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Med Biol Eng Comput (2012) 50:689699

DOI 10.1007/s11517-012-0913-9

ORIGINAL ARTICLE

Modeling the relationship between Higuchis fractal dimension


and Fourier spectra of physiological signals
Aleksandar Kalauzi Tijana Bojic
Aleksandra Vuckovic

Received: 27 December 2011 / Accepted: 26 April 2012 / Published online: 17 May 2012
 International Federation for Medical and Biological Engineering 2012

Abstract The exact mathematical relationship between


FFT spectrum and fractal dimension (FD) of an experimentally recorded signal is not known. In this work, we
tried to calculate signal FD directly from its Fourier
amplitudes. First, dependence of Higuchis FD of mathematical sinusoids on their individual frequencies was
modeled with a two-parameter exponential function. Next,
FD of a finite sum of sinusoids was found to be a weighted
average of their FDs, weighting factors being their Fourier
amplitudes raised to a fractal degree. Exponent dependence
on frequency was modeled with exponential, power and
logarithmic functions. A set of 280 EEG signals and
Weierstrass functions were analyzed. Cross-validation was
done within EEG signals and between them and Weierstrass functions. Exponential dependence of fractal exponents on frequency was found to be the most accurate. In
this work, signal FD was for the first time expressed as a
fractal weighted average of FD values of its Fourier

A. Kalauzi (&)
Department for Life Sciences, Institute for Multidisciplinary
Research, University of Belgrade, KnezaViseslava1,
11000 Belgrade, Serbia
e-mail: kalauzi@imsi.rs
T. Bojic
Laboratory for Radiobiology and Molecular Genetics,
Laboratory 080, Vinca Institute of Nuclear Sciences,
University of Belgrade, p.fah 522, 11001 Belgrade, Serbia
e-mail: tijanabojic@vinca.rs
A. Vuckovic
Biomedical Engineering Division, School of Engineering,
University of Glasgow, Glasgow, UK
e-mail: aleksandra.vuckovic@glasgow.ac.uk

components, also allowing researchers to perform direct


estimation of signal fractal dimension from its FFT
spectrum.
Keywords Fractal dimension  FFT spectra 
EEG signals  Weierstrass functions  Higuchis method

1 Introduction
Physiological, especially EEG signals have been analyzed
for decades through linear and nonlinear methods. Among
the first group of methods, Fast Fourier Transform is by far
the most frequently used approach, transferring the signal
from time to frequency domain and yielding amplitude and
phase spectra. More recently, nonlinear methods, originating from the chaos theory, provided a separate and
(partly) independent set of information about the signal,
consequently about the system generating it [1, 2, 14, 22].
One of the most frequently used quantities was the fractal
dimension (FD), serving as a measure of signal complexity
[7, 12, 13, 17]. The term fractal dimension refers to a
non-integer or fractional dimension of a geometric object.
Applications of FD within this framework include those in
time domain and the ones in the phase space. In case of the
former, FD of the original waveform is directly estimated
in the time domain, where the original signal itself is
considered a geometric figure. Phase space approaches
estimate the FD of an attractor in statespace domain. The
phase space representation of a nonlinear, autonomous, and
dissipative system can contain one or more attractors with
generally fractional dimension. Geometric objects with
fractal dimension 1 \ FD \ 2, such as the famous Koch
curve, are characterized by the property of self-similarity.
Their points neither lie on a one-dimensional curve, nor

123

690

two-dimensional plane, but somewhere in between.


Strictly speaking, physiological signals do not meet this
requirement. However, signals can be observed as numerical approximations of true fractal objects, more complex
ones having a greater FD. This forms the basis for the
construction of algorithms for FD estimation.
Many authors investigated a possible connection
between linear and nonlinear measures with various successes [6, 8, 15, 16, 18, 21, 26]. Specifically, a number of
previous studies attempted to relate different partial spectral signal properties with its FD value. Fox [6] and Higuchi [8], among others, studied the relationship between
the power exponent and signal FD, but this result is valid
only for signals obeying the power law. On the other hand,
Navascues and Sebastian [16] derived a theoretical implicit
relationship between a signal FD and its discrete power
spectrum or its Fourier Transform [18], but related to signals that have previously been interpolated with a fractal
interpolation function. Recently, we tried to model a relationship between high frequency amplitudes ([8 Hz) and
Higuchi FD of EEG signals in anesthetized rats [21].
However, a general and direct explicit mathematical relationship between amplitudes (or powers) of Fourier components and fractal dimension of recorded experimental
signals is missing in the literature. In this article, we tried
to model one possible form of this link, directly relating
signal FD with Fourier amplitude spectra of recorded onedimensional signals. Optimal values of model parameters
were calculated on a set of 280 sixty-second EEG signals,
recorded from ten healthy adult individuals in two states of
vigilance (wake and drowsy) and on a set of Weierstrass
functions, having theoretically defined FD and covering
nearly the whole FD range.

Med Biol Eng Comput (2012) 50:689699

0 Nm
1
k 
1@X
N 1
absxm ik  xm i  1kA Nm
Lm k
k i1
k k
1
where (N - 1)/([(N - m)/k]k) represents a normalization
factor. All signal lengths, Lm(k), are further averaged
forming the mean value of the signal length, L(k), for each
k = 2, , kmax:
Lk

k
1X
Lm k:
k m1

Signal complexity, expressed as the fractal dimension,


FD, is finally estimated as the slope of least squares linear
best fit from the plot of log(L(k)) versus log(1/k).
If one applies Higuchis algorithm to surrogate sinusoidal waveforms, the resulting fractal dimension (FD) will
depend on two factors: frequency of the waveform itself
(fs), as well as the sampling frequency (fsamp). Dependence
of FD on the waveform frequency for two values of fsamp
is presented in Fig. 1. Fractal dimension calculated with
Higuchis algorithm does not depend on sinusoids
amplitude or initial phase.
It is possible to derive an exact analytical expression
for FD = u(fs, fsamp) strictly following the procedure
described in Higuchis work [7] (for details, please see
Appendix). However, due to its complexity, there is a
practical reason to model the process with a simpler
mathematical expression. From Fig. 1 it can be seen that

1.8

2.1 Dependence of FD on the frequency of sinusoids


and signal sampling frequency

1.6

FD

2 Methods and results

1.4

According to Higuchis algorithm [7], starting from N


signal samples x(1), x(2), , x(N), a new self-similar time
series Xkm , with progressively reduced sample frequency, is
calculated as:


 
Nk
m
Xk : xm; xm k; xm 2k; . . .; x m
k
k
for m = 1, 2, , k, where m stands for the initial sample;
k = 2, , kmax, is the degree of sample frequency
reduction, kmax is an arbitrarily estimated parameter [19,
20] and square brackets stand for the integer part of a real
number. Signal length, Lm(k), is then computed for each of
the k time series Xkm as

123

1.2
fb

1
0

10

15

20

25

30

fs (Hz)

Fig. 1 Dependence of Higuchis fractal dimension on frequency for


two series of computer-generated sinusoids with increasing frequencies (fs). Solid line sampling frequency fsamp = 256 Hz, dashed line
128 Hz. White symbols FD values calculated according to the exact
formula [20, see the Appendix] for (open triangle) fsamp = 256 and
(open circle) 128 Hz

Med Biol Eng Comput (2012) 50:689699

691

Higuchis FD reaches its theoretical maximal value FD = 2 at


different breakpoint frequencies: fb & 30 Hz in case of
fsamp = 256 Hz and fb & 15 Hz for fsamp = 128 Hz. Therefore, it is necessary to adopt FD = min{u(fs, fsamp), 2} if the
frequencies beyond fb are to be included (necessary in most
cases). Two simple models were tested:

NpoX
fsamp

1
FDh fi ; fsamp
Npo fsamp i1
2
ub fi ; fsamp

err2 =point

Exponential model
FD ufs; fsamp

min ae fsamp  expke fsamp  fs 1; 2

and 3. The results are presented in Fig. 2. In the lowest two


panels, square fitting error was calculated according to the
expression

Power model

n
o
FD ufs ; fsamp min ap fsamp  fskp fsamp 1; 2 ;
3

both presuming that FD ? 1 if fs ? 0. In order to compare


their validity, a series of 50 surrogate sinusoids was
generated, with equal amplitudes and random phases,
differing in fs: fi = 1, 2, , 50 Hz, i = 1,, 50. A
resampling procedure was then performed on each member
of this set, yielding a total of 500 signals (fsamp = 50, 100,
150, , 500 Hz). All their FD values were calculated using
Higuchis algorithm, FDh, with kmax = 8 [19] and each
curve, FDh(fi), differing in fsamp, was nonlinearly fitted
(Nelder-Mead algorithm, MATLAB 6.5) with models 2

x 10

-3

0.1

ap

ae

0.05

4
2
0

200

400

200

400

600

200

400

600

3.1

0.5

ke

3
2.9
2.8
0

200

2.7

400

0.001

err2/point

0.001

err2/point

Fig. 2 Model parameter and


square error values, obtained by
fitting FD = u(fs, fsamp) with
exponential model (2) (left
panels) and power model (3)
(right panels), for different
sampling frequencies

where ub(fi,fsamp) denotes nonlinear part of the model


u(fi,fsamp), where frequencies fi lie to the left of the
breaking point fb, i.e., where ub(fi, fsamp) B 2. Further,
Npo(fsamp) is the number of fitting points. It depends on
fsamp and is equal to the number of generated sinusoids for
which FDh(fi,fsamp) B 2. For fsamp = 50, 100, 150, 200,
250, 300, 350, 400, 450, 500 Hz, these numbers were
Npo = 6, 12, 18, 24, 30, 36, 42, 48, 54, 60, respectively.
As can be seen on the lowest panels of Fig. 2, exponential
model proved to be more accurate than the power model for
all sampling frequencies. More, parameter ae was very
weakly dependent on fsamp (ae = 0.02538 0.00037) and
could be treated as a constant. On the other hand, 1/ke was
directly proportional to fsamp: linear regression yielded
fsamp = 31.42144/ke ? 1.68349 Hz, with the corresponding
Pearsons coefficient r = 0.999997. Therefore, it can be
approximated with ke = 31.42/(fsamp - 1.68) & 31.4/fsamp

200

fsamp (Hz)

400

200

400

fsamp (Hz)

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Med Biol Eng Comput (2012) 50:689699

s, since for most physiological signals fsamp 1.68 Hz. In


case of exponential model and for fsamp = 256 Hz, breakpoint frequency could be calculated as:
ae expke fsamp fb 1 2 ) fb
1=ke 256  log1=ae
29:74 Hz:

1.4
1.35
1.3 FD(19Hz)=1.2871

Also, a relationship between fsamp and fb could be


established:

FD (Higuchi)

1.25
1.2
1.15

FD(13Hz)=1.1256

1.1
FD(8Hz)=1.0462

1.05

fb log1=ae =31:4  fsamp 0:117  fsamp :

FD(2Hz)=1.0029

2.2 Fractal dimension of a finite sum of sinusoids

0.95

Higuchis fractal dimension of the sum of two sinusoids is


dependent on their frequencies as well as their amplitudes.
In other words, FD of a signal given by:
yt y1 t y2 t
A1 sin2pf1 t u1 A2 sin2pf2 t u2

0.9

0.2

0.4

0.6

0.8

4
1.2

yt y1 t y2 t A1 A2 ka sin2pf1 t u1
1  ka sin2pf2 t u2 :

A1 FDy1 A2 FDy2
:
A1 A 2

1.1
1.05
1

123

A1 uf1 ; fsamp A2 uf2 ; fsamp


:
A1 A2

0.5

a1

k a2

Fig. 3 a Fractal dimension of the sum of two sinusoids with


reciprocally varying amplitudes. Solid line, two signals having
relatively close frequencies (f1 = 8 Hz; f2 = 13 Hz); dashed line, a
bigger difference in frequencies (f1 = 2 Hz; f2 = 19 Hz). b Fractal
dimension of the sum of three sinusoids (f1 = 5; f2 = 10;
f3 = 15 Hz), as function of the two corresponding relative amplitude
factors ka1 and ka2, according to (8)

The same is valid in case of three componential sinusoids:


yt y1 t y2 t y3 t A1 A2 A3

 ka1 sin2pf1 t u1 1  ka1 ka2 sin2pf2 t u2



1  ka2 sin2pf3 t u3
8
where ka1 = A1/(A1 ? A2 ? A3), ka2 = A2/(A2 ? A3). An
example of this type is presented in Fig. 3b, where the sum
contains sinusoids with frequencies f1 = 5 Hz, f2 = 10 Hz
and f3 = 15 Hz. Here FD(y1 ? y2 ? y3) lies between
FD(y1) = 1.0179 and FD(y3) = 1.1704 for all values of
ka1 and ka2. Therefore, for a finite sum of n sinusoids, by
generalizing (7) we obtain:

By substituting (2) into (6), we obtain:


FDy1 y2 

0
0.5

As stated before, FD is generally a function of A1, A2, f1


and f2. However, by introducing the concept of reciprocal
amplitude variability, we actually reduced the number of
independent variables to three: ka, f1 and f2. For a chosen
pair of sinusoids, by fixing f1 and f2, FD could be observed
as a function of only one variable: FD(y(t)) = f(ka). As
Higuchis FD is insensitive to signal amplitude, it is
convenient to assume that A1 ? A2 = 1. This dependence
is presented in Fig. 3a, for two cases where f1 and f2 differ
for 5 Hz and for 17 Hz.
In both cases FD lies within the limits set by FD values
of the two componential sinusoids, i.e., FD(y1) B
FD(y1 ? y2) B FD(y2), where equalities apply when ka = 0
or ka = 1. Therefore, FD(y1 ? y2) might be expressed, in the
first approximation, as a weighted average of FD(y1) and
FD(y2), where amplitudes act as weighting factors:
FDy1 y2 

1.15

FD

depends on A1, A2, f1 and f2. As in this case, only relative


amplitudes contribute to total FD, it is convenient to introduce
reciprocal (or inverse) amplitude variability, where two
amplitudes vary in opposite directions, their sum remaining
constant. This can be formulated by introducing a relative
amplitude factor, ka = A1/(A1 ? A2), (0 B ka B 1), allowing
the signal to be written as:

FDy  FD

n
X
i1

!
yi

n
P

i1

Ai ufi ; fsamp
n
P
i1

:
Ai

Med Biol Eng Comput (2012) 50:689699

693

FDy1 y2 
FDy1 y2 

ka

1  ka

1.12

1.08

kex = 2.25
2

err /N = 1.20x10

-4

R2 = 0.88027

1.06

adj

0.2

0.4

0.6

0.8

0.6

0.8

ka kex1 1  ka kex2

1.1

10

kex

ka kex1 FDy1 1  ka kex2 FDy2

1.14

1.04

ka kex FDy1 1  ka kex FDy2


kex

FD (Higuchi)

In case of two sinusoids, if the weighted average was


exactly as in expressions (6) and (7), dependence of
FD(y1 ? y2) on ka would be linear, resulting in two straight
lines in Fig. 3a. As this is not the case, models for these
dependencies should be nonlinear. Even if an exact formula
for FD(y1 ? y2) = f(ka) was found, analogous to
FD = u(fi, fsamp) derived in the Appendix, it would
be extremely complicated. A most direct nonlinear
generalization of (7) is to introduce the power function of
amplitudes, Akex, and explore whether the introduced
exponent kex depends on fi. We fitted the solid line of
Fig. 3a (FD of the sum of 8 Hz and 13 Hz sinusoids) with
two versions of the power function, differing in the number
of explanatory variables,

1.14

:
1.12

A significant reduction in square error per point (more


than 73 times), and a rise in R2adj from 0.880 to 0.998 was
obtained when expression (11) was applied (Fig. 4). The
fact that resulting values of kex1 = 4.07 and kex2 = 2.27
mutually differed (Fig. 4b), clearly indicated that kex was
dependent on fi. For assessing the fitting quality, we used
the adjusted coefficient of determination [23]:
R2adj 1  1  R2

nd  1
;
nd  par  1

FD (Higuchi)

11
1.1

1.08

kex1 = 4.07
kex = 2.27
2
2

-6

err /N = 1.63x10

1.06

Radj = 0.99837

1.04
0

0.2

0.4

where R stands for the ordinary determination coefficient;


nd is the number of data; par is the number of explanatory
variables (model parameters). As this coefficient is adjusted to the number of explanatory variables, its use is recommended whenever qualities of regressions, differing in
par, are to be compared (as in Fig. 4).
After substituting ka = A1/(A1 ? A2) and taking into
account that A1 ? A2 = 1, (11) reduces to

kex1

kex2
A1
A2
FDy

FDy2
1
A1 A2
A1 A2
FDy1 y2 

kex1
kex2
A1
2
A1AA
A1 A2
2

A1 kex1 FDy1 A2 kex2 FDy2


A1

kex1

A2

kex2

:
12

A1 kex1 uf1 ; fsamp A2 kex2 uf2 ; fsamp


A1

kex1

Fig. 4 Modeling Higuchis fractal dimension of the sum of two sinusoids


(8 and 13 Hz), with reciprocally varying amplitudes. Plus symbols indicate
calculated FD, solid line indicates fitted with model. a One explaining
variable, kex, Eq. (10). b Two explaining variables, kex1 and kex2, Eq. (11)

and in general case

FDy  FD

kex2

A2

n
P

!
yi

Ai kexfi ufi ; fsamp

i1
n
P

:
Ai kexfi

14

i1

Finally, if the exponential model for u(fi, fsamp) is applied,


!
n
X
FDy  FD
yi

i1
;

n
X
i1

n
P

Considering Eqs. (2) and (3),


FDy1 y2 

ka

i1



Ai kexfi min ae  expke fsamp fi 1; 2
n
P

:
Ai kexfi

i1

13

15

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694

Equation (15) could be applied directly to an amplitude


FFT spectrum of a finite length one-dimensional signal,
where Ai and fi = if0 represent amplitude and frequency of
the ith Fourier component, respectively, f0 being the frequency resolution. If calculated by (15), FD(y) can be
conveniently denoted as FD spectral. A mathematical
model for the function kex(fi) remained to be found. After
some elementary experimenting, we concluded that kex(fi)
should be modeled with an ascending monotonous function
of frequency. Namely, by introducing descending functions
for kex(fi), we either obtained senseless results for FD
spectral (e.g., values were either beyond the natural range
1 \ FD \ 2), or FD spectral deviated from Higuchis FD
more than in case of ascending functions.
2.3 Application of the spectral method
on physiological signals
To test our method, we looked for a sufficiently rich set of
physiological signals, covering as much of the FD range as
possible. We chose the collection of 280 EEG signals
described in our previous papers [3, 24]. All recordings
were performed in accordance with the medical ethical
standards after the subjects signed the informed consent
form approved by the local ethical committee. Ten adult
healthy human individuals (seven males and three
females), age 2535 (mean SD: 28.3 6.5) years,
without mental disorders, were recorded after passing a
neurological screening. The subjects were lying in a dark
room with their eyes closed. A neurologist was monitoring
their state of alertness and preventing them from falling asleep
beyond N1 of NREM sleep. The individuals were not previously subjected to any sleep deprivation or deviation from
their circadian cycles and have not been taking any medicine.
Electrodes were positioned at 14 locations (F7, F8, T3, T4, T5,
T6, F3, F4, C3, C4, P3, P4, O1 and O2) according to the
International 1020 System with an average reference. Signals were sampled at a rate of 256 Hz, band pass filtered
between 0.5 and 70 Hz (with a software 50 Hz notch) and
artifacts were removed manually based on a visual inspection.
Signals from all individuals were classified into wake and
drowsy periods independently by two neurologists. Only
those signal sequences for which both experts agreed as being
either clearly awake or drowsy were used in the study (60 s for
each state and each subject).
However, this set of signals, consisting mainly of alpha
EEG oscillations superimposed on the Brownian-type background [3], covered only a part of the FD range (approx.
1 \ FD \ 1.5). This limitation was caused by the nature of
the Brownian fractal motion itself, known to be the first
integral of white noise. In order to stretch the signal FD values
to the remaining higher range (approx. 1.5 \ FD \ 2), we
included the set of their first derivatives, numerically obtained

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Med Biol Eng Comput (2012) 50:689699

by calculating first consecutive differences, using the diff


command in MATLAB 6.5. As expected, this operation
resulted in substituting the Brownian with the white noise type
of background, leaving the oscillatory content essentially
intact (not shown). As expected, Higuchis FD of differentiated signals stretched to occupy the upper FD range (initial
EEG signals 1.087 \ FD \ 1.506; differentiated 1.218 \
FD \ 1.940). By uniting the two set of signals into one matrix
of data (15,360 data 9 560 EEG channels) almost the entire
FD range was covered.
We tested three relatively simple three-parameter
mathematical expressions to model the ascending dependence of exponent kex on frequency:

exponential kex(fi) = af 9 exp(-kf 9 fi) ? cf


power kex(fi) = af 9 (fi)kf ? cf
logarithmic kex(fi) = af 9 log(kf 9 fi) ? cf

and compared their performances, by minimizing square


error between Higuchis and spectral FD:
sig
2
1 X
FDhj  FDsj ;
Nsig j1

squerr=Nsig

16

where Nsig denotes the number of signals, (FDh)j and (FDs)j


stand for Higuchis and spectral FDs of the jth signal,
respectively. In order to calculate optimal numerical values
for parameters af, kf and cf, we developed original programs in
MATLAB 6.5 by which parameters were iteratively adjusted.
Namely, the system starts from an initial point in the parameter space, calculates the square error (16) for each of the eight
cube vertices in this space (cube size being determined by the
current accuracy) and moves to the minimal error vertex. The
procedure is repeated until a local minimum is reached.
Resulting optimized parameters, square errors per signal, as
well as the corresponding Pearsons coefficients of linear
correlation, are presented in Table 1.
As presented in Table 1, all models proved to be relatively successful, yielding Pearsons coefficient r [ 0.99
and squerr/Nsig \ 0.001. However, the exponential model
was most accurate according to both criteria (squerr/Nsig
and r). Due to large signal ensembles, all correlations were
highly significant, p  0.001.
If we introduce the exponential model into (15), spectral
FD could be calculated as:
FDspectral y
n


P
Ai af expkf fi cf min ae  expke fsamp  fi 1; 2
 i1
:
n
P
Ai af expkf fi cf
i1

17
By using (17), the corresponding scatter plot for the 560
EEG signals, with parameter values contained in Table 1,

Med Biol Eng Comput (2012) 50:689699

695

Power model

af

-0.620

6.11
0.0180

2.6

0.118

1.8

1.6

cf

2.43

squerr/Nsig

3.55 9 10-4

8.34 9 10-4

7.89 9 10-4

1.3

0.99613

0.99267

0.99307

1.2

6.10

0.124

0.119

cf
squerr/Nsig

2.23
5.20 9 10-4

0.99612

100

1.4

1.1

0.0192
-4.94
8.24 9 10-4
0.99398

13.86
0.828
8.10 9 10-4

0.99401

Results were obtained for 280 analyzed EEG signals, their 280
derivatives and the set of Weierstrass functions, at sampling frequency fsamp = 256 Hz, and calculated with at least three significant
digits

and for fsamp = 256 Hz, is presented in Fig. 5a. Each dot
corresponds to one signal, with Higuchis FD on the abscissa
and spectral FD on the ordinate. All FFT spectra were
calculated using one 60 s epoch per signal, frequencies of
Fourier components being fi = i/60 Hz, i = 1, 2, , 3,000,
in the frequency range 0.016750 Hz. However, according to
Eq. (17), for actual calculations only Fourier components
below fb = 30 Hz were used.
2.4 Application of the spectral method on Weierstrass
functions
We also used Weierstrass functions (Wf), as another set of
data suitable for this analysis. They spread evenly across
the whole FD range and their FD values could be set as a
parameter during their generation [5, 9, 10, 12]. Analytically, they can be written as:
X
WHc t
ciH cos2pci t;
i

where c [ 1 and 0 \ H \ 1, H = 2 - FD, i = 1, , 400.


For each value of parameter c = 1.1, 1.2, , 3.0, a set of
99 Wf was generated, having FD = 1.01, 1.02, , 1.99;
the total number of signals being 20 9 99 = 1,980. Fractal
dimensions of all functions were analyzed both by Higuchis algorithm, using kmax = 8 [19, 20], as well as using
expression (15), for each of the three kex(fi) models. These
results are also presented in Table 1. Again, exponential
model showed the best results, according to both criteria.

1.1

1.2

1.3

1.4

1.5

1.6

1.7

1.8

1.9

FD Higuchi
2
1.9
1.8
1.7

FD spectral

kf

50

frequency (Hz)

1.38

Weierstrass functions
-0.870

1.5

0.0860

af

2.2
2

1.7

kf

-4.39

17.65

2.4

1.8

Logarithmic
model

EEG signals

2
1.9

FD spectral

Exponential
model

kex

Table 1 Optimized parameter values (af, kf and cf); minimized


square error per signal (squerr/Nsig); and Pearsons coefficient of
linear correlation (r) for the three models describing the dependence
of kex on frequency

1.6
1.5
1.4
1.3
1.2
1.1
1
1

1.1

1.2

1.3

1.4

1.5

1.6

1.7

1.8

1.9

FD Higuchi

Fig. 5 Scatter plot depicting Higuchis (abscissa) and spectral


(ordinate) FD data. a For each of the 280 EEG signals as well as
their 280 derivatives (560 points); b for the analyzed Weierstrass
functions (1,980 points). Calculations were done using expression
(17), with parameter values contained in Tables 1 and 2. The
corresponding dependence kex(fi) is presented as an inlet plot in the
upper left corner of (a)

The corresponding scatter plot is presented in Fig. 5b. Each


dot corresponds to one Wf, with Higuchis FD on the
abscissa, spectral FD on the ordinate. The latter were calculated with exponential parameters contained in Table 1
and using fsamp = 256 Hz.
2.5 Testing the method by cross-validation
In order to test the reliability of the obtained results, we
formed a new ensemble of EEG signals by randomly
splitting the available set into two equally large halves,
reducing thus each subset to 280 signals. Parameters of all

123

696

Med Biol Eng Comput (2012) 50:689699

Table 2 Mean standard deviation of 20 optimized parameter values (af, kf and cf); 20 minimized square errors per signal (squerr/Nsig) and 20
Pearsons coefficients of linear correlation (r), obtained for each model on each half from 10 random splits of the initial EEG signal set into two
Exponential model
af

-0.620 0.009

kf

0.0860 0.0019

cf

2.43 0.01

squerr/Nsig
r
Cross-validated squerr/Nsig
Cross-validated r

Power model

Logarithmic model

6.22 0.13

0.118 0.003

0.0178 0.0003

17.52 0.49

-4.50 0.12

(3.53 0.30) 9 10-4

1.38 0.01

(8.28 0.78) 9 10-4

0.99615 0.00034

(7.84 0.75) 9 10-4

0.99273 0.00070

(3.63 0.30) 3 1024

0.99312 0.00067

(8.46 0.79) 3 1024

0.99610 0.00036

(8.03 0.76) 3 1024

0.99267 0.00092

0.99305 0.00089

Bolded Mean standard deviation of the 20 square errors and 20 Pearsons coefficients after cross-validations performed between each of the
two corresponding halves of EEG signals

123

2
r = 0.99637
squerr/N = 0.000335

1.9

sig

FD spectral

1.8
1.7
1.6
1.5
1.4
1.3
1.2
1.1
1
1

1.1

1.2

1.3

1.4

1.5

1.6

1.7

1.8

1.9

1.7

1.8

1.9

FD Higuchi

2
r = 0.99376

1.9

squerr/N

sig

= 0.00315

1.8

FD spectral

three models were optimized on the first subset and used to


calculate spectral and Higuchis FD for each signal of the
second subset and vice versa, using fsamp = 256 Hz.
Square errors per signal, according to (16), and Pearsons
coefficients of linear correlation were calculated for each
training subset separately, as well as for the other, crossvalidated subset. In order to increase statistical weight of
the validation, this procedure was repeated ten times,
yielding 60 values for each of these quantities (20 per
model). The results are summarized in Table 2.
It is important to note that all 120 coefficients of linear
correlation, 60 values for the training set and 60 for crossvalidated sets, were r [ 0.99 (not shown in Table 2). As
can be seen in Table 2, in case of all three models, square
errors per signal were slightly greater for the cross-validated than those obtained for the training sets, while
Pearsons coefficients, as expected, were slightly reduced.
However, these differences were not significant. According
to MannWhitney U test (SPSS 13.0 for Windows), in case
of square errors Z = -1.298, p = 0.194 for the exponential; Z = -0.812, p = 0.417 for the power; Z = -0.920,
p = 0.358 for the logarithmic model. For Pearsons coefficients, the values were Z = -0.514, p = 0.607; Z =
-0.054, p = 0.957; Z = -0.149, p = 0.882, respecting
the same order. One example of such a cross-validation for
the exponential model is presented in Fig. 6a.
Somewhat less favorable results (except for the exponential model) were obtained when spectral FD for the set
of Weierstrass functions was analyzed with parameters
optimized for EEG signals, and vice versa. Specifically,
Pearsons coefficients were 0.99478 for the exponential,
0.98946 for the power and 0.98998 for the logarithmic
model when EEG was used as the training set; the values
were 0.99376 for the exponential, 0.97159 for the power
and 0.97225 for the logarithmic model when the system
was trained on Weierstrass functions. Square errors per
signal were 9.66 9 10-3 (exponential), 1.79 9 10-2
(power) and 1.71 9 10-2 (logarithmic) when EEG was the

1.7
1.6
1.5
1.4
1.3
1.2
1.1
1

1.1

1.2

1.3

1.4

1.5

1.6

FD Higuchi

Fig. 6 Cross-validation results. a One case (out of 20) in which one


random half of the EEG set was tested by exponential model
parameters previously optimized on the other half. b Cross-validation
where the whole EEG set was tested by exponential model parameters
optimized on Weierstrass functions. Pearsons coefficient and square
error per signal are indicated in the upper left corners

Med Biol Eng Comput (2012) 50:689699

training set; 3.15 9 10-3 (exponential), 2.34 9 10-2


(power) and 2.29 9 10-2 (logarithmic) when Weierstrass
functions were used as the training set. Again, exponential
model proved to be most successful, as both corresponding
correlations exceeded 0.99. Square errors per signal were
smaller for one order of magnitude in case of exponential,
compared to the other two models, although greater than in
intra-EEG cross-validation. The result of EEG/Wf crossvalidation is shown in Fig. 6b, where spectral FD values of
EEG signals were calculated with exponential model
parameters optimized on Weierstrass functions. A small
systemic FD spectral overestimation in the lower FD
Higuchi region appeared and is yet to be explored in future
work.

3 Discussion
A number of attempts were previously made to find a
relationship between signal spectral properties and its
fractal dimension. Fox [6] and Higuchi [8] established a
widely used connection between fractal FD and the exponent a, FD = (5 - a)/2, but valid for signals with powerlaw of the power spectral density, Pf / f a , and only in
the middle range of exponent a values (1 \ a \ 3). A
positive complexityfrequency correlation was noticed in
some earlier works. Ziller et al. [26] obtained a high statistical correlation between an index of mean frequency of
EEG and FD, performing a comparative study between
nonlinear indices and Hjorth methods by means of factor
analysis.
It was already noticed that in complex spectral profiles,
amplitude variations in different frequency regions could
have opposite effects on signal FD, indicating that it might
be the result of some kind of averaging. Our experiments
with unilateral cerebral injury in rat [11] revealed that a
direct and significant correlation (r = 0.8115) existed
between FD and signal power in the EEG gamma frequency range (32128 Hz), both quantities being increased
after the injury. As well, in our very recent work [21] we
found that an increase in signal FD could be obtained by
simultaneous increase in amplitudes in the higher frequency range ([8 Hz) of surrogate-filtered white noise.
The process was modeled mathematically and well correlated with the corresponding measurements of EEG in
anesthetized rats. However, in a somewhat lower frequency
range (alpha), an opposite phenomenon was observed in
humans. Using the same set of signals as in the present
study, we found an inverse relationship between signal
alpha amplitude and its FD and applied a four-parameter
logistic function to model the relationship [3]. Again, this
was a partial result, since the proposed model is valid only
for signals where one physiological oscillation is

697

superimposed on the existing background noise [3, 4]. All


these findings treated the spectralfractal link partially,
lacking a full mathematical connection between the two
quantities, valid for any frequency range. Our present work
could therefore be regarded as a generalization of the
results described in these studies, the obtained relationship
being applicable to signals with any spectral profile.
Relationship between monofractal, multifractal and
spectral measures of the human EEG, in different scalp
locations and sleep stages, was recently investigated [25].
The authors found that cross-correlations between these
measures had specific topographic and sleep stage properties. They also concluded that a multifractal measure
(range of fractal spectra, DD) was the best at sleep stage
classifications. Although we treated EEG signals in this
work as monofractal, as the first approximation, the results
reported in [25] suggest that it would be promising to
extend our approach to explore the relationship between
spectral and multifractal measures of EEG signals.
Dependence of such new modeling parameters on scalp
locations, in different sleep stages, might also yield new
insights into properties of human EEG.
According to data presented in Tables 1 and 2, the
question of choosing one among the three presented
models is still not resolved, as their performances turned to
be relatively comparable in case of physiological signals.
However, at this point, we would recommend using the
exponential model, as it performed best both when used on
separate sets as well as in cross-validation tests. This issue
will probably be resolved with the analysis of additional
signals, or with the appearance of a new and better model.
In an attempt to explain the nature of the obtained
relationship between a linear and a fractal quantity, let us
observe formula (17) and the inlet of Fig. 5. If kex was not
dependent on frequency but was rather fixed at values
kex = 1 or kex = 2, we would interpret signal FD as being
a weighted average of FDs of Fourier components with
either Fourier amplitudes or powers as weighting factors.
However, according to their fractal dimensionality,
weighting factors could be comprehended as new spectral
quantities, and we could even observe Ai (fi)kex(fi) as a new
type of spectrum.
In conclusion, beside finding that signal fractal dimension can be estimated as a fractal weighted average of its
Fourier component FDs, the presented approach could
provide a practical help to researchers when analyzing
biological time-series characterized with complex dynamics (EEG, ECG, respiration, etc). With our method, signal
FD could be calculated immediately after the FFT, rather
than running a separate FD algorithm. In future, we expect
our model parameters to be further refined, if tested on a
wider ensemble of signals. Finding a more suitable model
for the dependence of the exponent kex on frequency may

123

698

Med Biol Eng Comput (2012) 50:689699

also improve the technique, together with a sophistication


of the basic analytical expression itself (e.g., by introducing
a more realistic type of averaging).
Acknowledgments This work was financed by the Ministry of
Education and Science of the Republic of Serbia (Projects OI 173022
and III 41028). We thank Dr. Vlada Radivojevic and Mr. Predrag
Sukovic for their help and cooperation in obtaining and analyzing the
data and Dr. Zarko Martinovic for second opinions in visual analysis
and scoring of EEG records.

Appendix

where


4N  1a2
k
A Nm 2 sin2 xDt ;
2
k

k Nm


sin
1 kxDt
k
C
:
2 sinkxDt

Nm
B

As m appears within the square brackets as well, cosine


summation rule over index m cannot be performed
directly. Respecting that for most signals N  m,

 N 
therefore Nm
 k , after some elementary operations
k
equation (19) could be written as

 


k
1X
N
 1 kxDt u
L k
AB AC cos m2xDt
k m1
k
!


k
:
A cos2 mxDt  xDt u
2
2

We shall derive an exact expression linking the frequency


of a mathematical sinusoid with its fractal dimension,
according to the procedure described in [7]. In order to
apply trigonometric summation rules, instead of the absolute difference of signal samples, as in (1), we shall observe
the sum of squares
0 Nm
1
X
k 
1
N1
L2m k @
xm ik  xm i  1k2 A Nm :
k i1
k k
18

Finally, according to the summation rules,


L2 k

20

where
L1

Consequently, FD should be calculated according to a


slightly modified formula:
1
FD slopeln1=k; lnL2 k 1 k 1; . . .; kmax ;
2

AB AC
A

L1  L2
k
k
k

N 

k kxDt u sink 1xDt
 sinxDt


N
 cos
 1 kxDt u ;
k
cos


L2



k 1 sink 1xDt cos2u
k

 cos2  xDt u :
2
2 sinxDt
2

where
k
1X
L k
L2 k:
k m1 m
2

19

For a given sinusoid xi a sin xiDt u, where


i = 1, , N; a and u representing its amplitude and initial
phase and Dt = 1/fsamp, formula (18) becomes
0 Nm
X
k 
1
2
@
a sinm ikxDt u
Lm k
k i1
!
N1
a sinm i  1kxDt u2 Nm :
k k
After transforming the difference of sinuses into
product, and application of summation rule of squared
cosines over the index i, we can write
k
L2m k A B C cos 2m  xDt /
2
!

!


Nm
k
2

kxDt  cos m  xDt /


k
2

123

Expression (20) was verified by calculating FD of


x
sinusoids for f 2p
2; 4; . . .; 30 Hz; for fsamp = 256 Hz,
x
and f 2p = 1, 2,, 14 Hz, for fsamp = 128 Hz and the
results presented as symbols in Fig. 1.

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