Journal of Neuroscience Methods 154 (2006) 149160

Towards a proper estimation of phase synchronization from time series

M. Chavez a, , M. Besserve a , C. Adam b , J. Martinerie a
a
b

LENA-CNRS UPR-640, Hopital de la Salpetri`ere, Paris, France

LENA & Epilepsy Unit, Hopital de la Salpetri`ere, Paris, France

Received 20 September 2005; received in revised form 25 November 2005; accepted 9 December 2005

Abstract
In experimental synchronization studies a continuous phase variable is commonly estimated from a scalar time series by means of its representation
on the complex plane. The aim is to obtain a pair of functions {A(t), (t)} defining its instantaneous amplitude and phase, respectively. However,
any arbitrary pair of functions cannot be considered as the amplitude and the phase of the real observable. Here, we point out some criteria that the
pair {A(t), (t)} must observe to unambiguously define the instantaneous amplitude and phase of the observed signal. In this work, we illustrate
how the complex representation may fail if the signal possesses a multi-component or a broadband spectra. We also point out a practical procedure
to test whether a signal, not displaying a single oscillation at a unique frequency, has a narrow-band behavior. Implications for the study of phase
interdependencies are illustrated and discussed. Phase dynamics estimated from electric brain activities recorded from an epileptic patient are also
discussed.
2005 Elsevier B.V. All rights reserved.
Keywords: Phase synchronization; Time series; EEG; Epilepsy

1. Introduction
Phase synchronization of non-linear motions has recently
received attention in different research fields (Boccaletti et al.,
2002; Pikovsky et al., 2001). In neurosciences for example, one
of the most active topics is the study of the synchronization
mechanisms between neural populations. Evidence has lead to
the hypothesis that synchrony of neural assemblies (largely distributed local networks of neurons transiently linked by selective
interactions) would underlie the emergence of coherent global
behaviors (Engel et al., 2001; Schnitzler and Gross, 2005; Varela
et al., 2001). Based on theoretical studies of non-linear oscillators, experimental observation of phase synchronization has
been reported between different brain regions in both normal
and abnormal brain functions (Lachaux et al., 1999; Rodriguez
et al., 1999; Fell et al., 2001; Tallon-Baudry et al., 2004; Tass et
al., 1998).
In the theory of non-linear dynamics, the notion of phase is
related to the period of the limit cycle displayed by the system. If
the motion is, however, embedded in a complex attractor a phase
variable cannot be straightforwardly determined (Boccaletti et

Corresponding author. Tel.: +33 1 42161172; fax: +33 1 44243954.

E-mail address: mario.chavez@chups.jussieu.fr (M. Chavez).

0165-0270/$ see front matter 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.jneumeth.2005.12.009

al., 2002; Pikovsky et al., 2001). In experimental studies, the full

state of the system is not always accessible, but only one scalar
observable. A time series is currently represented on the complex
plane. By means of the analytic signal approach (Gabor, 1946)
one obtains a representation of the form z(t) = A(t) exp(i()(t)),
where the pair of functions {A(t), (t)} are related to the instantaneous amplitude and phase the real observable. This results
in a trajectory that rotates with a proper frequency (not necessarily unique and fixed) around a center. However, unless the
signal has a frequency narrow band behavior, this representation
may fail and the instantaneous phase cannot be properly defined
(Boashash, 1992; Cohen et al., 1999; Mandel, 1974; Oliveira
and Barroso, 1999; Picinbono, 1997; Vakman, 1996; Voelcker,
1966).
The usual solution is based on a band-pass filtering in order
to isolate a time scale, to which the analytic signal representation can be properly applied (Lachaux et al., 1999; Tass et
al., 1998). However, potential problems associated with filtering bandwidth have been pointed out (DeShazer et al., 2001;
Netoff and Schiff, 2002). In several experimental studies, the
Hilbert transform have been directly applied on neural activities possessing a relatively large (50 Hz) spectral support
(Freeman, 2004a,b; Freeman and Rogers, 2002; Jerger et al.,
2005; Mormann et al., 2003, 2000; Quian Quiroga et al., 2002).
The resulting complex representation z(t) = A(t) exp(i(t)) was

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M. Chavez et al. / Journal of Neuroscience Methods 154 (2006) 149160

then used to detect different phase dynamics related to both normal and pathological brain functions. In these works, authors
assume that the estimated variable (t) can define the instantaneous phase of the real observable, and they argue that it retains
information from the entire (broad) spectrum (Netoff and Schiff,
2002; Quian Quiroga et al., 2002).
In this work we show that this statement is not always true. In
fact, any arbitrary pair of functions {A(t), (t)} cannot define the
instantaneous amplitude and phase of a real observable. Further,
the application of the Hilbert transform to an arbitrary signal of
type x(t) = A(t) cos (t) does not necessarily result in a signal
of the form z(t) = A(t) exp(i(t)) (e.g. the Hilbert trans-form of
cos (t) may not be sin (t)). A practical consequence of this is
that the resulting instantaneous frequency (defined as the time
derivative of the instantaneous phase of the associated analytic
signal) does not correspond to a measurable frequency of the
observed signal x(t). This is particularly true for oscillations with
a broadband spectrum, as is often observed in neural activities. In
this work, we point out some practical criteria that the pair {A(t),
(t)} must observe to unambiguously define the instantaneous
amplitude and phase. We also point out a practical procedure
to test whether a signal, not displaying a single oscillation at a
unique frequency, can be considered as narrow-band. Developed
within information theory, these criteria are not always applied
in practical studies of phase synchronization.
In the context of phase synchronization of oscillators with
multiple time-scales, we illustrate some consequences of estimating a variable (t) from a broadband signal. We also illustrate
and discuss the implications for practical studies of phase interdependencies in epileptic brain dynamics. The structure of the
paper is as follows. In Section 2 we discuss the instantaneous
amplitude and phase of a signal. Main results are illustrated in
Section 3 by numerical simulations. Implications for the estimation of instantaneous phase from real signals are illustrated and
discussed in Section 4. Finally, the consequences for the study
of phase synchronization in brain signals are also illustrated and
discussed.
2. Phase of oscillatory signals
The phase of a dynamical system cannot be in general
uniquely defined. To define a phase of a continuous-time
autonomous system, it is necessary to locally define a variable
in the direction that corresponds to the zero Lyapunov exponent
(Boccaletti et al., 2002; Pikovsky et al., 2001). If the motion is
uniform, the phase is unambiguously defined by an angle in the
phase state.
In case of non-uniform limit cycles, a phase can be properly defined as a variable whose value is proportional to the
time between two crossings with a Poincare surface. However,
if the dynamics are more complex, a phase variable cannot be
straightforwardly determined. Quite often, the motion trajectory is projected on a plane such that it displays rotations around
some origin. An instantaneous phase is then determined as the
angle between the projection of each point and a particular direction on the plane (Boccaletti et al., 2002; Pikovsky et al., 2001).
Other geometrical projections are also possible to define a trajec-

tory such that it displays a cycle around a center (Osipov et al.,

2003).
2.1. Phase of scalar valued signals
In experimental studies, the full state of the system is not
always accessible, but only one scalar observation. In practice,
we want to represent any real observable as:
x(t) = A(t) cos (t),

(1)

where A(t) and (t) define the instantaneous amplitude and

phase, respectively. We notice that it is possible to associate
an infinite number of pairs {A(t), (t)} with any real signal
x(t). However, only well-defined pairs, referred to as canonical pairs, define unambiguously the instantaneous amplitude
and phase, i.e. there is a one to one correspondence between x(t)
and {A(t), (t)} (Cohen et al., 1999; Mandel, 1974; Picinbono,
1997; Vakman, 1996; Voelcker, 1966).
One solution is provided by the representation of the real
observable as a complex signal of the form z(t) = x(t) + iQ[x(t)],
where Q[] is an undefined operator. The objective is to obtain
a trajectory in the complex plane {x(t), iQ[x(t)]} whose phase
(t) is obtained through the representation z(t) = A(t) exp(i(t)).
The operator Q[] must, however, provide a pair of amplitude
and phase functions which verify some physical conditions
(Vakman, 1996):
(1) Amplitude continuity and differentiability: small perturbations to the signal x(t), should induce a corresponding small
change in the instantaneous amplitude A(t).
(2) Phase independence of scaling and homogeneity: scaling
the signal by positive constant c should have no effects on
the instantaneous phase and its derivative. Only the instantaneous amplitude should be scaled by c.
(3) Harmonic correspondence: the constant amplitude and
frequency of a simple sinusoid A0 cos(2f0 t + 0 ) should
remain their values, i.e. A(t) = A0 , (t) = 2f0 t + 0 .
Recently, a phase continuity condition has also been proposed to avoid the ambiguity that may arise in determining the
amplitude from z(t) when its magnitude is not positive-definite
(Cohen et al., 1999).
One solution is that provided by the representation of the real
observable as an analytic signal defined as x (t) = x(t) + iH(x(t))
(Gabor, 1946). Indeed, the analytic signal approach is the only
one, which does not violate the physical conditions mentioned
above (Cohen et al., 1999; Picinbono, 1997; Vakman, 1996). The
imaginary part of x (t) is the Hilbert transform of x(t) defined
as:

+
x(t)
1
d,
H(x(t)) = p.v.

where p.v. indicates that the integral is taken in the sense

of Cauchy principal value. In the frequency domain, the
Hilbert transform is obtained by applying a filter with response
i Sgn(f), where Sgn is the sign function (Panter, 1965). The
analytic signal represents thus a trajectory in the complex plane

M. Chavez et al. / Journal of Neuroscience Methods 154 (2006) 149160

{x(t), iH(x(t))} whose phase (t) can be defined through the

representation x (t) = A(t) exp(i()(t)).
If the real observable is of the form x(t) = (t) cos(w0 t +
) (the signal is purely modulated in amplitude), the pair
{(t), w0 t + } is canonical if and only if the spectrum of
(t) is zero for |f| > f0 , with w0 = 2f0 (Boashash, 1992;
Picinbono, 1997; Picinbono and Martin, 1983). Such spectral
conditions cannot, however, characterize any canonical pair
of the general form {A(t), (t)} (Picinbono, 1997; Picinbono
and Martin, 1983). Reciprocally, the fact that A(t) exp(i(t))
is the analytic signal of a real observation x(t) = A(t) cos()(t),
does not necessarily imply any spectral restriction for A(t) and
cos (t) (Picinbono, 1997; Picinbono and Martin, 1983; Vakman,
1996).
To consider A(t) exp(i(t)) as the analytic signal of
A(t) cos (t), the Hilbert transform of A(t) cos (t) must be equal
to A(t) sin (t) (Nuttall, 1966; Picinbono, 1997; Vakman, 1996;
Voelcker, 1966). Only if this latter condition is verified, the pair
{A(t), (t)} can be the canonical pair associated to the real signal
x(t).
To further discuss this point, it is necessary to use the
Bedrosian theorem about the Hilbert transform of the product of
two real functions (Bedrosian, 1963; Brown, 1974; Picinbono
and Martin, 1983). The main result of the theorem shows that,
if the spectral supports of two real functions x1 (t) and x2 (t) are
such that their Fourier transforms X1 (f) = 0 for f > B, and X2 (f) = 0
for f < B, then H[x1 (t)x2 (t)] = x1 (t)H[x2 (t)]; where H[] denotes
the Hilbert transform. A direct consequence of this theorem is
that:
H[A(t) cos (t)] = A(t)H[cos (t)],

(2)

when the spectral supports of A(t) and cos (t) do not overlap.
We must notice, however, that this does not necessarily imply
that:
H[cos((t))] = sin (t),

(3)

as required to define the pair {A(t), (t)} as a canonical pair.

2.2. The narrow band signals
The condition A(t) cos (t) + iA(t)H[cos (t)] = A(t) exp(i(t))
is verified for signals having their spectral support confined in
a narrow range centered on the main frequency of their spectra
(Boashash, 1992; Vakman, 1996; Voelcker, 1966; Picinbono,
1997). We must notice, however, that a canonical pair {A(t),
(t)} can unambiguously define the instantaneous amplitude
and phase of a signal whose spectrum does not necessarily
display a single oscillation with a unique and fixed frequency
(as a pure sinusoid modulated in amplitude). We can consider
for instance the case of the real chirp x(t) = cos(at2 ), whose
analytic signal is x (t) = exp(iat2 ) for t (Picinbono,
1997).
The narrow-band behavior implies that, for a real signal of the
form x(t) = A(t) cos (t), the relative variations of the amplitude
A(t) are very slow when compared with the variations of the
phase (t) (Delprat et al., 1992; Picinbono, 1997). This condition

directly implies that (Delprat et al., 1992):







 d(t) 
   1 dA(t)  ,

 A(t) dt 
 dt 

151

(4)

The more closely a signal approaches this bandlimited condition,

the more likely the pair {A(t), (t)} obtained with the Hilbert
transform will provide an accurate model for the real signal x(t).
3. When the instantaneous phase becomes meaningless
Mathematically, an infinity of pairs {A(t), (t)} can be generated for a unique complex representation. Nevertheless, the
relevance of an accurate model for the instantaneous amplitude
and phase follows not only from a mathematical convention, but
also from a physical interpretation.1
The instantaneous frequency of a real signal is currently
defined as the time derivative of the instantaneous phase of the
associated analytic signal  (t). However, a proper physical interpretation of the instantaneous frequency as the derivative of (t)
is only possible for some (very few) signals, with very particular spectral properties (Boashash, 1992; Cohen et al., 1999;
Loughlin and Tacer, 1997; Mandel, 1974; Nho and Loughlin,
1999; Nuttall, 1966; Oliveira and Barroso, 1999; Picinbono,
1997; Picinbono and Martin, 1983; Voelcker, 1966; Wei and
Bovik, 1998). As mentioned above, even though the Hilbert
transform can be applied to any arbitrary signal of the type
x(t) = A(t) cos (t), its complex representation may result to be a
function w(t) = B(t) exp(i(t)) for which the instantaneous frequency  (t) does not correspond to the physical (measurable)
frequency of the observed signal, obtained for instance, from
the successive zero crossings of x(t) (Callenbach et al., 2002;
Freund et al., 2003; Loughlin and Tacer, 1997; Mandel, 1974;
Oliveira and Barroso, 1999).
The instantaneous frequency of a signal with several spectral
components may paradoxically lie outside the frequency range
of the signal spectrum (Cohen et al., 1999; Loughlin and Tacer,
1997; Mandel, 1974; Oliveira and Barroso, 1999; Picinbono,
1997). This can be illustrated by the following example. Let
us to consider the two-tones signal x(t) = A1 exp(iw1 t) +
A2 exp(iw2 t) = A(t) exp(i(t)). The instantaneous frequency of
such signal is (Loughlin and Tacer, 1997; Mandel, 1974; Oliveira
and Barroso, 1999):
 (t) =

1
1
A2 A 2
(w2 + w1 ) + (w2 w1 ) 2 2 1
2
2
A (t)

(5)

where A2 (t) is the square of the instantaneous amplitude of the

analytic signal given by:
A2 (t) = A21 + A22 + 2A1 A2 cos((w2 w1 )t)

(6)

Although the signal is composed of two constant frequency

tones, its instantaneous frequency is time varying and displays
asymmetric deviations about the averaged frequency 0.5(w2 +
w1 ). A physical interpretation of the instantaneous frequency
1 By a physical interpretation we mean here that it can be physically measurable by a realizable system.

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M. Chavez et al. / Journal of Neuroscience Methods 154 (2006) 149160

can be done if it remains bounded by {w1 , w2 }. The condition

for this is (Loughlin and Tacer, 1997; Mandel, 1974; Oliveira
and Barroso, 1999):




A22 A21


1
 2
 A1 + A22 + 2A1 A2 cos((w2 w1 )t) 

(7)

The only possible solution is |A1 | = |A2 |, which yields a constant

instantaneous frequency at 0.5(w2 + w1 ). In case of asymmetric strengths,  (t) extends beyond the physical spectral range
without a physical consistency. A detailed discussion on more
general cases (e.g. time varying strengths A1,2 (t) or multicomponents signals) can be found in Loughlin and Tacer (1997) and
Oliveira and Barroso (1999). Similarly, if we consider now the
signal x(t) = A1 + cos(w1 t), we can straightforwardly see from
Eq. (5) that the instantaneous frequency becomes w1 only for
|A1  1. In contrast, for |A1 | 1 a proper physical interpretation
of the resulting instantaneous frequency is not possible. In practice, this case can be solved by a suitable transformation (e.g. a
demeaning) of the time series.
In general, if a real signal x(t) is monocomponent (it is
locally represented by one frequency and a spread about that
frequency) and narrow band, the instantaneous frequency  (t)
properly describes the frequency modulation law of the real
signal (Boashash, 1992; Cohen et al., 1999; Picinbono, 1997).
Further, for a monocomponent and narrow-band signal, the
instantaneous frequency estimated from its analytic signal is
always in accordance with a physically measured frequency, as
that obtained from the distance between successive zero crossings (Blachman, 1975; Boashash, 1992; Cohen et al., 1999;
Picinbono, 1997; Rice, 1982; Voelcker, 1966).
3.1. Accuracy of an estimated instantaneous phase
Practically, more closely an oscillation verifies the narrow
band condition given by Eq. (4), and H[cos (t)] = sin (t), more
likely the estimated pair A(t), (t) provides a proper model (with
a physical interpretation) for the observed signal. To illustrate
the relevance of an accurate model, let us consider the noisy
harmonic oscillator given by (Callenbach et al., 2002; Freund et
al., 2003).
x + x + 02 x =

(8)

Fig. 1. Signal x(t) and the associated phase (t) mod 2 obtained from Eq. (8)
for a D = 1. Vertical dotted lines indicate the times of zero crossing with a positive
slope. Vertical arrows indicate those zero crossings that are not accompanied by
the expected phase increase of 2.

with = 1 and natural frequency 0 = 1. Random forcing

is given by a Gaussian noise with
(t) =
v (t) = 0 and

(t)(t ) = 2D(t t ), where D is the intensity of the noise.

All our numerical examples were simulated by the Euler technique with a time step t = 0.005. For all simulations, a transient
of 104 points was discarded.
For a correct estimation of the instantaneous frequency of the
signal, an increase of 2 in the unwrapped instantaneous phase
should be observed at any zero crossing with positive slope. We
can notice in Fig. 1 that for our example, there are some amplitude crossings to positive x, at which (t) does not increase by 2.
As illustrated in Fig. 2, the observable of our example displays a
trajectory on the complex plane with multiple centers of rotation,
which renders difficult a correct estimation of the instantaneous
phase. A direct consequence is that the signal does not verify the
narrow band behavior, and H[cos (t)] = sin (t). Therefore, the
instantaneous frequency estimated from (t) cannot agree with
any physical frequency measured from the real signal x(t).
For the next example, let us consider the self oscillatory system perturbed by noise described by the following equations:
x = y,

y =
(1 x2 )y w2 x + (t),

(9)

where
= 0.1 and w = 1. Random perturbations are given by
a Gaussian noise (t), i.e.
(t) = 0 and
(t)(t ) = 2D(t t )
with an intensity D. The scalar observable is the variable x(t).

Fig. 2. (a): Trajectory of x(t) on the complex plane; (b): error H[cos (t)] sin (t); (c): the ratio
by the dotted line). For both plots (t) and A(t) were obtained with the Hilbert transform.

| (t)|
|A (t)/A(t)|

where  denotes time derivative (mean value is indicated

M. Chavez et al. / Journal of Neuroscience Methods 154 (2006) 149160

Fig. 3. Instantaneous phase (t) for the signal x(t) of the system given by Eq. (9). (a): narrow band behavior evaluated by the average ratio

153

| (t)|
|A (t)/A(t)|


as a function

of the noise intensity D 0.2 (dotted lines correspond to the mean values S.D. computed over 100 realizations with different random initial conditions); (b): power
spectra of x(t) for different noise levels (solid, dashed and slash-dotted lines correspond to the noise intensities D = 0, 1 and 10, respectively); (ce): trajectories on
the complex plane for different noise levels.

For D = 0 the motion describes a limit cycle at the frequency

w. The Hilbert transform yields a trajectory on the complex plane
with aclear unique
 center of rotation (Fig. 3(c)) and the average
| (t)|
ratio |A (t)/A(t)|  50, where
 denotes time average. The
pair {A(t), (t)} provides therefore an accurate model for x(t).
In contrast, if the noise intensity D is increased, the
 limit cycle

(t)|
becomes blurred by noise and the average ratio |A|
(t)/A(t)|
decreases (Fig. 3(a)) and the accuracy of the model decreases.
For D > 1, the variable  (t) cannot define anymore a physical
instantaneous frequency of the real observable. Qualitatively,
this can be observed on the complex plane by the fact that the
trajectory displays more and more multiple centers of rotation
(Fig. 3(d)(e)).

3.2. Relevance for the phase synchronization analysis

The use of the Hilbert transform in phase synchronization
analysis was introduced in Rosemblum et al. (1996). Since
then, most studies have dealt with phase-coherent oscillations
(motions which display a narrow and clear peak in the spectrum), for which the instantaneous phase can be straightforwardly defined (Boccaletti et al., 2002; Pikovsky et al., 2001).
For coupled non-coherent phase systems (as those displaying multiple time-scales oscillations) a phase synchronized
regime may also exist (Bove et al., 2004; Kiss et al., 2005;
Osipov et al., 2003), but nevertheless the phase dynamics is
not necessarily captured by the continuous phase variables
estimated through the Hilbert transform of the real observa-

Fig. 4. (a) Lyapunov exponents of the response system of Eq. (10) as a function of coupling strength
. Coupling strengths where the phase entrainment and
generalized synchronization appear are indicated by the vertical arrows. (b) Phase locking parameter obtained from the broadband signals (dashed curve) and
from the filtered signals (solid curve). Error bars were computed over 100 realizations with different random initial conditions. (c) Statistical significance of phase


locking values from filtered signals, expressed as S.D.{
} , from 1000 bootstrap realizations under the null hypothesis. The horizontal dotted line indicates where
values deviate more than 2 S.D.

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M. Chavez et al. / Journal of Neuroscience Methods 154 (2006) 149160

Fig. 5. (a) Example of the observed (x(t)) and filtered signals (xf(t)) from the system of Eq. (10); (b) power spectra of the observed and filtered time series; (cd)
trajectories on the complex plane of x(t) and xf(t), respectively.

tions (Bove et al., 2004; Kiss et al., 2005; Osipov et al.,

2003).
In contrast with these theoretical works, some experimental studies have claimed that the variable (t), estimated by
the complex representation of a broadband signal, may contain information from the entire (broad) spectrum and may
reflect the phase synchronized dynamics (Jerger et al., 2005;
Mormann et al., 2003, 2000; Netoff and Schiff, 2002; Quian
Quiroga et al., 2002). To illustrate a consequence of such erroneous assumption, let us consider a coupled system formed by
two multicomponent oscillators. Equations of motion read:
x = y,

y = Axy y(1 x2 ) Bx3 + C sin(xy t),

u = v,

v = Auv v(1 u2 ) Bu3 + C sin(uv t) +

(x u),

(10)

with Axy = 0.6, Auv = 0.2, B = 1, C = 2, xy = 0.6 and wuv =

0.65. Subscripts xy and uv refer to the oscillators described by the
variables (x, y) and (u, v), respectively. Parameters were set such
that both oscillators exhibit a chaotic motion for the uncoupled
case (Bove et al., 2004).
To evaluate the mutual entrainment, we have computed the
order parameter
(Boccaletti
et al., 2002; Pikovsky et al., 2001)



1 N
i
(t)
x,u
= N  t=1 e
 where x,u (t) = x (t) u (t) stands
for the difference between the continuous phase variables
obtained from the scalar observations (of length N) given by
variables x(t) and u(t). Weak synchronization results in a nearly
uniform distribution of the phase differences on the unit circle
and a small value of . In contrast, a phase synchronized state
yields a distribution of x,u (t) concentrated around a preferred
value, so that 1. Throughout this work, band-pass filtering
was performed with digital filters obtained from (N 1)th order
FIR filters with zero phase shifts.
To assess a significant phase locking different from null
hypothesis H0 (independence or unsynchronized state), we have

empirically estimated the distribution of under H0 by means

of a bootstrap method rather than asymptotic distribution theory (Efron and Tibshirani, 1993). This is obtained by randomly resampling with replacement, from the original x (t)
and u (t) independently, to generate another pair of observations {x (t), u (t)}. As this procedure destroys any dependence
between the two-phase variables, the distribution of under the
null hypothesis can be estimated. Further details of resampling
methods for circular variables can be found in Fisher (1995) and

Fig. 6. Schematic example of the brain structures explored by intracerebral electrodes, and the SEEG recordings of a seizure (electrodes have been superposed
on a basal view of a MRI brain slice). Electrodes labels stand for: (A) left temporal pole, (B) left amygdala, (C) anterior part of left hippocampus, (D) posterior
part of left hippocampus, (E) left posterior temporal lobe, (F) inferior left occipital lobe, (G) left occipital pole, (H) posterior part of right hippocampus and, (I)
anterior part of right hippocampus.

M. Chavez et al. / Journal of Neuroscience Methods 154 (2006) 149160

Allefeld and Kurths (2004). The block-bootstrap method used

here takes into account the local dependence structure in the data
by randomly drawing with replacement, blocks of observations
from the time series containing the phases variables x (t) and
u (t) (Politis et al., 1993). The blocks have a length L proportional to the correlation time of the original bandpass filtered
signals (twice the main period of the filtered signal). For all our
examples, qualitatively similar results were also obtained from
a classical surrogate data test (not shown) based on the Iterated
Amplitude Adjusted Fourier Transform (Schreiber and Schmitz,
2000) applied to the real signals.
To assess the significance of the values, the use of parametric tests of circular variables (as the Rayleigh or the Kuipers
test) may be an alternative statistics. Nevertheless, these meth-

155

ods assume the samples of the phase differences x,u (t) to be

independent. For real data estimated phase variables and their
differences are locally correlated in time; specially if they are
band-pass filtered. Parametric tests may therefore result in a very
stringent null hypothesis test: uniformity of x,u (t) on the unit
circle and independence of the samples. Moreover, parametric
test may become very sensitive to the marginal distributions of
the instantaneous phases (Fisher, 1995).
To investigate the region of couplings strengths where synchronization takes place, we have numerically computed the
Lyapunov spectrum (Boccaletti et al., 2002; Pikovsky et al.,
2001). For coupled non-autonomous systems, as that in Eq. (10),
the transition from independent motions to a phase synchronized
state follows the scenario described in Bove et al. (2004): at any

2
Fig. 7. Instantaneous phase of filtered SEEG
 signals,(a) the real time series in arbitrary units; (b) time-frequency content of the original signal |Wx (t, f)| (for a

definition see the text); (cd) average ratio

| (t)|
|A (t)/A(t)|

computed for the non-oscillatory activity (T = 010 s) and the rhythmic dynamics (T = 1020 s), as a function

of cut-off frequencies {f0 , f0 + bandwidth}; (ef) S.D. of the error H[cos (t)] sin (t) for the non-oscillatory and rhythmic activity, as a function of the cut-off
frequencies.

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M. Chavez et al. / Journal of Neuroscience Methods 154 (2006) 149160

2
Fig. 8. Instantaneous phase of an SEEG signal: (a) the real time series in arbitrary units; (b) time-frequency content 
of the original
 signal |Wx (t, f)| , with re-scaled

values in the dotted box area (new scale is indicated by the small color bar at the left of the box); (c) the average ratio

| (t)|
|A (t)/A(t)|

evaluated as a function of cut-off

frequencies {f0 , f0 + bandwidth}. Each matrix corresponds to the different activities within the gray boxes in (a).

value of the coupling strength, the system has always two zero
Lyapunov exponents, that correspond to the two times acting on
the non-autonomous systems. As coupling increases from zero,
the phase entrainment is manifested by the fact that one positive
Lyapunov exponent vanishes and remains zero for a broad range
of the coupling. In this state, the whole system shows at once
three zero Lyapunov exponents: the two corresponding to the
times, plus one that is a signature of a common phase. If coupling
is further increased, one of these three exponents becomes negative; indicating that complete (or generalized) synchronization
is set.2 Because the unidirectional coupling, the driver system
remains with one positive, one negative and one zero Lyapunov
exponent.
In Fig. 4(a) we report the estimated Lyapunov exponents of
the response system of Eq. (10) as a function of coupling strength

(computed according to the algorithm given by Eckmann and

Ruelle (1985), using a data length of 106 points).
In the absence of coupling the response system displays a
chaotic motion and thus, it has one positive, one negative and

2 This scenario contrasts with that observed between coupled autonomous

chaotic systems (Boccaletti et al., 2002; Rosemblum et al., 1996; Pikovsky
et al., 2001): in the absence of coupling each oscillator has one positive, one
negative, and one vanishing Lyapunov exponent. As the coupling is increased,
the positive and negative exponents remain, whereas one of the zero exponents
becomes negative.

one zero exponent. As coupling

increases, the positive exponent fluctuates around zero between 0.2 <
< 3.3. Finally, for

> 3.4 the response system has two negative and one zero Lyapunov exponents, which indicates that the synchronization is
established.
If phases are obtained directly from the broadband signals,
the resulting phase locking parameter does not capture the
phase dynamics of the coupled system, and it does not reflect
the phase synchronized state (Fig. 4(b)). In contrast, if an instantaneous phase is estimated from the slow time scales embedded
in signals (extracted by band-pass filtering the signals in the
frequency range = 0.6 0.25), the index properly reflects
the arising of a phase synchronization. For coupling strengths

1, phase-locking values of slow time-scales were found to

be significatively different from the null hypothesis of independence (Fig. 4(c)). This scenario also holds for the fast time-scale
oscillations (result not shown).
The poor results obtained from the broad-band approach
are explained by the fact that observations x(t) and u(t) have
multiple spectral components (Fig. 5(a) and (b)). The application of the Hilbert transform yields therefore a representation,
which exhibits multiple centers of rotation in the complex plane
(Fig. 5(c)), and the instantaneous phases cannot be well defined.
In contrast, the filtered signals display a clear peak in the spectrum, which leads to properly estimate the instantaneous phase
from the complex plane (Fig. 5(e)).

M. Chavez et al. / Journal of Neuroscience Methods 154 (2006) 149160

157

4. Implications for brain studies

To study the estimated phase dynamics of real data,
we have analyzed depth electroencephalographic signals (or
SEEG) from an epileptic patient candidate for a surgical
treatment. SEEG activities were recorded directly from brain
areas suspected to be involved in seizure generation (Fig. 6).
The number and the position of the depth electrodes were
determined by electrophysiologists and were not chosen for
the purpose of this study. SEEG signals were recorded by
means of depth electrodes using a common average reference, sampled at 400 Hz and bandpass filtered between 0.1 and
130 Hz.
4.1. Instantaneous phase of brain signals
The main problem in the estimation of an instantaneous phase
from neural data is related to the different time scales embedded in the signals. To evaluate whether the Hilbert transform
provides a proper instantaneous phase of SEEG time series we
have firstly band-pass filtered the signals with different bandwidths. Cut-offs frequencies were set to [f0 , f0 + bandwidth],
where the lower cut-off frequency f0 and the bandwidth were
independently varied from 2 to 30 Hz. For each filtered signal, we have then evaluated
condition by
 the narrow-band

(t)|
means of the average ratio |A|
.
As
mentioned
above,
(t)/A(t)|
if an oscillation is narrow band, its Hilbert transform yields a
pair of functions {A(t), (t)} such that H[cos((t))] = sin (t).
Following the relation (3), the more closely an oscillation
satisfies this condition, the more likely the estimated pair
{A(t), (t)} is a proper model yielding a physically interpretable instantaneous frequency. Here, the accuracy of this
approach was also evaluated by computing the S.D. of the error
H[cos (t)] sin (t).
Two typical situations are illustrated in Fig. 7. The signal
x(t) (recorded in the internal occipital region) displays two different dynamics: during the first half, an aperiodic activity can
be observed (open eyes condition), whereas a clear dominant
time scale at a frequency f 10 Hz appears in the second half
of the signal (closed eyes condition). As depicted in Fig. 7(d),
the oscillations containing the dominant frequency of the rhythmic discharge were found 
to fulfill the narrow band behavior
 (t)|
(a large value of the ratio |A|
(t)/A(t)| ), even in a large area
of the space parameters {f0 , f0 + bandwidth} (which includes
the region given by 0 < f0 < 12 and 0 < bandwidth 20). As
expected, the pair of functions {A(t), (t)} obtained from these
filtered oscillations verifies the condition H[cos((t))] = sin (t)
with low error values (Fig. 7(f)). This implies that, for oscillations in this region of the space parameters, the estimated variable (t) can straightforwardly define the instantaneous phase.
In contrast, for the non-oscillatory activity, an accurate model
of the instantaneous phase can be obtained only for the filtered oscillations with very narrow spectral support (Fig. 7(c
and e)).
As illustrated in Fig. 8(a and b), SEEG epileptic signals
exhibit often a time-varying spectra, i.e. they do not display

Fig. 9. Phase interdependencies computed from SEEG signals: (a) the real time
series in arbitrary units; (b) phase locking index, , estimated within a sliding
10 s window from the signals in the frequency ranges of 2030 Hz, 14 Hz and in


the broadband 190 Hz; (c) S.D.{
} , estimated from 1000 bootstrap realizations
under the null hypothesis.

a single oscillation at a unique frequency.3 An instantaneous

phase, properly denned for the rhythmic discharge observed during seizures, may be an improper model for the non-oscillatory
activity. This is illustrated in Fig. 8-(c): the oscillations embedded during the very rhythmic fast discharges observed at the
seizure onset (T = 2030 s) can be considered as narrow band
in a large area of the space
 {f0 , f0 + bandwidth},
 parameters
| (t)|
where the average ratio |A (t)/A(t)| takes large values. For
these narrow band oscillations, the estimated variable (t) is
an accurate model of the instantaneous phase. In contrast, for
the background activity (T = 212 s), or the spike and waves
discharge characteristic of the seizure (T = 3242 s), the estimated (t) can be properly associated to an instantaneous phase
3 Time frequency (TF) distributions were obtained by means of the wavelet
transform. A signal x(t) was convolved with a complex Morlets wavelet function
defined as w(t, f0 ) = A exp(t 2 /2t2 ) exp(i2f0 t). Wavelets were normalized
1/2
and thus A = (t )
. The width of each wavelet function (m = f0 / f ) was
chosen to be 7; where f = 1/2 t . TF content was represented as the energy of
the convolved signal: E(t, f0 ) = |w(t, f0 ) x(t)|2 .

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M. Chavez et al. / Journal of Neuroscience Methods 154 (2006) 149160

only in a very narrow region of the space parameters {f0 , f0 +

bandwidth}.
These results show that a band-pass filtering is necessary to
isolate a time scale for which an instantaneous phase can be properly defined. If the time series displays a clear dominant spectral
component (not necessarily at a unique and fixed frequency),
the complex representation provides an accurate model even if
the spectral support of the signal is relatively large. In contrast,
if the observable has a non-clear oscillatory behavior (as the
background activity), an instantaneous phase can be straightforwardly defined only for those oscillations obtained by a narrow
filtering.
We must notice that, although nonlinearities are not necessarily excluded from a signal with a narrow spectrum (Blachman,
1981, 1964), a very narrow band-pass filtering may induce an
important impairment in the temporal resolution, especially in

case of a time-varying spectrum, as that resulted from frequency

modulations. Therefore, a trade-off must be made between the
accuracy of the analytic signal model and the temporal resolution resulting form the filtering.
4.2. Phase synchronization of brain signals
As mentioned above, some empirical studies have reported
different phase synchronization phenomena in neural activities
possessing a relative broadband spectrum (Jerger et al., 2005;
Mormann et al., 2003, 2000; Netoff and Schiff, 2002). The rationale underlying these works is that the phase variables estimated
by the complex representation of broadband signals x(t) and
y(t), contains information from the entire spectrum and thus it
can reflect a phase synchronized state. However, a meaningful instantaneous phase can be obtained only from narrow band

Fig. 10. Matrices of synchrony between the SEEG signals: (a) the real time series, (b) matrices of values estimated from narrow band signals (2030 Hz) during
the two gray areas indicated in (a); (c) as in (b) but for the broadband signals (190 Hz). Signal labels are those of Fig. 6.

M. Chavez et al. / Journal of Neuroscience Methods 154 (2006) 149160

oscillations embedded in SEEG signals. The natural question

arises as to what is captured by a phase locking index when the
phases are estimated from unfiltered SEEG time series.
Let us firstly consider the temporal course of the estimated
phase locking index. For the pair of signals depicted in Fig. 9(a)
we have computed the parameter within a sliding 10 s window.
Results in Fig. 9(b and c) clearly show that index computed
from the broadband activities mainly detects the synchronization
of large spikes observed during the epileptic discharge. However,
the synchronized dynamics of low amplitude oscillations (as the
embedded fast oscillations present in the frequency range of
2030 Hz) are not taken into account. In fact, the synchronized
dynamics captured by the (t) of a broadband signal, is highly
biased by the oscillations with large amplitudes. The parameter
obtained from the signals filtered in the frequency band of
14 Hz (that corresponding to the spike and wave discharge)
yields a curve similar to that obtained from the unfiltered signals.
This can be explained by the fact that, as the Hilbert transform is
basically a non-local method (it is necessary to know the entire
signal to define H[x(t)]), short and small amplitudes may not be
taken into account (Callenbach et al., 2002; Freund et al., 2003).
The statistical significance of the values estimated from
narrow and broadband SEEG activities is illustrated in Fig. 9(c).
It is important to notice that, even though the instantaneous
phases are not properly defined, the phase-locking values may
result significatively different from a null hypothesis of independence. As explained above, the phases obtained from unfiltered
SEEG signals mainly capture the phase dynamics of oscillations
with large amplitudes. In the epileptic dynamics, these oscillations correspond to the spikes and waves discharges, which
are very synchronized. Thus, it is not surprising to find such
broadband correlations statistically significant. The pair-wise
phase-locking indices between all the signals in the recording are
reported in Fig. 10. During the large spike and waves (gray box
at T 3141 s), a large spatial region covering areas AG is suggesting by the broad-band approach as having strong interactions
(Fig. 10(c)). In contrast, during the same period, the narrow-band
filtering yields a more reduced region of strong interactions only
between the electrodes in areas GI (Fig. 10(b)). The broadband
approach mainly captures the synchronized state due to the large
oscillations, but cannot capture the wide synchronized dynamics of low voltage fast discharges observed at the seizure onset
(T 1828 s).
5. Conclusions
In this work we pointed out that the application of the
Hilbert transform to any signal of the type x(t) = A(t) cos (t),
may result in a complex representation w(t) = B(t) exp(i(t));
where (t) = (t). We stressed some criteria that the pair {A(t),
(t)} must verify to unambiguously define a proper instantaneous amplitude and phase of the signal. Practically, the more
closely an oscillation verifies the narrow band behavior, the more
likely the estimated variable  (t) corresponds to the physically
measurable instantaneous frequency.
For a monochromatic and narrow band signal, the complex
representation always yields a pair {A(t), (t)} which unam-

159

biguously defines the proper instantaneous amplitude and phase.

Bandpass filtering is therefore not an arbitrary operation to isolate a time scale of interest. It must, however, be guided by
a trade-off between the accuracy of the analytic signal model
and the temporal resolution, especially in case of frequency
modulations.
If a signal displays a non-oscillatory behavior (as the background activity in SEEG recordings) an instantaneous phase can
be properly defined only for those oscillations obtained by a narrow filtering. In contrast, if the recorded time series displays a
clear dominant spectral component (not necessarily at a unique
and fixed frequency), an accurate and meaningful model can
be obtained from those filtered oscillations containing the main
rhythmic discharge, even if they are filtered with a relatively
large bandwidth.
In the framework of phase synchronization, we have illustrated some consequences of estimating a variable (t) from
a broadband signal. Our simulations showed that, for coupled
oscillators with several spectral components, the broadband
approach cannot capture the phase synchronized dynamics. If
phase variables are estimated from unfiltered SEEG signals,
a phase synchronization analysis may be highly biased by the
large amplitudes. A phase locking test may even reveal high and
significant couplings between phase variables estimated from
broadband oscillations. Theoretical studies are therefore necessary to explain the meaning of these broadband correlations.
In the signal processing literature, different algorithms have
been provided for characterizing and extracting the instantaneous amplitude and frequency modulation laws from real time
series with different spectral components. Most of them rely on
a time-frequency representation (TFR) of signals. Under some
conditions (depending of the TFR used, the signal to noise ratio
and the spectral properties of the observed signal), the TFR
allows to separate the components located in distinct regions of
the time-frequency plane. A detailed description and discussion
of such algorithms can be found in Boashash (1992); Carmona
et al. (1997, 1999); Delprat et al. (1992); Le Van Quyen et al.
(2001); Oliveira and Barroso (1999) and Wei and Bovik (1998).
Adaptive or data-driven methods (Huang et al., 1998; Rossberg
et al., 2004) could also be an alternative for the analysis of multicomponent signals.
The approach presented here should be widely applicable in
different situations of practical interest as in Melice et al. (2001).
Although the concept of instantaneous phase has received an
increasing interest in different biological fields, the conclusiveness of any experimental study can be limited by an improper
use and interpretation of this valuable theoretical tool.
Acknowledgement
Special thanks are due to M. Rosemblum for valuable suggestions and critical reading of the manuscript.
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