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Indications of nonlinear deterministic and finite-dimensional structures in time


series of brain electrical activity: Dependence on recording region and brain
state

Article  in  Physical Review E · January 2002


DOI: 10.1103/PhysRevE.64.061907 · Source: PubMed

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PHYSICAL REVIEW E, VOLUME 64, 061907

Indications of nonlinear deterministic and finite-dimensional structures in time series


of brain electrical activity: Dependence on recording region and brain state
Ralph G. Andrzejak,1,2,* Klaus Lehnertz,1,† Florian Mormann,1,2 Christoph Rieke,1,2 Peter David,2 and Christian E. Elger1
1
Department of Epileptology, University of Bonn, Sigmund-Freud-Strasse 25, 53105 Bonn, Germany
2
Institut für Strahlen- und Kernphysik, University of Bonn, Nußallee 14-16, 53115 Bonn, Germany
共Received 14 May 2001; published 20 November 2001兲
We compare dynamical properties of brain electrical activity from different recording regions and from
different physiological and pathological brain states. Using the nonlinear prediction error and an estimate of an
effective correlation dimension in combination with the method of iterative amplitude adjusted surrogate data,
we analyze sets of electroencephalographic 共EEG兲 time series: surface EEG recordings from healthy volunteers
with eyes closed and eyes open, and intracranial EEG recordings from epilepsy patients during the seizure free
interval from within and from outside the seizure generating area as well as intracranial EEG recordings of
epileptic seizures. As a preanalysis step an inclusion criterion of weak stationarity was applied. Surface EEG
recordings with eyes open were compatible with the surrogates’ null hypothesis of a Gaussian linear stochastic
process. Strongest indications of nonlinear deterministic dynamics were found for seizure activity. Results of
the other sets were found to be inbetween these two extremes.

DOI: 10.1103/PhysRevE.64.061907 PACS number共s兲: 87.19.La, 05.45.⫺a, 05.45.Tp, 87.19.Xx

I. INTRODUCTION 关23兴, depression 关24兴, and schizophrenia 关25兴 mostly during


cognitive activity and in comparison against healthy control
The theory of deterministic chaos deals with complex dy- subjects. In particular, recordings from epilepsy patients have
namical systems that are characterized by the fact that they often attracted researchers’ attention 关9,26 – 41兴. This is due
can be rather simple to describe, e.g., by a set of nonlinear to outstanding features of actual seizure activity and, more-
differential equations, but can show a complicated, often er- over, to the medical indication to perform recordings inva-
ratic, temporal evolution 关1兴. Nonlinearity as a necessary sively in epilepsy patients, which offers a unique view of the
condition for such chaotic behavior is present in many dy- dynamical system human brain.
namical systems found in nature. For a neuronal network Interpretations of results ranged from ‘‘evidences for cha-
such as the brain, nonlinearity is introduced even on the cel- otic attractors’’ underlying the alpha rhythm 关7兴, sleep re-
cordings 关11兴, or epileptic seizures 关33,35,40兴, to the conclu-
lular level, since the dynamical behavior of individual neu-
sion that EEG data of healthy volunteers ‘‘may be more
rons is governed by threshold and saturation phenomena.
appropriately modeled by linearly filtered noise’’ 关15兴. In be-
Moreover, the hypothesis of an entirely stochastic brain can
tween these two extremes, authors concluded significant in-
be rejected due to its ability to perform sophisticated cogni- dications of nonlinearity but no indication of low dimension-
tive tasks. For these reasons, the electroencephalogram ality or determinism 关3–5,8,13兴. Besides the aim of finding a
共EEG兲 appears to be an appropriate area for nonlinear time certain dynamical model for the EEG, it was furthermore
series analysis 共NTSA兲 techniques, the practical spin-off investigated if relative changes of the calculated quantities
from the theory of deterministic chaos 关2兴. are capable of differentiating between different physiological
The structure of the brain, however, is highly compli- brain states 关14,15,17兴, increasing insight into brain dysfunc-
cated. Furthermore, the EEG always results from a huge tion 关9,16,21–25兴 or even of yielding information useful for
number of individual neurons, each interacting with its diagnostic purposes 关26,28 –30,34兴. The anticipation of im-
neighboring neurons as well as with remote neurons whose pending epileptic seizures is a further challenging aspect that
electric potentials are not included in the measurement. It is was investigated by a number of studies 关31,36 –39兴.
therefore questionable whether EEG time series, particularly Nevertheless, it remains uncertain whether the aforemen-
those of short duration, can carry enough information to re- tioned varying results indeed reflect different dynamical fea-
veal dynamical properties of the underlying system brain. tures of brain electrical activity, or whether they must instead
Many studies are known from the literature in which NTSA be attributed to differences in parameters of the respective
techniques were applied to different kinds of EEGs from algorithms and recording setups. Thus the aim of our study is
humans, such as recordings from healthy volunteers at rest to compare dynamical properties of brain electrical activity
关3–10兴, sleep 关11–13兴, during periods of cognitive activity from different extracranial and intracranial recording regions
关14 –17兴, under the influence of low doses of ethanol 关18兴 or and from different physiological and pathological brain
anesthetics 关19兴, or from patients with diseases like states, using fixed analysis parameters. Apart from the differ-
Alzheimer’s 关16,20兴, Parkinson’s 关21,22兴, Creutzfeldt-Jakob ent recording electrodes used for extracranial and intracranial
EEG registration, all other recording parameters were fixed.
Some of the morphological characteristics of the different
*Electronic address: ralphandrzejak@yahoo.de EEG time series under investigation, which are obvious to an

Electronic address: klaus.lehnertz@ukb.uni-bonn.de expert’s eye, will be sketched in the following.

1063-651X/2001/64共6兲/061907共8兲/$20.00 64 061907-1 ©2001 The American Physical Society


RALPH G. ANDRZEJAK et al. PHYSICAL REVIEW E 64 061907

EEG time series recorded extracranially during the re-


laxed state of healthy subjects with eyes closed show a pre-
dominant physiological rhythm, the so-called alpha rhythm
in a frequency range of 8 –13 Hz, an activity which is most
pronounced at the back of the head 关42兴. In contrast, broader
frequency characteristics are obtained for open eyes. EEG
time series are also recorded intracranially in humans, how-
ever only in the framework of a presurgical evaluation of
focal epilepsies. In this context the implantation of electrodes
is carried out to exactly localize the seizure generating area
which is termed the epileptogenic zone 关43兴. During a sei-
zure free interval the EEG recorded from within the epilep-
togenic zone is often characterized by intermittent occur-
rences of so-called interictal epileptiform activities.
Investigation of these steep, sometimes rhythmic high ampli-
tude patterns in EEG recordings contributes to a localization
of the epileptogenic zone. Fewer and less pronounced inter- FIG. 1. Scheme of the locations of surface electrodes according
ictal epileptiform activities can be found at recording sites to the international 10-20 system. Names of the electrode positions
distant from the epileptogenic zone. Finally, the EEG re- are derived from their anatomical locations. Segments of sets A and
corded during epileptic seizures, termed ictal activity, is al- B were taken from all depicted electrodes.
most periodic and of high amplitude, resulting from hyper-
synchronous activity of large assemblies of neurons. tained only activity measured during seizure free intervals,
We tested indications of deterministic and/or low- set E only contained seizure activity. Here segments were
dimensional structures in the aforementioned EEG time se- selected from all recording sites exhibiting ictal activity.
ries against the null hypothesis that these properties are com- All EEG signals were recorded with the same 128-
patible with a Gaussian linear stochastic and stationary channel amplifier system, using an average common refer-
process that was passed through a monotonic static but a ence 关omitting electrodes containing pathological activity 共C,
possibly nonlinear measurement function. To this end, a non- D, and E兲 or strong eye movement artifacts 共A and B兲兴. After
linear prediction error 关44兴 and an estimate of the correlation 12 bit analog-to-digital conversion, the data were written
dimension 关45兴 were calculated in a reconstructed state space continuously onto the disk of a data acquisition computer
关46兴 for both the original EEG time series and an ensemble system at a sampling rate of 173.61 Hz. Band-pass filter
of surrogate time series 关47兴. To reduce the probability of settings were 0.53– 40 Hz 共12 dB/oct.兲. Exemplary EEGs are
rejections of this null hypothesis, due solely to nonstationar- depicted in Fig. 3.
ity, EEG segments were chosen under an inclusion criterion
of weak stationarity. B. Steps of analysis
1. Surrogate time series
II. METHODS
For each time series s⫽39 surrogate time series were gen-
A. Data selection and recording techniques erated using the technique of Schreiber and Schmitz 关47兴.
Five sets 共denoted A–E兲 each containing 100 single- This iterative amplitude adjusting scheme results in surro-
channel EEG segments of 23.6-sec duration, were composed gates that consist of the original sample values and have
for the study. These segments were selected and cut out from power spectra ‘‘practically indistinguishable’’ 关47兴 from
continuous multichannel EEG recordings after visual inspec- those of the original time series. The underlying null hypoth-
tion for artifacts, e.g., due to muscle activity or eye move-
ments. In addition, the segments had to fulfill a stationarity
criterion described in detail in Sec. II B. Sets A and B con-
sisted of segments taken from surface EEG recordings that
were carried out on five healthy volunteers using a standard-
ized electrode placement scheme 共cf. Fig. 1兲. Volunteers
were relaxed in an awake state with eyes open 共A兲 and eyes
closed 共B兲, respectively. Sets C, D, and E originated from our
EEG archive of presurgical diagnosis. For the present study
EEGs from five patients were selected, all of whom had FIG. 2. Scheme of intracranial electrodes implanted for presur-
achieved complete seizure control after resection of one of gical evaluation of epilepsy patients. Depth electrodes were im-
the hippocampal formations, which was therefore correctly planted symmetrically into the hippocampal formations 共top兲. Seg-
diagnosed to be the epileptogenic zone 共cf. Fig. 2兲. Segments ments of sets C and D were taken from all contacts of the respective
in set D were recorded from within the epileptogenic zone, depth electrode. Strip electrodes were implanted onto the lateral and
and those in set C from the hippocampal formation of the basal regions 共middle and bottom兲 of the neocortex. Segments of set
opposite hemisphere of the brain. While sets C and D con- E were taken from contacts of all depicted electrodes.

061907-2
INDICATIONS OF NONLINEAR DETERMINISTIC AND . . . PHYSICAL REVIEW E 64 061907

共where x̄ denotes the mean of the respective subsegment兲 and


the center frequency

N * /2
2 ␻ iS共 ␻ i 兲
m ␻j ⫽
N*

i⫽1 S共 ␻i兲
共2兲

共where S denotes the amplitude of the Fourier transform of


the respective subsegment兲 were calculated. The fluctuation
of these properties among subsegments was quantified using
the average deviations
n
1
F ⫽
x
n 兺 兩 m xj ⫺m x兩 ,
j⫽1
共3兲

n
1
F ␻⫽
n 兺 兩 m ␻j ⫺m ␻兩 ,
j⫽1
共4兲

where the overbar denotes mean of all 16 subsegments. As


FIG. 3. Exemplary EEG time series from each of the five sets. an inclusion criterion, both F ␻ and F x of the original time
From top to bottom: set A to set E 共denoted EEG-a to EEG-e兲.
series were required to range within the distribution calcu-
Amplitudes of surface EEG recordings are typically in the order of
lated from the respective surrogate ensemble, i.e., both val-
some ␮ V. For intracranial EEG recordings amplitudes range around
ues must neither exceed the maximum nor fall below the
some 100 ␮ V. For seizure activity these voltages can exceed
1000 ␮ V.
minimum of the surrogate distribution.

esis is that the time series is compatible with a Gaussian 3. Estimate of an effective correlation dimension
linear stochastic and stationary process measured by a static Using delay coordinates xi ⫽(x i ,x i⫹ ␶ , . . . ,x i⫹(m⫺1) ␶ )
and monotonic, possibly nonlinear, function. Since disconti- 关46兴 and the correlation sum
nuities between the end and beginning of a time series are
known to cause spurious spectral frequency components, N⫺1 N⫺1
2
segments of 4396 samples were at first cut out of the record- C 共 ␧,N 兲 ⫽
共 N⫺T 兲共 N⫺T⫺1 兲 兺 兺
i⫽0 j⫽i⫹T
⌰ 共 ␧⫺储xi ⫺x j 储兲
ings. Within these longer intervals, the beginning of each of
the final segments of N⫽4096 samples was then chosen in 共5兲
such a way that the amplitude difference of the last and first
关where ⌰ is the Heaviside step function, ⌰(a)⫽0᭙a⭐0
data points was within the range of amplitude differences of
consecutive data points, and the slopes at the end and begin- and ⌰(a)⫽1᭙a⬎0兴 the correlation dimension D 2 is de-
ning of the time series had the same sign. This algorithm fined 关45兴 by
avoids the use of window functions for a calculation of the
power spectrum. A comparable technique was applied in Ref. D 2 ⫽ lim lim d 共 ␧,N 兲 , 共6兲
N→⬁ ␧→0
关18兴.

2. Weak stationarity criterion


where

The probative force of a rejection of the surrogates’ null ⳵ ln C 共 ␧,N 兲


hypothesis for deterministic and/or low-dimensional struc- d 共 ␧,N 兲 ⫽ . 共7兲
⳵ ln ␧
ture is limited, since stationarity is included in this null hy-
pothesis. On the other hand, this particular property allows
From these definitions it follows that a true correlation di-
one to use surrogates in a test for nonstationarity. Here we
mension cannot be calculated from time series of finite
propose such a test as a preanalysis step that eventually re-
length and limited accuracy. An estimation of an effective
duces the probability of rejections of the null hypothesis due
correlation dimension, however, can be obtained for those
to nonstationarities.
time series where a quasiscaling behavior of d(␧,N) is found
EEG-time series and respective surrogates were each di-
at least for a limited range of the hypersphere radius ␧ 关50兴.
vided into n⫽16 nonoverlapping subsegments 共length N *
The applied steps of analysis and the choice of parameters
⫽256). For each subsegment ( j⫽1, . . . ,n) the average de-
follow Ref. 关36兴, and use the algorithm described in Ref.
viation of amplitudes
关51兴. With a fixed time delay ( ␶ ⫽1 sampling time兲, d(␧,N)
N* was calculated for a range of embedding dimensions (m
1
m xj ⫽
N*
兺 兩 x i ⫺x̄ 兩
i⫽1
共1兲 ⫽1, . . . ,25) using the maximum norm and applying a
Theiler window 关52兴 (T⫽5 sampling times兲. The range of ␧

061907-3
RALPH G. ANDRZEJAK et al. PHYSICAL REVIEW E 64 061907

was chosen to match the resolution of the analog-to-digital parameter values reported were obtained from preanalysis
converter, and divided into 128 intervals. A ‘‘quasiscaling with regard to an optimum differentiation between nonlinear
region’’ 关 ␧ l ,␧ u 兴 is defined by deterministic and linear stochastic model systems. In order to
meet the requirements of the respective statistics, we chose
␧ u ⫽max兵 ␧ 兩 d 共 ␧,N 兲 兩 m⫽1 ⬎0.975其 , 共8兲 all parameters independently for both P and D 2,e f f .

␧ l ⫽min兵 ␧ 兩 兩 d 共 ␧ u ,N 兲 兩 m⫽25⫺d 共 ␧,N 兲 兩 m⫽25兩 5. Levels of null hypothesis testing - Statistical methods
⭐0.05d 共 ␧,N 兲 兩 m⫽25其 . 共9兲 All following steps of analysis were carried out for P and
D 2 , e f f . In the following, M stands for any of the two mea-
If ␧ u and ␧ l existed, and the number N r of ␧ values in sures. The null hypothesis was tested on two levels: on one
关 ␧ l ,␧ u 兴 was greater than or equal to 5, the estimate level for every individual EEG segment, and on a second
␧u level for each of the five sets of EEG segments. On the
1
D 2,e f f ⫽
Nr 兺
␧⫽␧ l
d 共 ␧,N 兲 兩 m⫽25 共10兲 individual level the null was rejected if M EEG ranged outside
the distribution calculated from all of its surrogates
兵 M Sur i⫽1, . . . ,s 其 . For a given set and measure, let R min be the
was computed. If no quasiscaling existed or if D 2,e f f ⭓7.2 number of rejections of the null hypothesis which were
⬇2 log N 共cf. Ref. 关53兴兲, D 2,e f f was set to an arbitrary value caused by the fact that M EEG was smaller than the minimum
of D u ⫽10. of 兵 M Sur i⫽1, . . . ,s 其 . To rate a given number of rejections of the
null hypothesis, the probability p min to find R min or less re-
4. Nonlinear prediction error jections on a set of n ⫽100 time series just by chance was
For each reference point xi (i⫽1, . . . ,N⫺m ␶ ) in a re- calculated as
constructed state space 共embedding dimension m⫽6 and
time delay ␶ ⫽8 sampling times兲 a fixed number (k⫽5) of
冉 冊冉 冊 冉 冊
R min k n⫺k
n 1 1
nearest neighbors 兵 x j 其 j⫽1, . . . ,k was used to perform an p min⫽ 兺
k⫽0 k s⫹1
1⫺
s⫹1
. 共15兲
H-step prediction:
k
1 In complete analogy, we calculated the probability p max to
xg
i⫹H ⫽
k 兺 xj⫹H .
j⫽1
共11兲 find R max or less rejections that were caused by the fact that
M EEG exceeded the surrogates’ maximum.
The difference between the actual xi⫹H and predicted trans- On the set level one surrogate per EEG segment was used.
lation xg In accordance with Ref. 关3兴, values of 兵 M EEG 其 and 兵 M SUR 1 其
i⫹H is the local prediction error
were used as paired observations for a nonparametric Wil-
␧ i,xg
i⫹H
⫽ 兩 xi⫹H ⫺xg
i⫹H 兩 . 共12兲 coxon signed rank test. In order to ensure that the choice of
D u did not influence results of the null hypothesis testing on
the set level, the Wilcoxon test was carried out with different
The local prediction error for the mean of the time series x̄ is values of D u .
␧ i,x̄⫽ 兩 xi⫹H ⫺x̄兩 , 共13兲
III. RESULTS
where x̄ is an m-dimensional vector that carries the mean in
Figure 4 depicts results of exemplary EEGs. Table I and
each of its component. Finally the nonlinear prediction error
Fig. 5 summarize the results of all EEG segments and sets.
共P兲 is calculated from
On the individual level, sets E and D exhibited highest and
second highest R min values for both P and D 2,e f f . For all
R共 ␧ i,xg )
P⫽
i⫹H
, 共14兲 sets, the use of P led to higher R min values than the use of
R共 ␧ i,x̄兲 D 2,e f f . This was particularly true for sets B and C, for which
the strongest discordance between the two measures was
where R indicates the root mean square. For a nearest neigh- found: while for P both R min values were significant, they
bor search for every reference point xi , a Theiler window were both nonsignificant for D 2,e f f . Concordance was found
(T⫽25 sampling times兲 was applied to its own trajectory only for set A: here none of the two measures led to signifi-
segment and to neighboring trajectory segments: In a first cant R min values. None of the R max values was significant.
step, vectors with indices 兵 i⫺T, . . . ,i⫺1,i⫹1, . . . ,i⫹T 其 Segments with rejection of the null hypothesis for both P and
were discarded. In a second step, out of a group of nearest D 2,e f f were found in sets D and E only.
neighbors passing the first step but closer to each other in For the vast majority of segments D 2,e f f could not be
time than T, only the one nearest to xi was included. The calculated, and was therefore set to D u 共cf. Table I兲. For sets
second step is important to ensure that information for the P A and B, this was the case for all EEG segments and almost
is gathered from multiple adjacent trajectory segments rather all surrogates. Consequently, the null hypothesis on the set
than from only one trajectory segment 共cf. Refs. 关48,49兴兲. level could not be tested using D 2,e f f . For set C, only a few
The prediction horizon H was set to 65 sampling times. The segments resulted in D 2,e f f ⬍D u , whereas most segments re-

061907-4
INDICATIONS OF NONLINEAR DETERMINISTIC AND . . . PHYSICAL REVIEW E 64 061907

FIG. 4. Results for the exemplary EEG times series depicted in Fig. 3. From top to bottom: results for EEG-a to EEG-e. Left column:
P EEG and P SUR 1, . . . ,s vs prediction horizon H. Circles mark P EEG . Right column: d(␧,N) EEG and d(␧,N) SUR 1, . . . ,s vs the logarithm of the
hypersphere radius ␧ for an embedding dimension m⫽25. Diamonds mark d(␧,N) EEG . In addition, d(␧,N) EEG for embedding dimension
m⫽1 is given. Asterisks mark cases for which the null hypothesis was rejected. Note that for EEG-b there is a limited range of the
hypersphere radius ␧ for which d(␧,N) EEG was below the surrogates minimum. Hence the null hypothesis could be rejected. Neither the
EEG nor the surrogate time series, however, resulted in a finite value of D 2,e f f , so that the null was not rejected for D 2,e f f . Only for
examples EEG-d and EEG-e values of D 2,e f f could be estimated: 5.5 and 4.4, respectively.

2,e f f ⫽D 2,e f f ⫽D u , and therefore entered the Wil-


sulted in D EEG SUR
level could be rejected.
coxon test as binded observations. A noteworthy number of Using P set A was the only one for which we obtained a
D EEG
2,e f f values was calculated only from EEG time series of nonsignificant p Wilc value. For all other sets the null hypoth-
sets D and E. These sets were the only ones that resulted in esis could be rejected on the set level. Although decreasing
significant p Wilc values, so that the null hypothesis on the set mean values of P EEG were found in the set order

061907-5
RALPH G. ANDRZEJAK et al. PHYSICAL REVIEW E 64 061907

TABLE I. Results for P and D 2,e f f on the individual level 共rows 1 and 2 and 6 and 7兲 and on the set level
共rows 3 and 4 and 8 and 9兲. Values of p max are not listed, since all were nonsignificant. Values in row 5
denote the number of segments for which a value of D 2,e f f could be computed for the EEGs and the
surrogates, respectively. The last row contains the number of segments for which the null was rejected for
both measures. n.s.: values of p⬎0.05 are assumed to be nonsignificant. x: no Wilcoxon test was carried out
for sets A and B 共see the body text兲.

A B C D E

R min /Rmax 4/1 9/3 14/3 37/0 89/0


P p min n.s. ⬍0.001 ⬍0.001 ⬍0.001 ⬍0.001
p Wilc n.s. 0.004 ⬍0.001 0.001 ⬍0.001
Z Wilc -0.6 -2.9 -7.0 -3.5 -8.6
EEG/SUR
D 2,e ff ⬍D u 0/1 0/1 7/7 27/9 76/5
R min /Rmax 0/0 0/0 0/1 17/2 56/0
D 2,e f f p min n.s. n.s. n.s. ⬍0.001 ⬍0.001
p Wilc x x n.s. ⬍0.001 ⬍0.001
Z Wilc x x -1.0 -3.7 -7.6

P&D 2,e f f R min /Rmax 0/0 0/0 0/0 10/0 40/0

A-C-B-D-E, smallest values were still found to be higher IV. DISCUSSION


than 0.5 共cf. Fig. 5兲.
In summary, the null hypothesis of an underlying linear Our study showed clear differences in dynamical proper-
stochastic and stationary process, measured by a static and ties of brain electrical acitivity from different extracranial
monotonic but possibly nonlinear measurement function as and intracranial recording regions and from different physi-
represented by the iterative amplitude adjusted surrogates, ological and pathological brain states. Despite the assumed
could be rejected for sets D and E for both P and D 2,e f f . For nonlinear deterministic nature of neuronal dynamics, a qua-
sets B and C, only the use of P led to a rejection, while these silinear stochastic and high-dimensional appearance of the
sets appeared to be compatible with the null for D 2,e f f . Set A EEG, as found for set A, consistent with results reported in
was the only set which was compatible with the null hypoth- Refs. 关4,9,15兴, might originate from both the huge number of
esis for both measures. neurons included in an EEG measurement and the compli-
cated structure of the brain. Particularly for surface EEG
recordings, a further blurring of possible dynamical struc-
tures in the EEG is caused by filter processes due to different
conductivities of the skull and other intermediate tissue. Cer-
tain imposed constraints in dynamics, however, might de-
mask or further strengthen nonlinear deterministic traits of
neuronal dynamics. Results found with P for set B suggest
that the closing of eyes might represent the imposing of such
a constraint in dynamics resulting in the well-known physi-
ological alpha rhythm. For no segment of sets A and B, how-
ever, a conclusive indication of a finite dimension or even a
low dimension could be obtained. Therefore, a differentiation
of the conditions of eyes closed and eyes open, such as re-
ported in Refs. 关14,16兴, could not be obtained. Regarding
these aspects, the results of our study are in agreement with
other studies carried out on surface EEG recordings of
healthy volunteers 关3,5,6,8,13,18兴, where indications of non-
linearity but not of an underlying low dimensional structure
were found.
The strong indications of nonlinear deterministic struc-
FIG. 5. Results for P 共upper panel兲 and D 2,e f f 共lower panel兲 for tures found for set D were certainly often related to interictal
sets A–E. For every measure and set, circles depict the mean value epileptiform activity, as also reported in Refs. 关28,29兴. In
of 兵 M EEG 其 , and diamonds the mean value of 兵 M SUR 1 其 ; bars on some cases, however, NTSA measures might be capable of
symbols are given by the ranges of these distributions. Vertical lines detecting more subtle dynamical manifestations of the dis-
in between the symbols depict those values of M EEG for which the ease epilepsy. This view was supported by a number of stud-
null hypothesis was rejected on the individual level by the fact that ies 关26 –28,30,34,41兴, all of which demonstrated a successful
M EEG was smaller than the minimum of 兵 M SUR 1, . . . ,s 其 . localization of the epileptogenic zone during seizure free in-

061907-6
INDICATIONS OF NONLINEAR DETERMINISTIC AND . . . PHYSICAL REVIEW E 64 061907

tervals, and the anticipation of seizures by analysis of multi- age any further statistical analysis of the set level which as-
channel EEGs recorded from epilepsy patients 关31,36 –39兴. sumes the sets to be homogeneous.
The results of these studies, as well as the present one, sug- Doubtlessly, sets under investigation exhibited distinct
gest that the pathological epileptic process imposes certain linear properties described by power spectra and amplitude
constraints on neuronal dynamics. Even in the absence of distributions. However, since these properties were shared by
seizure activity these constraints appear to be reflected by the surrogates, they cannot account for results given here. It
nonlinear deterministic traits in the EEG, as suggested by is important, however, to point out that a rejection of the
results found for set D. Most prominently, however, this phe- surrogates’ null hypothesis is only a necessary but not suffi-
nomenon was observed during seizure activity 共set E兲. This cient criterion for nonlinearity. Surrogates that were used are
finding is in correspondence with previous studies on intra stationary by construction. Therefore, even if a simple sta-
cranial 关29兴 and extracranial 关9,32兴 recordings of epileptic tionarity inclusion criterion was used to select the EEG seg-
seizures. Theiler 关32兴 even a priori assumed seizure activity ments, nonstationarity as a cause of ‘‘false’’ positive rejec-
to be ‘‘undoubtedly nonlinear.’’ tions cannot be excluded. Since this stationarity test is based
When comparing extracranial and intracranial recording on linear properties of the time series, it can neither be
locations, it is important to note that the latter integrate po- highly sensitive nor highly specific for nonstationarities of
tentials over a much smaller steradian, i.e., fewer neurons nonlinear dynamical systems. Nonlinear techniques calcu-
contribute to the measured potentials, which furthermore are lated in a reconstructed state space such as the one proposed
less filtered as compared to extracranial recording locations. in Ref. 关54兴 could help to overcome this shortcoming. Fur-
This might explain differences in results from sets A and C. thermore, Kugiumtzis 关55兴 showed that although the iterative
An additional and not contradictory explanation might be amplitude adjusted surrogates are more consistent in repre-
given by the following. Set C was measured from brain re- senting the given null hypothesis than older techniques 关56兴,
gions which were proven to be nonepileptogenic but which the remaining mismatch of linear correlations of the original
may nevertheless participate in secondary, nonautonomous time series can still be relevant, and can cause false rejec-
epileptic processes initiated by the epileptogenic zone. tions of the null. Since these and other shortcomings weaken
The significant numbers of rejections R min on the indi- the probative force of the applied method, we only use the
vidual level allow two different interpretations. On the one term indication rather than evidence of nonlinear determin-
hand, the sets could be assumed to have a certain distribution istic structures.
of some distinct dynamical property not included in the null It has become a common point of view that values of an
hypothesis. Due to the limited sensitivity of the applied test estimate of the correlation dimension calculated from an un-
statistics for this very property, the individual null will be known dynamical system cannot be taken as a true estimate
rejected only for segments in one tail of this distribution. of a number of degrees of freedom. Particularly, our results
Differences of R min values between sets could then be ex- give no indication of chaos in the underlying dynamical sys-
plained by different centers and widths of these distributions. tem brain. In a way this is to be expected, since a purely
Given the respective calculation parameters used in our chaotic behavior of brain functions would consequently im-
study, both higher values and a higher intergroup variability ply that our brains’ behavior is changed dramatically by each
of R min were found for P as compared to D 2,e f f . A compari- and every arbitrary small input.
son between Refs. 关4兴, and 关8兴, as well as data reported in In accordance with other studies, our results show that an
Ref. 关18兴 show analogous results. This could be interpreted application of NTSA measures to EEG dynamics offers in-
as a higher degree of sensitivity of P for indications of dy- sights into the dynamical nature and variability of the system
namical structures in EEG time series. The contrary conclu- brain. As a feedback for NTSA, complicated properties of
sion, i.e., a lower level of specificity, cannot of course be EEG dynamics can further motivate one to improve existing
ruled out. methods and develop new methods 关57兴.
On the other hand, the sets could consist of different sub-
ACKNOWLEDGMENTS
sets, each containing segments of different dynamical nature.
This idea was followed in Ref. 关8兴, where Stam et al. con- We are grateful to Wieland Burr, Thomas Kreuz, Thomas
cluded that their ‘‘study underscores the heterogeneous na- Schreiber, and Guido Widman for useful discussions. This
ture 关 . . . 兴 of the alpha rhythm from a dynamical point of work was supported by the Deutsche Forschungsgemein-
view.’’ This interpretation of different subsets would discour- schaft.

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