Synchronization likelihood: an unbiased measure of generalized synchronization in multivariate data sets
Introduction
A central problem in the study of normal and disturbed brain function is the question how functional interactions take place between different specialized networks. Understanding the coordination between brain regions is important in the context of information processing in the healthy brain [4], [5], [6] but also in the case of neurological disease. Loss of neurons and connecting fibre systems may lead to diminished interactions and cognitive dysfunction such as in Alzheimer’s disease [7], whereas pathologically increased synchronization is the hallmark of epileptic seizures [2], [8]. Usually, functional interactions are studied by considering time series of electrical potentials (electroencephalogram (EEG)) or magnetic field strengths (magnetoencephalogram (MEG)) recorded from different brain areas. Similarities between these time series are taken to reflect functional influences between the neuronal networks generating the time series. Similarities between time series are commonly quantified with linear techniques, in particular estimates of the coherency, which is a normalized measure of linear correlation as a function of frequency (e.g. [9], [10]).
While this approach has produced a large body of knowledge on normal and pathological brain function, it has a number of limitations. First coherency estimates are not suitable to characterize non-stationary data with rapidly changing interdependencies. Possibly, modifications such as event-related coherence can overcome this limitation [11]. A more important limitation is that methods such as coherency only capture linear relations between time series, and may fail to detect non-linear interdependencies between the underlying dynamical systems. Recently a variety of methods have been proposed to detect more general types of interactions between dynamical systems. One line of research is based on the analytical signal concept [12]. Here, the instantaneous phase of both time series is computed, and interactions are quantified in terms of time-dependent n:m phase locking (n and m being integers). This approach has been successful in the study of EEG seizure data [13] and in the study of synchronization between muscle and cortical activity. However, this approach is only valid when the time series are approximately oscillatory. A more general approach is based upon the theory of non-linear dynamical systems. It was demonstrated in the 1980s and early 1990s that, contrary to intuition, two interacting chaotic systems can also display synchronization phenomena [14], [15], [16], [17]. Initially synchronization was understood as identical synchronization, implying equality of the variables of the coupled systems. In the context of unidirectionally coupled driver response systems Rulkov et al. [18] introduced the wider concept of generalized synchronization. Generalized synchronization exists between two dynamical systems X and Y when the state of the response system Y is a function of the state of the driving system X:Y=F(X). When F is continuous, and xi, xj are two points on the attractor of X which are very close together, then the corresponding points yi, yj on Y will also be close together. An important feature of generalized synchronization is that the corresponding time series need not resemble each other.
Since the concept of generalized synchronization was introduced, several algorithms have been proposed to detect this type of interdependencies in experimental time series. Rulkov et al. [18] proposed a mutual false nearest neighbours (MFNNs) parameter and another measure based upon the predictability of the response dynamics by the driver dynamics. The idea of using mutual predictions between driver and response systems was further elaborated by Schiff et al. [19] and later applied to seizure EEG data in [2], [8]. Arnhold et al. [1] proposed a very simple measure for non-linear interdependencies, which is based upon a ratio of average distances between index points, their nearest neighbours and their mutual nearest neighbours (the mutual nearest neighbours of xi have the time indices of the nearest neighbours of yi). All of these methods claim to be able to detect non-linear dependencies between systems as well as asymmetry due to driver response interactions. However, it has been shown that identifying the driver and the response system in the case of asymmetric interactions is not always straightforward [1], [20], [21]. Rather, the asymmetries in interdependence measures may reflect the different degrees of freedom of the two systems [1], [20]. Pereda et al. [3] have also shown that these measures do not only reflect interdependencies between the time series but are also influenced by the properties of the individual dynamical systems, in particular their dimensionality. Pereda et al. [3] propose to overcome this problem with appropriately constructed surrogate data. While this may be valid it is also somewhat cumbersome and difficult to use with non-stationary data.
In this paper we propose a synchronization likelihood measure S which avoids the bias pointed out by Pereda et al. and gives a straightforward normalized estimate of the dynamical interdependencies between two or more simultaneously recorded time series. The measure is closely related to the concept of generalized mutual information as introduced by Pawelzik and co-workers [22], [23] and this measure can also be computed in a time-dependent way, making it suitable for the analysis of non-stationary data.
This paper is organized as follows. In Section 2 we describe the synchronization likelihood S. In Section 3 we study the properties of S by applying it to a test system of two non-linearly coupled Hénon systems. The performance of S in the case of real EEG and MEG data is studied in Section 4. Finally, we discuss the main results, in particular the strengths and weaknesses of the proposed method in relation to other available algorithms, and propose some directions for future research in Section 5.
Section snippets
The synchronization likelihood
We consider M simultaneously recorded time series xk,i, where k denotes channel number (k=1,…,M) and i denotes discrete time (i=1,…,N). From each of the M time series embedded vectors Xk,i are reconstructed with time-delay embedding [24]:where l is the lag and m is the embedding dimension.
For each time series k and each time i we define the probability Pk,iε that embedded vectors are closer to each other than a distance ε:
Test signals
To study the properties of our proposed synchronization measure, the synchronization likelihood Sk,i, we consider two unidirectionally coupled chaotic Hénon maps as described in [19]. One of the systems X (with state variable xi) is the driver system and Y (with state variable yi) is the response system. y is a function of x:y=F(x). The coupled Hénon systems are described by the following difference equations:The strength of the
Epilepsy
In this section we demonstrate the potential applicability of S to human multichannel EEG and MEG data. An important field for application of synchronization measures is epilepsy. During epileptic seizures (and possibly even in the 10–20 min preceding a seizure [28]) the activity of different brain regions becomes highly synchronized. Previous studies have suggested that at least some of the dynamical dependencies during a seizure are non-linear [8]. As an example we study an EEG at the
Discussion
We proposed a novel measure of dynamical interdependencies between time series which preserves some of the strengths of other algorithms based on the concept of generalized synchronization while avoiding the bias as noted by Pereda et al. [3]. A minimum requirement for any synchronization measure is that it changes in a systematic way when the coupling strength between two dynamical systems increases. We used two coupled Hénon systems as a test bank following [19]. While this is a very simple
Acknowledgements
The EEG data analysed in this paper were recorded at the Department of Clinical Neurophysiology of the Leyenburg Hospital, The Hague. The MEG data were recorded at the MEG Centre of the Vrije Universiteit, Amsterdam. Subjects were referred by the outpatient clinic for memory disorders of the Vrije Universiteit (Prof. Ph. Scheltens; Dr. Y.A.L. Pijnenburg). We would like to thank the two anonymous referees for helpful comments on an earlier draft of this paper.
References (30)
- et al.
A robust method for detecting interdependencies: application to intracranially recorded EEG
Physica D
(1999) - et al.
Nonlinear interdependencies of EEG signals in human intracranially recorded temporal lobe seizures
Brain Res.
(1998) - et al.
Assessment of changing interdependencies between human electroencephalograms using non-linear methods
Physica D
(2001) - et al.
Use of non-linear EEG measures to characterize EEG changes during mental activity
Electroenceph. Clin. Neurophysiol.
(1996) - et al.
Complexity and coherency: integrating information in the brain
TICS
(1998) - et al.
Application of a neural complexity measure to multichannel EEG
Phys. Lett. A
(2001) - et al.
Magnetoencephalographic analysis of cortical activity in Alzheimer’s disease. A pilot study
Clin. Neurophysiol.
(2000) - et al.
EEG coherency. I. Statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales
Electroenceph. Clin. Neurophysiol.
(1997) - et al.
EEG coherency. II. Experimental comparisons of multiple measures
Clin. Neurophysiol.
(1999) - et al.
Event-related coherence as a tool for studying dynamic interaction of brain regions
Electroenceph. Clin. Neurophysiol.
(1996)
Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients
Physica D
Mutual information and global strange attractors in Taylor–Couette flow
Physica D
Investigation of non-linear structure in multichannel EEG
Phys. Lett. A
Anticipation of epileptic seizures from standard EEG recordings
Lancet
Testing for no linearity in time series: the method of surrogate data
Physica D
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