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Patterns of attractor dimensions of sleep

EEG
Article in Computers in Biology and Medicine October 1995
Impact Factor: 1.24 DOI: 10.1016/0010-4825(95)00032-Y Source: PubMed

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Sadasivan Puthusserypady

National Institute of Mental Health an

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Compur.

Biol. Med. Vol. 25. No. 5, pp. 455-462,

1W5
Copyright
0 1W5 Elscvicr
Science Ltd
Printed
in Great Britain.
All rights reserved

INlO-4825&i $9.50+0.00

PATTERNS

OF ATTRACTOR
DIMENSIONS
EEG

N. PRADHAN,*

P.K.

S.
DUITS

SADASIVAN,*

CHATTERlIt

and

OF SLEEP
D.

NARAYANA

*Dept.
of Psychopharmacology,
National
Institute
of Mental
Health
& Neurosciences,
Bangalore-560029,
India;
*Dept.
of Psychiatry,
National
Institute
of Mental
Health
Neurosciences,
Bangalore-560029,
India;
and #Dept.
of Electrical
Communication
Engineering,
Indian
Institute
of Science,
Bangalore-560012,
India
(Received

3 October

1994;

in reuised

form

17 March

&

1995)

Abstract-Low
dimensional
chaos
is a property
of many
physiological
oscillatory
systems
including
the brain.
Time series of sleep EEG
records
have been analyzed
in the framework
of
recent
developments
in nonlinear
dynamics.
One of the characteristics
of a chaotic
time series is
its attractor
dimension.
The running
attractor
dimension
of a chaotic
time series
may reflect
changes
in states more accurately
than manually
scored
records.
In the present
study
the attractor
dimensions
of consecutive
EEG
segments
of five sleep records
were analyzed.
The block
of the
EEG
segment
(window)
was shifted
by various
lengths
along the entire
sleep data of each subject
thus producing
a running
attractor
dimension
curve
for each record.
The attractor
dimension
values
for different
sleep stages were significantly
different.
The pattern
of the running
attractor
dimension
closely
matched
the scored
hypnograms
in these five sleep records.
EEG
Attractor

Sleep
dimension

stages

Hypnogram
Running
attractor

Nonlinear
dimension

dynamics

Chaos

1. INTRODUCTION
The complicated dynamical behavior of the brain activity is reflected in the recording of
its electrical activity, the electroencephalogram
(EEG). As an individual moves from a
resting
awake
state
to
various stages of sleep, the EEG shows changes that are
characteristic of the respective sleep stage. Even though the sleep EEG has been
extensively studied using methods of time domain analysis and by the application of
spectral methods, the nature of the underlying neuronal processes has remained unclear.
Recent developments in the understanding of nonlinear dynamics and the theory of
chaos may be seen as a way out of the impasse of dealing with large scale cooperative
neuronal behavior [l]. Nonlinear dynamical analysis of EEG signals has been described
previously [2]. This paper analyses the physical and dynamical aspects of the brains
electrical activity during sleep from this new perspective and indicates possible future
directions in the analysis of transitional activities of the brain.
Sleep is considered to be a stable process and is universal in the animal kingdom. The
phylogeny of sleep has revealed an evolution whose complexity parallels the evolutionary process of the brain [3,4]. Two basic sleep behaviors are noticed in human beings:
quiet, resting, synchronized or nonrapid eye movement (NREM) sleep and an active
dreaming, desynchronised, paradoxical or REM sleep. In biological systems, the transition from chaotic dynamics to periodic behavior is often a marker of disease or
dysfunction as seen in epilepsy and coma for example [5]. Evidence suggests that chaotic
dynamics provide a mechanism for desynchronisation
of potentially
fatal
periodic
cortical behaviors by 10~ dimensional controls. The interposition
of REM within the
quasiperiodic slow wave sleep may be viewed from this angle. During wakefulness,
various behaviors are clearly not reflected as transitions in an EEG record. Therefore
sleep EEG with its established and known transitional states is a good candidate for
455

456

N.

Table

Subject
1
2
3
4
5

et al.

PRADHAN

I. Characteristics
subjects

of

Sex

Age

M
M
F
M
F

45
20
25
17
32

exploration through the application of nonlinear methods. In this paper, the importance
of the emerging trends of nonlinear dynamics and chaos to neurobiology is discussed in
the context of the various states of sleep behavior.
The attractor dimension is the most widely used measure to describe the chaotic
behavior of experimental time series data [6]. Several excellent reviews of the concept of
an attractor dimension have appeared recently [7,8]. The attractor dimension of a
system is the minimum number of dimensions of a phase-space that can contain the
trajectory generated by the system. The dimension of a system may be viewed as its
number of degrees of freedom [S]. The attractor dimension of periodic systems is a whole
number whereas the dimensions of chaotic systems are fractions. A comparison of
systems can be made by referring to this quantity. Researchers have mainly focused on
the absolute value of the attractor dimension (D2). It would be better, however, to
concentrate on how the value of D2 changes in response to changing states of brain
activity. The concept of a running attractor dimension may be useful in this context [9].
The changing state of the brain activity, as occurs during sleep, can be monitored
through the running attractor dimensions of the EEG. In this study we have analyzed the
various transitional states of the brain in sleep with reference to the attractor dimension
of the EEG signal.
2. DATA

COLLECTION

Five subjects in the age group 17-45 years were recruited for the study (Table 1).
These were normal volunteers without any history of neuropsychiatric illnesses or intake
of any psychotropic drugs. Subjects were acclimatised to the sleep laboratory for two
nights and polysomnographic
data was obtained using a Nihon Kohden polysomnographic system for the third night. Each recording session lasted 8 h. One channel (C3A2) of sleep EEG data along with the EOG (two channels) and EMG (one channel)
were acquired by direct digitization to a micro-computer
(PC-AT) through an ADC
coupled to an array processor (Data Translation, DT-2841, DT-7020) at 128 samples/s/
channel. For varying sensitivities, the EEG amplifier outputs ranged between 1.2 and
6.2 V which are of a sufficient magnitude for digitization by the 12 bit ADC with
adequate resolution [lo]. The data were ported to a high speed graphics workstation (HP
9000/735). The raw EEG signals were filtered through a bandpass (0.2532 Hz) 4th order
Butterworth filter twice cascaded. The EOG and EMG signals were also filtered through
low pass (1.0 Hz) and high pass (30.0 Hz) filters, respectively. The filtration removes
many unwanted signals (artifacts) and the filtered data are suitable for sleep scoring. A
computer assisted program was used to classify and score the sleep records as per the
manual of Rechtschaffen and Kales [ 111. In the present study two experienced polysomnographers scored all the records independently. They differed in their scoring of sleep
stages in less than 5% of the 30 s epochs. Differences were resolved by discussion and a
consensus rating assigned to the discrepantly scored epochs. The sleep pattern thus
scored is called a hypnogram.
The sleep EEG signal was further analyzed for the
attractor dimension values using singular value decomposition (SVD) methods [12,13].
The entire sleep EEG data were then analyzed in blocks using the technique of running
attractor dimension.

Patterns of attractordimensions
of sleepEEG
3. CALCULATION

OF ATTRACTOR

457

DIMENSION

Temporally the EEG is a single dimensional piece of data. Being a time series, the
EEG at any given instant of time has only one phase variable. A multidimensional phasespace can be constructed from the measurement of a single variable (like the electrical
potential) [14]. For a time series V(t), i=O, 1,2,3, . . . . N, the phase space vector
x(t) is constructed by assigning coordinates
x,(t) = V(t)
X?(f) = V(t+ T)

x,(t)=V(t+(d-l)T),
where T is a delay time and d is the embedding dimension. The lag or delay T is
determined by the first zero-crossing of the corresponding autocorrelation function [15].
We have used an embedding dimension, d= 16, in our study. After construction of the
multidimensional phase-space vectors from the EEG data segments, the attractor
dimensions are calculated.
4. SINGULAR

VALUE
APPROACH
FOR
ATTRACTOR
DIMENSION

ESTIMATION

OF

The dimension of the attractor is a characteristic feature of the underlying neuronal

process generating the EEG signals. The dimension value of the attractor is of
significance in feature detection of various brain states and in classification and differentiation of various types of neural activities including those occurring in a sleep cycle. The
attractor dimension directly reflects the degrees of freedom of the system under study.
Therefore, the nonlinear dynamics provide a model for signal generation and temporal
prediction which may help in determining the nature of neuronal processesgoverning the
state of brain activity in sleep.
The overall interpretation of a sleep record is based on a qualitative impression about
the changing patterns in EEG, EMG and EOG activity. The resulting picture, the
hypnogram, depicts the progressive transitional behavior of the brain during the sleep
cycle. This study utilizes the singular value decomposition of subsets of phase space
trajectories to evaluate the attractor dimension. The application of the SVD method to
EEG and its computational efficiency in comparison to the Grassberger Procaccia
Algorithm [7] has been described in detail elsewhere [12, 161. The data length requirement of the SVD method for its application to EEG analysis has been evaluated.
5. RUNNING

ATTRACTOR

DIMENSION

OF SLEEP

EEG

The technique of running attractor dimension has been used in this paper. A window
is applied to the EEG data in which the attractor dimension of the contents is calculated.
The window is moved along the EEG. By sliding the window it is possible to generate a
curve whose points correspond not only to the time axis of the time series, but reflect the
attractor dimension at any given time. In this study, we present the continuous attractor
dimension of sleep EEG data with the conventional hypnogram of the sleep record to
demonstrate the utility of running attractor dimension as a method for extracting
information on the transitional patterns of brain activity during sleep. The effects of
window length and shift have been studied to show the optimality of these two
parameters in a given application.
The attractor dimension values of various sleep stages were compared using a
statistical package (SYSTAT: SYSTAT Inc., Evanston, IL, U.S.A., 1988) on an IBM
PC-AT. The mean and standard error of mean was calculated and comparisons between
the stages were made using the one-way analysis of variance (ANOVA).

N.

458

et al.

PRADHAN

6. RESULTS
Running attractor dimension curves with varying lengths of data windows (512, 1024,
2048, 4096, 8192, 16,384 and 20,480 points) were obtained (Fig. 1 a-g) while the data
window shifted by a fixed length (64, 128, 256, 512 and 1024 points) along the whole of
the EEG record. The attractor dimension measurements with different lengths of data
windows
produced different values for the same data. The running attractor dimension
curves with small data windows
were grossly different from those with large data
windows even though the information content of the actual pattern lay embedded within
these (Fig. la-g) and was obtained from the same sleep EEG record of one subject. The
attractor dimension values ranged from 1.O to 19.98 for a data window of 512 points and
2.08 to 8.44 for a data window of 20,480 points. For a window length of 4096 points,
attractor values were within 1.84 to 11.94. Thus there is no meaning in comparing
attractor values, unless the window size is kept constant. Therefore, the number of data
points or the window length of the data may be considered as one of the important
factors that accounts for discrepancies in the values of attractor dimension reported by
different researchers. The running attractor dimension curves for the entire sleep EEG
record show constancy in the pattern of sleep behavior. The transitions in sleep processes
are encountered as the sleep progresseswith time. The values of the attractor dimension
were significantly lower in slow wave sleep as compared to stage 1 or stage 2 sleep. The
attractor dimension values for REM sleep were significantly higher as compared to the
slow wave sleep and comparable to the awake stage (Table 2). The F-Ratio (F
(5,24) =801.588, p<O.OOO) implies a significant difference in the values of attractor
dimension for different sleep states. The phase-spaceplots show discerning patterns for
alpha and beta activities (in a wakeful state) and that of delta activity (in stage 4 sleep)
(Fig. 2 a-c). The phase-space plots of alpha and delta activity are strongly indicative of
limit cycle behavior of low dimensional attractors. This may reflect synchronization of
activities in neuronal ensembles. In contrast the phase-spaceplot of beta activity is more
Shift

64

128

Fig. 1. Running
attractor
dimension
lengths and shifts. The data length or
(16 s) (d) 4096 (32 s) (e) 8192 (64 s) (f)
are given by 64,

256

512

1024

for a single night sleep record of 8 h with different

window
the window sizes are (a) 5 12 (4 s) (b) 1024 (8 s) (c) 2048
16,384 (128 s) and (g) 20,480 (160 s) data points. The shifts
128, 256, 512 and 1024 data points.

Patterns

of attractor

dimensions

Tabte 2. Attractor
sion
of
different
stages
(Mean
N=5)
Awake
Stage
Stage
Stage
Stage
REM

of sleep EEG

459

dimensleep
f SEM,

8.70 (0.14)@
7.26 (0.21)@
6.88 (0.32)@
5.36 (0.22)@
4.45 (0.12)@
9.20(0.16)@

1
2
3
4

SEM-Standard
sample

Error
Mean,

of
Cp

(p<0.ooo).

suggestive of high dimension chaotic behavior which appears like random activity. The
dimension values are higher in wakefulness and light sleep. It also increases to the level
of wakefulness during REM. The hypnogram scored by the visual analysis of the sleep
record is matched closely by the changes in the running attractor dimension (Fig. 3).
Independently,
the running attractor dimension curve may be seen as an objective
measure of the transitional states in sleep.
7. DISCUSSION
The analysis of EEG in the past several decades has been attempted by the
phenomenological
approach in which the EEG is seen to be a band-limited
signal
produced by some black-box with unknown or white Gaussian noise input [17]. In this
paper, the more recent model-based approach, incorporating concepts developed in the
area of nonlinear dynamics and chaos theory have been used. The model-based approach
to EEG interpretation
has the advantage that computer analysis will produce information not easily derived from visual inspection of the EEG traces. Therefore, this
method may provide information which was hitherto not extractable from EEG. The
attractor dimension curves presented in this study may be a potential means of
understanding the transitional process of the chaotic dynamics involving large scale
neuronal behavior of the brain during sleep. We have presented a hypnogram and the
attractor dimension time record of the sleep EEG. The transitions in the sleep behavior
can be clearly discerned in the attractor dimension record which corresponds to the
changes seen in the hypnogram. The attractor dimensions with different shifts of 64, 128,
256,512 and 1024 points along the data file with a fixed window length of 4096 points did
not affect the pattern of the attractor curves. Moving the data window by small steps
resulted in a greater number of attractor dimension values, and an increase in the data
points of the shift resulted in fewer attractor dimension values without any change in the
shape of the attractor curve. The attractor dimension analysis for all the different
window lengths with different shifts showed consistency in the pattern of the attractor
dimension curves. The complexity and transitions of sleep behavior are maintained in all
the running attractor dimension curves of the sleep EEG data recorded for the five
subjects in this study. It may be mentioned that a sleep EEG record may contain 3.6
mega samples and is about 32 megabytes of floating voltage values. The analysis of such
(a)

Alpha

activity

(b)

Fig. 2. The phase space plots of different

Beta

activity

EEG activities:
(c) delta activity.

(c)

(a) alpha activity.

Delta

activity

(b) beta activity.

and

et al.

N. PRADHAN

460

8
REM

Stage4

Hypnogram
I

Stage 3
Stage 2

Stage 1

Awake
Movement

Not

scored

4
1

12

Time

in hours

I
I

I
8

,
1

Running
I

attractor
I

dimension
I

10
8
s

6
4
2
c
0

Fig. 3. Hypnogram

and running

attractor

I
5

Time

in hours

dimension

for a typical

I
9

sleep record

voluminous
data for understanding
the patterns of brain activity poses considerable
problems. A scorer has to visually score the sleep data and at times it may be subjective
[ 111. The running attractor dimension method has been applied to sleep EEG in this data
set of five nights of sleep data. This method may also find possible applications in other
EEG monitoring situations such as anesthesia, coma, epilepsy and other neurological
emergencies.
The chaotic model of EEG generation, i.e. the notion that simple, nonlinear systems
can produce complex and almost random looking output, is very appealing [ 181. The fact
that the EEG appears unpredictable,
yet is bounded to a limited frequency
and
amplitude range with a few basic rhythms and waveforms points to chaotic aspect of the
brains electrical activity [19]. There are a number of transitions
from one stage of
activity to another. The degree of chaoticity varies in different stages. The present study
of the analysis of sleep EEG has been made here keeping in mind the nonlinear
deterministic
nature of EEG [20].
The attractor dimension has been used to study different sleep stages. The estimated
attractor dimension of slow wave sleep of stage 2 (D2 = 5.03) and stage 4 (D2 = 4.0-4.4)
was first reported by Babloyantz et al. demonstrating
the presence of a low dimensional
chaos in EEG [l]. It has been followed by a number of reports of attractor values in
various stages of sleep in human beings and other experimental animals [21]. The slow
wave sleep (D2 = 4.25) is well differentiated
from the REM sleep (D2 = 6). The sleep
results are the most stable results and are reproducible whereas there is a wide variation
in the reported waking state D2 values (2.4-11.0). There have been no attempts to see
whether the D2 patterns of the entire sleep data have any similarity to a hypnogram.
Even though a certain amount of training and subjectivity is encountered in evaluating
the sleep by sleep staging and scoring, it is probably the only method known in sleep

Patterns

of attractor

dimensions

461

of sleep EEG

physiology. In this paper we have studied the running attractor dimension values of sleep
records. We have presented the attractor dimension values in different stages of sleep
(Table 2) and the pattern of the changes in the attractor dimension has clearly delineated
the transitional states in sleep. During slow wave sleep, there is a loss of complexity in
large neuronal assemblies which is reflected in a low attractor dimension value (D2 =
4.2-4.8 for stage 4 NREM) implying a transitional state with loss of degrees of freedom.
It may be ascribed to a loss of positive feedback processes in the brainstem reticular
structures. It is hoped that nonlinear dimensional and trajectory analysis may become
another tool for discriminating
various normal and pathological states as the spectral
methods. The nonlinear dynamics, being a model driven approach, give a more direct
way of causal links between psychological processes and the neuronal substrate than does
the simple representation of EEG in the frequency domain [22].
8. SUMMARY
Chaotic dynamical analysis is a fundamentally
different approach to the analysis of
EEG. Deterministic
mathematical models of neuronai systems can give rise to complex
chaotic dynamics in the absence of stochastic fluctuations in the variables of brain
potentials. Chaotic dynamics are expected in nonlinear feedback systems possessing time
delays such as those that are expected to occur in recurrent inhibition and from the
periodic forcing of neural oscillators. The implications of chaotic dynamics and mathematical modeling of EEG generation in transitional states may throw new light on our
understanding of brain and behavioral states. Sleep is a naturally occurring behavioral
state that has inherent transitions. It is one of the most stable of animal behaviors. The
phylogenetic evolution of complexity of the transitional states of sleep parallels the
emergence of complex networks in brain development. Therefore, the complexity of the
dynamics of brain activity in sleep has been the subject of investigation in this paper. We
have presented the extraction of features of sleep behavior using the concept of an
attractor dimension. Evaluation of the nonlinear parameter through running attractor
dimension reveals a pattern which may be viewed as an objective measure of brains
transitional states in sleep behavior. The pattern matches to conventional visual scoring
- the hypnogram.
Our interpretations
may help in the analysis and modeling of
neuronal systems in the future. These attractor dimension values may have a physiological meaning with reference to neuronal activities. The methodology is also of importance
in analyzing other oscillatory and transitional states of brain activity seen in epilepsy,
task loaded attentional states, cognitive task performance and in various states of
consciousness. In short, this paper presents the physical and dynamical aspects of the
brains electrical activity in sleep from the new perspective of nonlinear dynamics. The
importance of the emerging trends of nonlinear science to neurobiology
has been
highlighted with reference to the concept of the attractor dimension.
Acknowledgemenr-The
09/48/92).
Government

work has been supported

of India.

by a grant

from

Department

of Biotechnology

(BT/R&D/

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About the Author-N.

PRADHAN obtained
his M.D. degree in Psychological
Medicine
from the
National
Institute
of Mental Health and Neurosciences
(NIMHANS),
Bangalore,
India in 1977.
He continued
in the same Institute
as resident doctor and became a faculty member in 1979. He
held positions
as Lecturer,
Assistant
Professor
and Associate
Professor in Psychiatry.
Currently
he is an Additional
Professor
and heads the Department
of Psychopharmacology.
His research
interest is in biological
psychiatry.
Currently
he is involved
in the research in applications
of
nonlinear
dynamics
and theory of chaos to neurodynamics
and cognitive
psychology.
He is the
A nonlinear
dynamical
study of transitional
principal
investigator
for the research
project
processes of brain activity using sleep data, which has been awarded to him by the Department
of Biotechnology,
Government
of India. The present work is an outcome of the project.

About the Author-P.

K. SADASIVAN obtained
his B.Tech and M.Tech
from the University
of
Calicut,
Kerala,
India in 1986 and 1989 respectively.
He received
his Ph.D degree from the
Department
of Electrical
Communication
Engineering,
Indian Institute
of Science, Bangalore,
India in 1995. Currently,
he is working
as a Research
Associate
in the project,
A nonlinear
dynamical
study of transitional
processes of brain activity using sleep data at NIMHANS.
His
research
interests
are in biomedical
signal processing,
nonlinear
dynamics
and chaos, neural
networks,
etc.

About the Author-SOMNATH

CHATTERJI obtained
his M.D. degree in Psychological
Medicine
from the National
Institute
of Mental Health and Neurosciences
(NIMHANS),
Bangalore,
India
in 1982. He continued
in the Department
of Psychiatry
as an Assistant
Professor
and as an
Associate
Professor.
Currently,
he is an Additional
Professor
in the same Department.
His
research interest is in biological
psychiatry.
He has been collaborating
with Dr N. Pradhan
in
various research projects.

About
the Author-D.
NARAYANA
Durr
obtained
his B.E. degree
from the Bangalore
University
and M.E and Ph.D from the Indian Institute
of Science, Bangalore,
India. He is
presently
working
in the same institute
in the Department
of Electrical
Communication
Engineering
as an Associate
Professor.
He had earlier worked
in the areas of acoustics and
speech signal processing.
At present,
he is working
in the area of applications
of digital signal
processing to the analysis of biomedical
signals; in particular,
brain signals. He is the principal
coinvestigator
for the project
A nonlinear
dynamical
study of transitional
processes of brain
activity using sleep data with Dr N. Pradhan.