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July 6, 2010 8:55 WSPC/S0218-1274 02678

International Journal of Bifurcation and Chaos, Vol. 20, No. 6 (2010) 1723–1729
c World Scientific Publishing Company
DOI: 10.1142/S0218127410026782

STATISTICAL COMPLEXITY AND NONTRIVIAL


COLLECTIVE BEHAVIOR IN
ELECTROENCEPHALOGRAPHIC SIGNALS
M. ESCALONA-MORÁN
Grupo de Ingenierı́a Biomédica, Facultad de Ingenierı́a,
Universidad de Los Andes, Mérida, Venezuela
Laboratoire Traitement du Signal et de l’Image (LTSI),
Université de Rennes 1, Campus Scientifique de Beaulieu,
Bât. 22, 35042 Rennes Cedex, France
INSERM U642, LTSI, Bât. 22, 35042 Rennes Cedex, France
M. G. COSENZA
Centro de Fı́sica Fundamental,
Universidad de Los Andes, Mérida, Venezuela

R. LÓPEZ-RUIZ
DIIS and BIFI, Facultad de Ciencias,
Universidad de Zaragoza, E-50009 Zaragoza, Spain

P. GARCÍA
Laboratorio de Sistemas Complejos,
Departamento de Fı́sica Aplicada, Facultad de Ingenierı́a,
Universidad Central de Venezuela, Caracas, Venezuela

Received December 16, 2008; Revised July 27, 2009

We calculate a measure of statistical complexity from the global dynamics of electroencephalo-


graphic (EEG) signals from healthy subjects and epileptic patients, and are able to establish a
criterion to characterize the collective behavior in both groups of individuals. It is found that
the collective dynamics of EEG signals possess relatively higher values of complexity for healthy
subjects in comparison to that for epileptic patients. To interpret these results, we propose a
model of a network of coupled chaotic maps where we calculate the complexity as a function of
a parameter and relate this measure with the emergence of nontrivial collective behavior in the
system. Our results show that the presence of nontrivial collective behavior is associated to high
values of complexity; thus suggesting that similar dynamical collective process may take place
in the human brain. Our findings also suggest that epilepsy is a degenerative illness related to
the loss of complexity in the brain.

Keywords: Complexity; brain dynamics; collective behavior; coupled map networks.

1723
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1724 M. Escalona-Morán et al.

The concept of complex systems has become a new of individuals. It is found that the collective dynam-
paradigm for the search of mechanisms and a uni- ics of EEG signals possess relatively higher values
fied interpretation of the processes of emergence of complexity for healthy subjects in comparison to
of structures, organization and functionality in a that for epileptic patients. Our results support the
variety of natural and artificial phenomena in dif- view that epilepsy is characterized by a loss of com-
ferent contexts [Badii & Politi, 1997; Mikhailov & plexity in the brain, as indicated by measurements
Calenbuhr, 2002; Kaneko & Tsuda, 2000]. One com- of the dimension correlation [Babloyantz & Des-
mon criterion for defining complexity is the emer- texhe, 1986], algorithmic complexity [Rapp et al.,
gent behavior: collective structures, patterns and 1994], and anticipation of seizures [Martinerie et al.,
functions that are absent at the local level arise 1998].
from simple interaction rules between the constitu- In order to interpret our results, we propose a
tive elements in a system. Phenomena such as the model of coupled chaotic maps where we calculate
spontaneous formation of structures, organization, the measure of complexity as a function of a param-
spatial patterns, chaos synchronization, collective eter and relate this measure with the emergence
oscillations, spiral waves, segregation and differenti- of nontrivial collective behavior in the system. Our
ation, formation and growth of domains, and social results show that the appearance of nontrivial col-
consensus, are examples of self-organizing processes lective behavior is associated to high values of com-
that occur in various contexts such as physical, plexity; thus suggesting that similar dynamical col-
chemical, biological, physiological, social and eco- lective process may take place in the human brain.
nomic systems. Several measures of complexity have been pro-
There has been much interest in the study of posed in the literature. Here we employ the concept
the phenomenon of emergence of nontrivial collec- of statistical complexity, introduced by Lopez-Ruiz
tive behavior in the context of systems of interacting et al. [1995]. This quantity is based on the statistical
chaotic elements [Kaneko, 1990; Chaté & Man- description of a system at a given scale, and it has
neville, 1992a, 1992b; Pikovsky & Kurths, 1994; been shown to be capable of discerning among dif-
Shibata & Kaneko, 1998; Cosenza, 1998; Cosenza & ferent macroscopic structures emerging in complex
González, 1998; Cisneros et al., 2002; Manrubia systems [Sánchez & Lopez-Ruiz, 2005]. The amount
et al., 2004]. Nontrivial collective behavior is char- of complexity C is obtained by computing the prod-
acterized by a well defined evolution of macroscopic uct between the entropy H, and a sort of distance
quantities coexisting with local chaos. Models based to the equipartition state in the system, named the
on coupled map networks have been widely used disequilibrium D. Thus, the statistical complexity
in the investigation of collective phenomena that is defined as [Lopez-Ruiz et al., 1995]
appear in many complex systems [Kaneko & Tsuda, R R  
2000]. In particular, networks of coupled chaotic   1 2
C = H · D = −K ps log ps · ps − ,
maps can exhibit nontrivial collective behavior. s=1 s=1
R
A paradigmatic example of a complex system is
(1)
provided by the human brain. It consists of a highly
interconnected network of millions of neurons. The where H and D are, respectively, the entropy and
local dynamics of a neuron in general behaves as the disequilibrium; ps represents the probability
a nonlinear excitable element [Herz et al., 2006]. associated to the state s; R is the number of states,
From the signal of a single neuron, it is not possi- and K is a positive normalization constant. Note
ble to understand the highly structured collective that ps may vary for different levels of observation,
behavior and functions of the brain. reflected in R. The quantity C can sum up relative
In this paper, we investigate the relative com- values of complexity in a specific system at a given
plexity of the human brain by considering the level of description.
collective dynamics that arise from the local dynam- The EEG data base used in this study con-
ics of groups of neurons, as manifested in elec- sists of records from 40 individuals in an age
troencephalographic (EEG) signals. We calculate a range between 22 and 48 years old. These indi-
measure of complexity from the global dynamics viduals are classified into four groups: (I) a group
of EEG signals from healthy subjects and epilep- of 10 healthy subjects; (II) a group of 10 epilep-
tic patients, and are able to establish a criterion to tic patients receiving treatment with Phenobarbi-
characterize the collective behavior in both groups tal for at least 18 months; (III) a group consisting
July 6, 2010 8:55 WSPC/S0218-1274 02678

Statistical Complexity and Nontrivial Collective Behavior in Electroencephalographic Signals 1725

of 18 epileptic patients that have not yet received


medical treatment; and (IV) a group of two epileptic
patients who experienced spontaneous seizures dur-
ing the EEG recording. All the epileptic patients in
the data base were diagnosed generalized epilepsy
manifested through tonic-clonic seizures.
The record of the EEG signal from each indi-
vidual was carried out over 19 channels connected
to scalp electrodes according to the international
10–20 system [Jasper, 1958]. The potentials were
measured with respect to a reference level consisting
of both ears short-circuited. The signal was digital-
ized at a sampling frequency of 256 Hz and A/D
conversion of 12 bits, and filtered to bandwidth Fig. 1. Statistical complexity of healthy subjects (group I),
between 0.5 and 30 Hz. All the EEG signals were epileptic patients subject to treatment (group II), epileptic
recorded with the individuals at rest and with eyes patients without treatment (group III), and epileptic patients
closed, during a one-hour period, between 8 a.m. undergoing seizures (group IV). Vertical lines indicate the
limits for each group. The order of the individuals in each
and 10 a.m. We consider continuous segments of the
group does not have any meaning.
EEG signals containing between 15 000 to 30 000
points, with no significant artifacts.
A channel in the EEG signal represents an aver- of complexity correspond to the patients undergoing
age of a set of neurons in a specific part of the brain. epileptic seizures (group IV). This measure of com-
The 19 channels in each EEG can be considered as plexity allows us to discern between healthy sub-
simultaneous time series coming from different parts jects and epileptic patients. Among EEG signals
of an interacting dynamical network. The collective from epileptic patients, those signals from patients
behavior of such a dynamical network at a given under treatment seem to possess slightly greater
time t can be described by, the instantaneous mean complexity than those from patients without treat-
field ht , defined as ment. However, the quantity C is not very efficient
M for distinguishing between the different groups of
1  j epileptic patients. The spread of the values of the
ht = et , (2)
M complexity found in group I indicates a greater vari-
j=1
ability in the statistical properties of EEG signals
where ejt is the real value registered by electrode j from the healthy subjects.
at discrete time t, j = 1, . . . , M ; and M = 19 is the It is important to say that other choices for
number of electrodes. the partition of states of the EEG signal are pos-
The probability distribution of the mean field sible, and hence different values for the H and D
values corresponding to a given EEG signal is con- measures can be obtained, without affecting the
structed from the time series of ht calculated for overall behavior of the statistical quantity C. For
that signal. We define the number of states R as instance, Rosso et al. [2003] divided the time axis of
a partition consisting of R equal size segments on EEG signals into nonoverlapping temporal windows
the range of values of ht . Next, the probability ps on which the wavelet energy at different resolution
associated to the s state is calculated. Here we set levels can be calculated.
R = 103 for all the EEG signals. Then, Eq. (1) is In order to give an interpretation to the above
used to calculate the statistical complexity C asso- results, we propose a dynamical model. We consider
ciated to the mean field for each EEG. a system of N interacting nonlinear, heterogeneous
Figure 1 shows the statistical complexity of the elements forming a network, where the state of ele-
mean field of the EEG signal for all the individuals ment i (i = 1, 2, . . . , N ) at time t is denoted by
in each group from the data base. Figure 1 indi- xit . The evolution of the state of each element is
cates that the complexity measure for the global assumed to depend on its own local dynamics and
dynamics of the EEG signal is higher in healthy on its interaction with the network, whose intensity
subjects (group I) in relation to that of epileptic is described by the coupling parameter . Then, we
patients (groups II, III, and IV). The lowest levels consider a network of maps subjected to a global
July 6, 2010 8:55 WSPC/S0218-1274 02678

1726 M. Escalona-Morán et al.

interaction as follows [Cisneros et al., 2002]


N
 
xit+1 = (1 − )fi (xit ) + fj (xjt ), (3)
N
j=1

where the function fi (xit ) describes the local dynam-


ics of map i. The usual homogeneous globally cou-
pled map system [Kaneko, 1990] corresponds to
having the same local function for all the elements,
i.e. fi (xit ) = f (xit ). As local chaotic dynamics,
we choose the logarithmic map f (x) = b + ln |x|,
x ∈ (−∞, ∞), where b is a real parameter. This
map does not belong to the standard class of uni-
versality of unimodal or bounded maps. Robust
chaos occurs in the parameter interval b ∈ [−1, 1],
with no periodic windows and no separated chaotic
bands on this interval [Kawabe & Kondo, 1991].
Heterogeneity in the maps is introduced by con-
sidering fi (xit ) = bi + ln |xit |, where the values bi
are uniformly distributed at random in the interval
[−1, 1].
As the macroscopic variable for this system, we
consider the instantaneous mean field defined as
N
1 
ht = fj (xjt ). (4)
N
j=1

Figure 2(a) shows the bifurcation diagram of


the mean field ht of the globally coupled heteroge-
neous map network, Eq. (3), with bi ∈ [−1, 1] and
N = 104 , as a function of the coupling strength .
For each value of , the mean field was calculated at
Fig. 2. (a) Bifurcation diagram of ht as a function of  for
each time step during a run of 102 iterates starting
a coupled heterogeneous map network, Eq. (4), with bi ∈
from random initial conditions on the local maps, [−1, 1] and N = 104 . (b) Bifurcation diagram of a local map
uniformly distributed on the interval xi0 ∈ [−8, 8], xit versus , exposing the underlying chaotic dynamics. (c)
after discarding 103 transients. The local maps are Complexity C as a function of .
chaotic and desynchronized (see Fig. 2(b)). How-
ever, the mean field in Fig. 2(a) reveals the exis-
tence of global periodic attractors for some intervals in Fig. 2(a) shrink, indicating that the global peri-
of the coupling parameter. This is the phenomenon odic attractors become better defined in the large
of nontrivial collective behavior where macroscopic system limit.
order coexists with local disorder in a system of Figure 2(c) shows the complexity C of the
interacting dynamical elements. Different collective mean field as a function of . Here, the observa-
states emerge as a function of the coupling . In this tion level was set at R = 15. When the value of  is
representation, collective periodic states at a given small, the bifurcation diagram of ht shows a period-
value of the coupling appear as sets of vertical seg- one collective attractor, which implies that for this
ments which correspond to intrinsic fluctuations of parameter range the system follows the standard
the periodic orbits of the mean field. Increasing the statistical behavior of uncorrelated disordered vari-
system size N does not decrease the amplitude of ables that yield a single period for its mean field. At
the collective periodic orbits. Moreover, when N is the chosen level of resolution, the complexity mea-
increased, the widths of the segments that make a sure considers the macroscopical variable as laying
periodic orbit in the bifurcation diagrams such as in a single state, thus giving C = 0. The complexity
July 6, 2010 8:55 WSPC/S0218-1274 02678

Statistical Complexity and Nontrivial Collective Behavior in Electroencephalographic Signals 1727

C remains zero up to a critical value of the cou- coupled map network cannot be inferred from the
pling c  0.04. The onset of the complexity at the knowledge of the dynamics of a single map. Thus,
value c resembles a first order phase transition. As the lower values of complexity found in the global
the periodicity of the collective orbit increases, more dynamics of the EEG signals from epileptic patients
states are occupied by the probability distribution may be associated to a decrease in the ability to
of the mean field ht . The probability distribution of generate collective organization and functions in the
ht corresponding to a periodic collective state is not brain affected by such physiological condition.
uniform and consists of a set of distinct “humps”. A As we have mentioned, the measure of the sta-
nonuniform probability distribution and few occu- tistical complexity depends on the level of obser-
pied states lead to larger values of the complexity vation (number of states R) considered for the
C, as observed for the period-two collective orbit. computations. Figure 3(a) shows the statistical com-
When the system enters chaotic collective motion, plexity as a function of the number of states for the
more states are occupied by the probability distri- mean field value from an EEG signal of a healthy
bution of the mean field and therefore this proba- subject. In Fig. 3(b), a similar plot of ht is shown for
bility becomes more uniform. As a consequence, the the value of the coupling parameter  = 0.2 in the
complexity decreases. coupled heterogeneous map network, Eq. (3).
The emergence of ordered collective behavior Figure 3 shows that the measures of the com-
in the coupled map network, Eq. (3), cannot be plexity in both systems tend to constant, asymp-
attributed to the existence of windows of periodic- totic values when the number of states R is
ity nor to chaotic band splitting in the local dynam- increased. For the coupled map network, the num-
ics. Figure 2 shows that higher values of complexity ber of states used in the computations was R = 15,
are associated to the occurrence of nontrivial collec- while for the EEG signals we employed R = 1000;
tive behavior in a network of interacting dynamical these values lie in the corresponding asymptotic
elements. We have obtained similar results for dif- regime for each system.
ferent network topologies and different local map In the heterogeneous coupled maps network,
dynamics. This result adds support to the concept the size of the system N can be related to the min-
of complexity as an emergent behavior; in this case imum number of states or level of description Rc
the ordered collective behavior is not present at that should be used in the calculation of C. The
the local level. Furthermore, these results suggest width of a vertical segment in the bifurcation dia-
that similar dynamical collective processes may take gram of ht at the level of description Rc is given by
place in the human brain. From the dynamics of a R−1
c . In addition, we have observed that this width
single neuron as an excitable element it is not pos- is proportional to the statistical dispersion of the
sible in general to characterize the collective behav- points inside the segment, which in turn decreases
ior of the brain, as the collective behavior of the with the size of the system following the law of large

0.3 0.3
Complexity (C)
Complexity (C)

0.2 0.2

0.1 0.1

0 0
0 500 1000 1500 0 15 30 45 60 75 90
number of states (R) number of states (R)
(a) (b)
Fig. 3. (a) Complexity C as a function of R for the mean field from EEG signals for a healthy subject. (b) C as a function
of R for the coupled heterogeneous map network, Eq. (3),  = 0.2.
July 6, 2010 8:55 WSPC/S0218-1274 02678

1728 M. Escalona-Morán et al.

numbers as N 1/2 . Then, R. López-Ruiz acknowledges support from Post-


grado en Fı́sica Fundamental, Universidad de Los
1 1
∼ √ ⇒ N ∼ R2c , (5) Andes, Venezuela, during his visit there in July
Rc N 2008. P. Garcı́a thanks C.D.C.H.T, Universidad
thus, for a given system size N , it is possible to Central de Venezuela, for support. The authors
estimate the minimum number of states that should thank Hospital Luis Gomez Lopez, in Barquisimeto,
be considered for the computation of the statistical Venezuela, for providing the clinical data base and
complexity in this system. Correspondingly, for the diagnoses.
resolution level R = 15 that we employed in Fig. 2,
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sejo de Desarrollo Cientı́fico, Humanı́stico y statistical measure of complexity,” Phys. Lett. A 209,
Tecnológico (C.D.C.H.T.), Universidad de Los 321–326.
Andes (ULA), Venezuela, under grant C-1692-10- Manrubia, S. C., Mikhailov, A. & Zanette, D. H. [2004]
05-B. M. Escalona-Morán acknowledges support Emergence of Dynamical Order (World Scientifc,
from C.D.C.H.T.-ULA under grant I-1075-07-02-B. Singapore).
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