-factor defines the sign

Λi = . (4)

M of the correlation coefficient and the scalar Sij represents the

λ̄oj /λ̄sj

result of a one-sided Mann–Whitney–Wilcoxon-rank test (in-

j =1

cluding Bonferroni correction for multiple testing), i.e. it can be

The Λi are then substituted in the definition of the ‘‘S-esti- equal to zero and one only.

One may apply the significance test

mator’’ introduced by Carmeli and coworkers (Carmeli et al., to the absolute values Cij (as proposed in the original article

2005): Rummel et al., 2010) or directly to Cij . As we found a slightly im-

proved sensitivity to detect small genuine correlations when

M

the Cij are object of the significance test, we proceed in the

Λi log (Λi )

i =1

present study in this way. Note, the CCS-matrix is no longer

SI = 1 + . (5) a quadratic form and hence its eigenvalues are not necessarily

log (M )

positive. However, as each of the entries of this matrix is sup-

The definition is motivated by the information theoretical con- posed to already give an estimate of the genuine bivariate cor-

cept of entropy, although the index SI is certainly not an en- relations, no diagonalization is necessary in order to separate

tropy, as the Λi are no probabilities. However, definition (5) random and genuine contributions. Instead, one may estimate

provides an estimator for the amount of genuine correlations. the whole amount of genuine correlation within a multivariate

If all M signals are uncorrelated, the eigenvalues derived from data set as the average over the matrix elements:

original data and surrogates coincide. Hence, all Λi are equal to M

1/M and therefore SI = 0. If on the other hand all M signals are 2

CCSij .

CMat = (8)

identical, Λi = 0 for all i = 1, . . . , M − 1 and ΛM = 1. Hence, M (M − 1) i>j

in this case it holds that SI = 1.

(b) Cross-Correlation Strength CCS (Müller et al., 2011, 2008): (d) Finally we introduce a fourth measure in the following manner:

Any particular (random or genuine) correlation pattern causes We define the elements of an interrelation matrix called ‘‘sig-

a specific repulsion scheme of the eigenvalues. This finding nificant average correlations’’ as the average correlation coef-

is basic for defining the CCS-coefficient. It consists of the ficient estimated over the segment L.

comparison between the eigenvalues of the equal-time cross- NT

Sij o,k

= cijo Sij .

correlation matrix derived from the original data and the sur- SACij = cij (9)

rogates respectively. As repulsions may occur at any location NT k=1

along the spectrum, each of the eigenvalues is compared in- o,k

dividually. The normalized sum of significant differences may In the last formula, cij denotes the equal-time cross-

correlation coefficient between data channel ‘i’ and ‘j’ esti-

serve as a measure for the amount of genuine correlations of a

mated at the k-th data window of the original data. NT is

multivariate data set:

the number of windows within the segment L of the original

M recording and Sij represents again the outcome of the Mann–

λ̃i − λ̃si Si

o

Whitney–Wilcoxon-rank test (including Bonferroni correction

i=1

CCS =

−1

M . (6) for multiple testing). The genuine correlation strength may

M − λ̃M +

s

λ̃i

s then be estimated in a similar way as for the CCS-matrix:

i=1 M

2

SACij .

In this formula the λ̃ and λ̃ are the medians of the i-th eigen-

o s SMat = (10)

i i M (M − 1) i>j

value derived from the original data and the surrogates. Be-

cause of the factor Si only significant differences according With the exception of the synchronization index, all measures

to the nonparametric Mann–Whitney–Wilcoxon-rank test are yield numerical estimates on a predefined significance level

taken into account. It is equal to zero if the null hypothesis of fixed to 1% (including Bonferroni correction) throughout the

zero genuine correlations cannot be rejected, i.e. the particular paper.

eigenvalues are statistically equivalent. Otherwise, it is equal

to one and the difference between the two eigenvalues enters 2.2. A simple model system

the sum.

CCS varies between zero and one. If no genuine correlations The performance of linear or nonlinear interrelation measures

are present, all eigenvalues derived from the original data are is usually tested by (a) analyzing the data derived from theoretical

A.O. Marín García et al. / Neural Networks 46 (2013) 154–164 157

test models (e.g. Ansari-Asl et al., 2006; Kreuz et al., 2007) or (b) to not sensitive to the sign of the correlation, this consideration is only

empirical data measured under well defined specific conditions relevant for the CCS- and SAC-matrix.

(Mormann et al., 2005). As theoretical test models nonlinear For the numerical studies we varied ρ from zero to one in steps

dynamical systems are frequently used, which are linearly or of 0.02 and for each value of ρ we generated 100 independent

nonlinearly coupled. Then one measures the sensitivity of the realizations. Then we calculated the median value of the 100

interrelation-estimators as a function of the coupling strength and estimates of the correlation measures and the 95% significance

its robustness as its behavior under additive white or colored noise. interval.

However, in most cases, the analytical value for genuine cross- For estimating the correlation measures we generated seg-

correlations (or other bivariate measures) is unknown and one ments of L = 2000 sampling points. The time unit was set to 200

only tests if an interrelation measure detects the variation of the sampling points. Then the segment L corresponds to a 10 s interval.

coupling strength. Here we want to compare the performance of The segment is then divided in NT = 10 non-overlapping windows

the measures not only between each other but also with regard to of length T = 200. Furthermore, we generated from each segment

the analytical results of genuine cross-correlations. For this reason, NL = 10 IAAFT surrogates, which are divided in the same way in

we employ an analytically treatable test model. The fact that the shorter data windows of length T . In this way we get an ensemble

following model is a linear one constitutes no restriction as we aim of Nsurr = 100 random matrices representing the null-hypothesis

to test exclusively linear correlation measures. We define M time of zero genuine correlations.

series as:

We then define a frequency unit such that 1 Hz corresponds to

Xi = (1 − ρ)ξi + ρη, for i = 1, . . . , k 1/(time unit). For the present case we considered a frequency range

and (11) of 0.1–100 Hz for all the data derived from the above-described

numerical models.

Xi = ξi , for i = k + 1, . . . , M .

The ξi and η are independent colored or Gaussian white noise, 2.3. EEG data

i.e. ⟨ξi ⟩ = ⟨η⟩ = ⟨ξi η⟩ = 0 and ξi2 = 1 = η2 , where ⟨∗⟩ denotes

the average. Importantly, the ξi are generated for each of the time As a proof of principle we analyzed exemplarily several in-

series individually while η is a common noise component, which tracranial recordings of three patients suffering from pharma-

is the same for k ≤ M time series. Furthermore, the amount of coresistant epilepsy. Non-invasive studies had not allowed to

genuine correlations does not depend on the type of noise used. unequivocally localize the seizure onset zone and the patients un-

The power spectra of the time series only influence the amount of derwent long-term intracranial EEG recordings at the Department

random correlations while the parameter ρ controls the strength of Neurology of the University of Bern, Switzerland. Beside the

of genuine correlation. If ρ = 0 all M time series are independent need for invasive EEG studies, further inclusion criteria were excel-

and, hence, they do not contain any genuine cross-correlations. In

lent post-surgical outcome, here defined as class 1 or 2 according to

the limiting case ρ → 1, the independent noise term vanishes and

the ILAE classification (Wieser et al., 2001). The ethics committee

the k time series become identical and equal to η. In this case the

of the Kanton of Bern had approved retrospective analysis of EEG

respective correlation coefficients become equal to one. With this

data. In addition, all the patients had given written informed con-

test model it is also possible to generate mutually uncorrelated

sent that their data from long-term EEG might be used for research

clusters of correlated time series. This can be achieved by using

and teaching purposes.

different and mutually independent noise terms for each cluster.

The number of implanted electrodes for patient one was 42, for

For the numerical studies four different correlation patterns

patient two 88 and for patient three 47. All electroencephalograms

derived from model (11) are considered. With the exception of

considered in this paper have been recorded with a sampling

model A, in all cases the total number of time series has been fixed

to M = 19. frequency of 512 Hz. As in the case of the test models, the segment

length L has been chosen as 10 s, which was divided in 10 one-

Model A: is just the bivariate case solved by formula (11), viz. two second windows T . The segments have been moved with a 5 s

time series are successively correlated by increasing the step width along the recordings in order to obtain the temporal

coupling parameter ρ . evolution of the three correlation measures.

Model B: two of 19 data channels are correlated with strength

parameter ρ .

3. Results

Model C: three mutually independent correlation clusters are

formed. Two clusters contain 7 signals and the third one

5 time series. The signals of each cluster are correlated 3.1. Analytical considerations

with the same strength determined by ρ . In this case 52

from 171 matrix elements contain genuine correlations. The most important feature of the test model described in Sec-

Model D: 11 signals are correlated with strength ρ . In this case 55 tion 2.2. is that it can be treated analytically. In order to evaluate

of 171 matrix elements contain genuine correlations. the correlation integral one has to normalize the time series, such

that they have zero mean and unit variance. Hence,

We considered two variants of each model with the same amount

of genuine, but different strength of random correlations: (a) Gaus- (1 − ρ)ξ1 + ρη

sian white noise and (b) 1/f noise (pink noise) has been used for X1 = (12a)

the variables ξ and η. 1 − 2ρ + 2ρ 2

All definitions of the multivariate measures are based on the (1 − ρ)ξ2 + ρη

Pearson correlation coefficient, which takes values between minus X2 = . (12b)

1 − 2ρ + 2ρ 2

and plus one, while many other bivariate measures as e.g. the mu-

tual information or the phase coherence are positive. In order to Evaluating the correlation integral yields the correlation coefficient

test the performance of the different techniques when a positive as a function of ρ :

definite bivariate measure is used, we also constructed the multi-

variate measures based on the absolute value of the Pearson co- ρ2

efficient. However, as the eigenvalues of the correlation matrix are C12 (ρ) = . (13)

1 − 2ρ + 2ρ 2

158 A.O. Marín García et al. / Neural Networks 46 (2013) 154–164

This result holds for two time series only. If in a multivariate data analytical result Cgen (formula (15)). For the case of the eigenvalue-

set mK ≤ M time series are correlated with the same strength pa- based measures also the corresponding analytical result (formula

rameter ρ , the amount of genuine cross-correlation is given by: (17) and (18) respectively) is drawn for comparison.

We start with the discussion of the simplest case of bivariate

ρ2 mK (mK − 1) correlation pattern. In Fig. 1results obtained for model A (Fig. 1(a)

Cgen (ρ) = . (14)

1 − 2ρ + 2ρ M (M − 1)

2 to (f)) and model B (Fig. 1(g) and (h)) are shown. The synchroniza-

tion index (Fig. 1(a)) is by construction far from the analytical re-

Finally, for the case of KG clusters the amount of genuine correla-

tions is given by sult Cgen . The analytical result SIa is qualitatively different and takes

systematically values lower than Cgen . Therefore, the numerical es-

ρ2 KG

mK (mK − 1)

timate of the synchronization index stays almost always far from

Cgen (ρ) = . (15) Cgen (beside of the ranges ρ ≈ 0 and ρ ≈ 1) but approximates sat-

1 − 2ρ + 2ρ 2 k=1 M (M − 1) isfactory the theoretical curve SIa . As expected, the accuracy of the

If we assume block structure of the correlation matrix (3) and estimates decreases in the case of 1/f noise with somewhat larger

absence of random correlations, also for the eigenvalue based statistical fluctuations.

measures analytical formulas can be derived. Considering a single On the other hand the CCS-coefficient (Fig. 1(b)) describes

cluster with mK pairwise correlated signals with correlation coef- the theoretical curve Cgen considerably well. This is because for

ficient C (ρK ) from formula (13). Then the normalized eigenvalues model A Cgen and CCSa coincide. The same is true for the estimates

(Eq. (4)) read: of CMat (Fig. 1(c) and (d)) and SMat (Fig. 1(e) and (f)). Because

these measures contain a significance test, its sensitivity is reduced

1 − C (ρK ) such that small genuine and random correlations cannot be

Λi = ∀i = 1, . . . , mK

M distinguished such that the respective measure is set to zero. CCS

1 + (mK − 1)C (ρK ) starts to detect genuine correlations at about ρ ≈ 0.25 (white

ΛmK = (16) noise) and ρ ≈ 0.35 (1/f noise). The matrix measures are slightly

M

more sensitive (ρ ≈ 0.2 and ρ ≈ 0.3 for white and colored noise

1

Λi = ∀i > mK . respectively). Then, for higher values of the strength parameter

M CCS as well as CMat stay close, although somewhat below, the

This simplifies that for a situation with KG mutually independent theoretical curve. However, Cgen lies always within the 95%

groups, where the signals of each group are correlated pairwise confidence interval of CCS and CMat . The best performance in the bi-

correlated with strength C (ρK ), K = 1, . . . , KG the synchroniza- variate case shows SMat (Fig. 1(e) and (f)). Its median values of the

tion index reads: numerical estimates lie almost exactly upon the theoretical result.

1−C (ρ )

1−C (ρK )

The situation is qualitatively the same when a positive bi-

KG (m K −1)

K

log

M M variate measure in terms of the absolute value of the Pearson cor-

SIa = 1 +

K =1

i =1

log (M ) relation is used for the construction of the matrices CCSij and SACij

(Fig. 1(d) and (f)), although in this case the sensitivity is slightly re-

duced. If the significance test would have been performed for the

1+(mK −1)C (ρK ) 1+(mK −1)C (ρK )

M

log M

absolute values of the correlation matrix, Fig. 1(b), (c) and (d) were

+

log(M ) almost identical. Now the numerical estimates of CMat (Fig. 1(d))

are quantitatively very close to those of CCS (Fig. 1(b)). However,

(M −L) qualitatively CMat shows the same performance than in the case

1

1

M

log M

+ (17) shown in Fig. 1(c). This result could be anticipated because in this

i=L+1

log(M ) case the distributions of the absolute values of the correlation co-

KG

efficients enter the statistics, i.e. similar to the eigenvalues, which

where L = K =1 mK counts the total number of correlated chan- determine the CCS-coefficient there is no distinction between pos-

nels. itive and negative correlations.

In the same manner one obtains for the same multi-cluster In contrast it is more surprising that also SACij is only weakly

situation for the CCS-coefficient: affected by this change. In the case of SMat one should expect that

KG the average over the absolute value of the correlation coefficients

1

CCSa = (mK − 1)C (ρK ). (18) in Eq. (9) is less effective than in the former case. As opposed to this

M − 1 K =1 consideration the qualitative behavior of SMat is almost identical to

that observed in Fig. 1(e).

Formulas (15), (17) and (18) will be used in the following for

Table 1 gives an overview of the performance of the considered

the comparison with the different correlation measures estimated

correlation measures. The mean percentage error (Eq. (19)) of CCS

from the numerical data. Furthermore, a quantitative evaluation

is slightly higher than the one of CMat . The worst performance in

of the performance of the numerical estimates is provided by the

these terms shows the synchronization index. Although its esti-

mean percentage error (MPE), defined as:

mates are not strained by any kind of significance test, which natu-

Numerics analytics

rally decreases the sensitivity to detect small genuine correlations,

Cmeasure (ρ) − Cmeasure (ρ) dρ

its overall behavior yields the largest relative errors. With respect

MPE = analytics . (19)

Cmeasure (ρ)dρ to the mean percentage error the most precise measure in the bi-

variate case is SMat . Its MPE for pink noise is still lower than the

MPE of CMat for white noise.

3.2. Numerical results for model data This observation is qualitatively confirmed when turning to the

multivariate case of two correlated data channels (model B). In

In all figures displaying results derived from model data, the this case CMat and SMat behave also quantitatively similar as in

dashed line (green curve) indicates the results of the case of white the bivariate case of model A. The sensitivity and the magnitude

noise, the solid line (red curve) the corresponding results obtained of fluctuations are comparable for both measures and they ap-

for 1/f -noise and finally the thick solid line (black curve) shows the proximate the analytical result Cgen satisfactorily. For this reason

A.O. Marín García et al. / Neural Networks 46 (2013) 154–164 159

a b

c d

e f

g h

Fig. 1. Shown is the amount of genuine correlation for the bivariate case in panel a to f (model A) and the multivariate case of two correlated signals (model B) in panel g

and h. Green and red curves correspond to the realization of the models with white and 1/f noise respectively. Shown are median values for 100 realizations and the 95%

significance interval. (a) Synchronization index, (b) CCS-coefficient, (c) and (d) shows CMat based on the Pearson coefficient and its absolute value respectively, (e) and (f)

the same as (c) and (d) for SMat . The panels (g) and (h) display the results for the synchronization index and the CCS-coefficient respectively. The bold continuous presents

the analytical result Cgen , the thin dotted line in panel (a) and (b) and equivalently in panels (g) and (h), reflect the analytical results for SIa and CCSa respectively. (For

interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

only the results for the synchronization index SI (Fig. 1(g)) and the concise overview over the performances of the measures also for

CCS-coefficient (Fig. 1(h)) are shown. However, Table 1 provides a the analysis of this model. In short, the lowest relative error is again

160 A.O. Marín García et al. / Neural Networks 46 (2013) 154–164

Mean percentage error (Eq. (19)) of the four correlation measures estimated for

approximate the analytical result CCSa for large ρ -values. As in the

model A to D. The comparison is performed with the analytical result Cgen and for

the eigenvalue based measures also for the analytical formulas SIa and CCSa . case of model B the analytical results SIa and CCSa are far from Cgen

and show qualitatively a different behavior.

Model Measure Noise type MPE1 (%) MPE2 (%) MPE3 (%)

Much more favorable are the results for CMat and SMat (Fig. 2(c)

1/f 10.23 10.23 and (e) respectively). Both measures approximate the theoretical

CCS

WN 4.13 4.13

curve considerably well almost along the whole ρ -range. A direct

1/f 37.56 11.33 comparison between both measures reveals again that SMat shows

A SI

WN 32.89 4.67 a slightly better sensitivity for the detection of small genuine

1/f 8.44

interrelations and its median values fall almost exactly upon the

CMat

WN 3.88 analytical results. CMat starts to rise at larger ρ -values and stays

always slightly below Cgen . This is also documented in the mean

1/f 3.24 percentage error, which is notably smaller for SMat in than for CMat .

SMat

WN 1.01

In the case where a strictly positive bivariate measure is used for

1/f 48.96 88.92 the construction of the matrices CCSij and SACij the situation is

CCS

WN 372.01 52.12 qualitatively similar (Fig. 2(d) and (f)). Now the sensitivity of SMat is

1/f 106.45 50.38 reduced such that the measure starts to react at somewhat larger

SI

B WN 120.26 40.38 ρ -values. Its sensitivity is now comparable to that of CMat for both,

the white noise and the colored noise data. However, also in this

1/f 11.34

CMat

WN 4.39

case the approximation to the analytical curve is superior. The

median values of SMat describe the ρ -dependence of Cgen well.

1/f 8.68 Finally, we comment on the results obtained for the case of

SMat

WN 2.07 model D, where 11 data channels get correlated into a single

1/f 118.93 27.94 cluster. As the results obtained for CMat and SMat do not reveal

CCS

WN 161.79 11.06 any new information, we focus solely on the discussion of SI and

1/f 62.33 29.94 CCS. The respective results for model D are shown in Fig. 2(g)

SI

C WN 63.30 14.27 and (h). The CCS-coefficient describes the analytical result CCSa

well, at least for the case of white noise. The numerical estimates

1/f 10.33

CMat maintain almost a constant distance to CCSa along the whole

WN 4.24

curve such that the relative error reduces with increasing ρ . The

1/f 7.07 synchronization index, on the other hand, fails to describe the

SMat

WN 1.88 analytical results SIa almost along the whole range of ρ -values,

1/f 47.44 20.47 which is also documented via a considerably high mean percentage

CCS

WN 64.05 6.22 error. Table 1 provides a comprehensive summary also for model B.

1/f 46.27 53.18 Like in the other cases SMat performs best, followed by CMat .

SI

D WN 31.97 23.95 This behavior is qualitatively similar to that observed previ-

ously. However, interesting in this case is the quantitative com-

1/f 10.11 parison. In the case of model C, 52 non-diagonal elements of the

CMat

WN 4.25

equal-time cross-correlation matrix are affected by genuine cor-

1/f 6.91 relations. In the case of model D the number of matrix elements

SMat

WN 1.90 carrying genuine correlations is 55. Hence, the amount of genuine

cross-correlations (as defined by GCS in Eq. (1)) is larger for the

case of model D than for model C. However, the numerical esti-

detected for SMat followed by CMat . The worst estimates provide the

mates of both eigenvalue-based measures are significantly lower

two eigenvalue-based measures. This is true for the comparison

for model D. This could be expected because for model C it turns

with Cgen as well as for the comparison with the analytical results

out that SIa (ρ → 1) = 0.63 and CCSa (ρ = 1) = 0.89 while for

SIa and CCSa . For white as well as for pink noise the mean percent-

model D it holds that SIa (ρ → 1) = 0.47 and CCSa (ρ = 1) = 0.56.

age errors are notably larger than the MPE of those indices derived

This implies that the number of matrix elements containing gen-

from matrices. The sensitivity of both coefficients is clearly reduced

uine contributions and, therefore, the amount of genuine correla-

as compared to the previous case and now even for large couplings

tions within a multivariate data set, has at least in certain situations

(ρ ≈ 1) the estimates for white and pink noise are different, which

a lower influence of the estimate of CCS and SI than the spatial or-

indicates a less robust behavior against noise for eigenvalue based

ganization of the cross-correlation pattern.

measures. Poorest performance for model B shows clearly the CCS-

coefficient. It seems that in particular CCS is less sensitive to detect

small correlation structures, viz. when the number of correlated 3.3. Application to real world data

channels is much smaller than the dimension of the multivariate

data set. In Fig. 3 we present exemplarily the application of the correla-

Next we turn to the analysis of data derived for more complex tion measures to the intracranial EEG recordings of three patients,

interrelation schemes as realized in model C, viz. when three mu- suffering from pharmacoresistent epilepsy.

tually independent correlation clusters are formed (Fig. 2(a) to (f)). In all cases, the numerical values obtained for the CCS-

For the synchronization index we observe qualitatively the coefficient are substantially larger than those estimated by the

same behavior as for model A, although with a considerably other measures. Furthermore it is striking that although the esti-

higher mean percentage error (see Table 1). The values of MPE mates of SMat are always larger than those of CMat the time evolu-

are now more than twice as large as in the bivariate case. Slightly tion of both measures reveal almost exactly the same pattern. Even

better in terms of the mean percentage error performs the CCS- tiny details of SMat -curves are reproduced by CMat for all three pa-

coefficient. Furthermore it shows a somewhat higher sensitivity tients. As we have shown already in the previous section that SMat

A.O. Marín García et al. / Neural Networks 46 (2013) 154–164 161

a b

c d

e f

g h

Fig. 2. Results for model C (three mutually independent groups) are displayed in panels (a) to (f) and model D (one correlation cluster containing 11 channels) in panels

(g) and (h). Color coding is similar to Fig. 1. Shown are median values for 100 realization and the 95% significance interval. (a) Synchronization index, (b) CCS-coefficient,

(c) and (d) show CMat based on the Pearson coefficient and its absolute value respectively, (e) and (f) the same as t (c) and (d) for SMat . The panels (g) and (h) display the

results for the synchronization index and the CCS-coefficient respectively. The bold continuous presents the analytical result Cgen , the thin dotted line in panel (a) and (b)

and equivalently in panels (g) and (h), reflects the analytical results for SIa and CCSa respectively. (For interpretation of the references to colour in this figure legend, the

reader is referred to the web version of this article.)

162 A.O. Marín García et al. / Neural Networks 46 (2013) 154–164

Fig. 3. Results of the analysis of intracranial data of epilepsy patients: panel (a) and (b) seizure 1 of patient 1, panel (c) and (d) seizure of patient 2 and panel (e) and (f) for

patient 3. Panels (a), (c) and (e) display the CCS-coefficient (blue) and the synchronization index (red) and panel (b), (d) and (f) present the result for SMat (blue) and CMat

(red). The vertical black lines indicate seizure on- and offset. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of

this article.)

is slightly more sensitive and more precise in approximating the this peak constitutes the maximal value during the whole time

analytical results Cgen , it was expected that in general SMat > CMat . course shown in Fig. 3(c). Furthermore, SI does not encounter

As the differences in the performance are moderate, one could also the broad minimum just after seizure offset. Instead, during the

anticipate that both measures show the same time evolution. How- entire post-seizure period it fluctuates somehow around a nearly

ever, qualitative differences can be seen in comparison with the constant average value. On the other hand, neither SMat nor CMat

CCS-coefficient and the synchronization index. indicate such a pronounced maximum during seizure as the CCS-

For instance, in the case of patient 1 (Fig. 3(a) and (b)) the coefficient and SI do. Several peaks in the pre- and post-seizure

synchronization index shows only tiny fluctuation in the pre- period encounter much larger values and also the minimum of the

seizure phase. Then it increases during seizure, but notably CCS-coefficient just after seizure offset is less pronounced by the

later than the three other measures and misses completely the SAC- and CCS-matrix.

pronounced maximum during the first half of the seizure marked Finally, for patient 3 (Fig. 3(e) and (f)) both eigenvalue-based

by them. At seizure offset it decreases gradually instead of the measures show a pronounced broad maximum during the first half

abrupt drop shown by the competing methods, such that it reaches of the seizure. SMat and CMat also present some larger fluctuations

its pre-seizure level only at the end of the shown time-course. The after seizure onset, but by no means such a prominent maximum.

CCS-coefficient shows the main characteristics during the seizure Furthermore, the CCS-coefficient shows strong fluctuations during

as the measures derived by the matrices CCS and SAC. the pre- and post-seizure period, which are absent in the time

For patient 2 (Fig. 3(c) and (d)) both eigenvalue-based measures evolution of the other measures. In this case, the CCS-coefficient

show a pronounced maximum during the seizure. In either case, even encounters values much below those of SI.

A.O. Marín García et al. / Neural Networks 46 (2013) 154–164 163

4. Conclusions the sensitivity of CMat and SMat is slightly reduced under this

condition but performs otherwise with similar quality as for the

In view of the studies concerning the model data one can draw usual Pearson-coefficient.

the following conclusions: Also the computational cost is more favorable for the SAC-

The performance of methods based on the eigenvalues of the matrix. In terms of robustness both measures show an equally sta-

interrelation matrices is far of being optimal as we revealed by ble behavior. Furthermore, the CCS- and SAC-matrix provide the

comparing their numerical estimates with those of competing opportunity to study the dynamics of the topology of the func-

techniques and analytical results. The mean percentage error with tional network of a spatially extended system. In this case, one may

respect to the analytical results SIa and CCSa is in all considered understand the matrix as a weighted network and one may ap-

cases (with exception of model A) at least twice the MPE-value ply graph-theoretical tools in order to obtain detailed information

derived for the matrix based measures but occasionally it is more about e.g. the efficiency of information transfer, clustering, vul-

than an order of magnitude larger (compare with white noise val- nerability and other network properties (Horstmann et al., 2010;

ues of SMat for model B, C and D of Table 1). Furthermore, it turns out Kramer & Cash, 2012; Kramer, Kolaczyk, & Kirsch, 2008; Lehnertz

that the sensitivity CCS-coefficient reduces drastically for the de- et al., 2009; Schindler, Bialonski, Horstmann, Elger, & Lehnertz,

tection of small genuine correlation structures. In this case, also the 2008; Stam & Reijneveld, 2007).

robustness of this measure against the amount of random correla- In the present study we refrained from examining the depen-

tions is drastically reduced (Fig. 1(h)). On the other hand, it seems dence of the results on the parameters T , NT and NL . In previous

that the synchronization index shows similar deficiencies when studies the dependence of CCS matrix elements calculated from

several independent clusters are formed (Fig. 2(g)). In any case, the EEG signals turned out rather weak (Rummel et al., 2011). We do

sensitivity and robustness of both eigenvalue based measures is not expect a different finding for the measures discussed in the

deficient in comparison to the performance of SMat and CMat . The present paper. The reason is that in all cases the non-parametric

information of the whole amount of random as well as genuine and robust Mann–Whitney–Wilcoxon U-test is used for hypothe-

correlations of the multivariate data set is condensed in the distri- sis testing.

bution of eigenvalues. The separation of both contributions is more The application to exemplary intracranial EEG recordings

difficult when M eigenvalues are considered than M (M − 1)/2 ma- (Fig. 3) clearly illustrates how the deficiencies of eigenvalue-based

trix elements directly. measures may lead to serious discrepancies when interpreting the

However, we find that the most crucial deficiencies of both

results. First one notices that the CCS-coefficient provides in gen-

eigenvalue-based measures constitute on the fact that they do not

eral too large estimates. However, this might be of less importance

only depend on the strength of genuine correlations and the size of

if at least the time evolution reproduces qualitatively the correct

the correlation structure, but also on the topology of the correlation

correlation dynamics. Unfortunately this is not the case, neither

pattern. Beside that the numerical estimates of SI and CCS provide

for the CCS-coefficient, nor for the synchronization index. There

in general only a poor approximation of their corresponding ana-

may appear pronounced maxima in situations where the amount

lytical counterpart, they differ almost always drastically from Cgen .

of genuine correlations does not change at all. Broad regions of in-

Although they are originally declared as measures for the strength

creased correlations or sharp well pronounced peaks might occur

or total amount of genuine correlations (Cui et al., 2010; Müller

as illustrated in the seizure period of Fig. 3(c) and (e). Finally, also a

et al., 2011, 2008) they depend strongly on the spatial arrangement

systematic underestimation and a complete missing of prominent

of correlations.

maxima as shown in Fig. 3(a) and (d) may happen. Especially the

For instance, if the correlation pattern changes from a larger

drastically different behavior during critical periods of the record-

correlation cluster to several smaller structures such that the over-

ings, namely seizure on- and offset or the immediate post-seizure

all magnitude of genuine cross-correlations stays constant, eigen-

value based measures nevertheless might show a drastic increase period may cause confusions and misleading neurophysiologic in-

(compare the results derived from model C and D). Therefore, al- terpretations. In order to understand the brain dynamics generat-

ternations of this correlation measure do not necessarily indicate ing epileptic seizures or if one tries to discover the mechanism used

variations of the amount of genuine correlations but simply topo- by the brain to terminate the crisis, one needs definitely reliable

logical changes of the correlation pattern. measures whose numerical estimates are qualitatively and quan-

Only the measure derived from the CCS- and the SAC-matrix titatively correct (Netoff & Schiff, 2002; Schindler, Leung, Elger, &

show under all test conditions considered so far a stable and sat- Lehnertz, 2007).

isfying performance. For all cases (small, medium and large cor- In summary, we find measures based on the eigenvalues of

relations structures, few or many cluster formation) they reflect the equal-time cross-correlation matrix to be problematic when

quantitatively the amount of genuine correlations of a multivari- for the analysis of real world data. When analyzing the time

ate data set with a good accuracy. That is because the compari- evolution of cross-correlations, quantitative as well as qualitative

son with surrogate data as expressed in formula (7) and (9) discrepancies may occur. The reason is that the spectrum of

allows a reasonable estimate of genuine correlations from rather eigenvalues of the correlation matrix does not only contain

short time series. In particular SACij provides a good approxima- information about the magnitude of the cross-correlations, but also

tion of the correlation integral (2), which has to be evaluated over about their spatial distribution. Each spatial correlation structure

an infinite range. The small mean percentage errors of SMat are provokes its particular repulsion scheme of the eigenvalues (Baier

mainly caused by its reasonably good but still finite sensitivity; et al., 2007; Müller et al., 2005, 2006). Hence, eigenvalue based

small genuine correlations are not detected because the nonpara- measures automatically contain structural information about the

metric Mann–Whitney–Wilcoxon-rank may not distinguish origi- functional network and the time evolution of such measures

nal data from surrogates. Otherwise, the median values of SMat drop present a uncontrolled mixture of strength and topology features

precisely upon the analytical curves of Cgen . of the correlation pattern of a multivariate data set.

Furthermore, both concepts deliver reasonable results, when The CCS and SAC-matrix, on the other hand provide sensitive

the interrelation matrix is based on a positive measure. This and robust measures, which permit quantitative estimates of the

implies that our results can be expected to hold also when applied amount of genuine correlations within a multivariate data set

to measures as e.g. mutual information or phase coherence instead (as defined for time series of infinite length) even from finite

of the Pearson coefficient. Taking the absolute value of the equal- and eventually short time series. Additionally, they offer the

time cross-correlations has simulated this situation. It seems that possibility to study structural properties of the functional network

164 A.O. Marín García et al. / Neural Networks 46 (2013) 154–164

and provide detailed information about the spatial distribution Kramer, M. A., Kolaczyk, E. D., & Kirsch, H. E. (2008). Emergent network topology at

of cross-correlations. By using so called shift surrogates (Netoff seizure onset in humans. Epilepsy Research, 79, 173–186.

Kreuz, T., Mormann, F., Andrzejak, R. G., Kraskov, A., Lehnertz, K., & Grassberger, P.

& Schiff, 2002) instead of using the computationally expensive (2007). Measuring synchronization in coupled model systems: a comparison of

iterative Fourier-based surrogates (Schreiber & Schmitz, 2000) the different approaches. Physica D, 225, 29.

complexity of the methods can be considerably reduced. We also Laloux, L., Cizeau, P., Bouchaud, J.-P., & Potters, M. (1999). Noise dressing of financial

correlation matrices. Physical Review Letters, 83, 1467.

checked for the performance of the methods using shift surrogates Lehnertz, K., Bialonski, S., Horstmann, M. T., Krug, D., Rothkegel, A., Staniek, M.,

obtaining qualitatively similar results. However, the time saving et al. (2009). Synchronization phenomena in human epileptic brain networks.

might be orders of magnitude in dependence of the number of data Journal of Neuroscience Methods, 183, 42–48.

Mormann, F., Kreuz, T., Rieke, C., Adrrzejak, R. G., Kraskov, A., David, P., et al. (2005).

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Furthermore, the results obtained for genuine correlation Müller, M., Baier, G., Galka, A., Stephani, U., & Muhle, H. (2005). Detection and

matrices might be relevant for the usage of sample co-variance characterization of changes of the correlation structure in multivariate time

series. Physical Review E, 71, Art. No. 46116.

matrices (Raudys & Sausargiene, 1998) in the context of pattern

Müller, M., Baier, G., López Jiménez, Y., Marín García, A. O., Rummel, C., &

recognition. With the increased velocity by using shift surrogates Schindler, K. (2011). Evolution of genuine cross-correlation strength of focal

also an application as a kind of control mechanism during the onset seizures. Journal of Clinical Neurophysiology, 28(5), 450–462.

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Physical Review E, 65, Art. No. 066126.

Acknowledgments

Plerou, V., Gopikrishnan, P., Rosenow, B., Nunes Amaral, L. A., & Stanley, H. E. (1999).

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(Project No. 156667). K.S. is grateful for the support of the Raudys, S., & Sausargiene, A. (1998). Structures of the covariance matrices in the

classifier design. In Lecture notes in computer science: vol. 1451. Advances in

study by the Swiss National Science Foundation (project no. SNF pattern recognition (p. 583).

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