ORIGINAL ARTICLE

Covariation of EEG Synchronization and Emotional State as

Modied by Anxiolytics
Miroslaw Wyczesany,* Szczepan J. Grzybowski,* Robert J. Barry,
Jan Kaiser,* Anton M. L. Coenen, and Anna Potoczekx

Summary: The relationships between subjective estimation of emotional

state and synchronization patterns in cortical emotional systems were
investigated. The emotional state varied between groups using diazepam,
buspirone, and placebo. The University of Wales Institute of Science and
Technology Mood Adjective Checklist was used for the assessment of
emotional state in the drug condition, yielding three estimates of emotional
state: Energetic Arousal, Tension Arousal, and Hedonic Tone. These
measures were correlated with the Synchronization Likelihood index of the
resting EEG. Increased affective valence and arousal were related to an
increased level of synchronization between frontal and right temporoparietal
emotional areas. Two identied centers of synchronization, localized in the
temporal and centroparietal regions, appeared to be functionally distinct.
Stable relationships between subjective emotional state measures and cortical
EEG synchronization patterns were conrmed, especially for the valence and
energetic arousal estimation. A higher synchronization is associated with
increased emotional valence and arousal, and this can thus be seen as a neural
correlate of emotional experiences.
Key Words: EEG synchronization, Emotional state, Mood, Activation, Buspirone, Diazepam.
(J Clin Neurophysiol 2011;28: 289e296)

he present study addresses the relationship between subjective

qualities of the individuals emotional state and cortical activity
as expressed in the EEG. Subjective emotional state is assessed by
the University of Wales Institute of Science and Technology Mood
Adjective Checklist (UMACL) (Matthews et al., 1990). These are
considered to reect both the energetic/arousal and the valence
dimensions of subjective emotional state. Note that the energetic
arousal (EA) and the tension arousal (TA) scales, while primarily
loading on energy/arousal, also include some valence load, positive
and negative, respectively.
The general assumption underlying this study is that the
experiential aspect of the affective state is a function of brain systems
related to emotions. Thus, changes in subjective emotional experience can be associated with specic changes in EEG activity. These
changes are presumably best observable over those cortical areas

From the *Psychophysiology Laboratory, Institute of Psychology, Jagiellonian University, Krakow, Poland; Brain & Behaviour Research Institute, School of
Psychology, University of Wollongong, Wollongong, Australia; Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen,
Nijmegen, The Netherlands; and Department of Psychiatry, Jagiellonian University School of Medicine, Krakow, Poland.
Supported by the Polish Ministry of Science and Higher Education funds reserved
for scientic research (2009).
Address correspondence and reprint requests to Miroslaw Wyczesany, PhD,
Ingardena 6, Krakow 30060, Poland; e-mail: miroslaw.wyczesany@uj.edu.pl.
Copyright 2011 by the American Clinical Neurophysiology Society

ISSN: 0736-0258/11/2803-0289

related to emotional processing. To modify the emotional state of

subjects, two psychoactive drugs were used, diazepam and buspirone, both primarily used as anxiolytics. Based on the above general
assumption, it is expected that both the subjective state of a person
and his or her brain activity will be affected by these drugs. In
previous studies, covariation between emotional state and the power
in the EEG was shown (Wyczesany et al., 2008, 2009). This relation,
which is rather stable across different experimental conditions, indicates the existence of cortical correlates of subjective states.
To date, most attempts to identify cortical regions whose
activities covary with the emotional state have concentrated on the
frontal area, although some authors claim that frontal and prefrontal
activities change with the ongoing emotional state (Demaree et al.,
2005). The valenceearousal concept of Heller (Heller, 2009; Heller
and Nitschke, 1998) distinguishes two cortical emotional systems:
the frontal area, related to valence or motivational value of the
affective state, and the right temporoparietal area, regulating behavioral, autonomic, and subjective aspects of nonspecic emotional
arousal. According to this model, the experiential aspects of emotions are reected in state-dependent changes of activation in these
areas. Previous data provide partial support showing that the areas
specied in the model of Heller are related to subjective estimation
of the emotional state in different conditions. However, the spectral
power methods used so far do not provide information about the
possible functional connections between these areas. To overcome
this disadvantage, a synchronization analysis is used in the present
experiment. Synchronization methods are used for determining the
level of interaction of two signals measured by separate electrodes.
As a general class of nonlinear methods, synchronization analysis is
sensitive to phase relationships, while amplitudes of the signals do
not affect the results. This is an advantage over traditional linear
analyses. Synchronization can be considered as an index of functional integration between distant cortical areas (Varela et al., 2001).
In the present experiment, the Synchronization Likelihood (SL) index (Stam and Van Dijk, 2002), which is based on the concept of
generalized synchronization (Rulkov et al., 1995), is used. The SL
has been used successfully to investigate interactions between
cortical areas engaged in cognitive processes, such as memory
(Molnr et al., 2009), visualespatial processing (Micheloyannis
et al., 2003), attention (Gootjes et al., 2006), and movements
(Calmels et al., 2006).
In using synchronization methods, it is assumed that phase
similarity between two signals is an index of functional dependence
of these signals. Based on this method, it can be determined whether
the synchronization level and the emotional state reported by
subjects show patterns of covariation. In the present article, we
focus on the two emotional systems described in the model of Heller,
so that frontal and right temporoparietal areas, related to these
systems, are considered in the analyses. The synchronizations

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289

M. Wyczesany et al.

Journal of Clinical Neurophysiology  Volume 28, Number 3, June 2011

between these systems are expected to reveal their mutual relationships. The role of the frontal cortex and its hemispheric specialization is well documented; many studies support the link of the left
frontal area with positive emotions, while the right frontal area is
linked with negative emotions. Conversely, some studies give
support for alternative opinions, in the sense that only the right
hemisphere is specialized in all types of emotions (for review, see
Demaree et al., 2005). Some suggestion of functional heterogeneity
within the right temporoparietal system can also be found in our
previous data (Wyczesany et al., 2010).
The present experiment used drugs, diazepam and buspirone,
to modify the emotional state of the participants. Both these drugs
have anxiolytic effects. Diazepam (DZP) belongs to the benzodiazepines, a wide class of minor tranquilizers, sharing sedative,
anxiolytic, muscle-relaxing, and amnesic properties. Benzodiazepines have a general depressing effect on the central nervous system
by modifying the g-aminobutyric acid-A receptor, which is then
more easily activated by g-aminobutyric acid, the main inhibitory
brain neurotransmitter (Mehta and Ticku, 1999; Olkkola and Ahonen,
2008). In the present study, diazepam was expected to decrease both
the energetic and the tension aspects of subjective arousal. The second drug, buspirone (BSP), is a newer anxiolytic drug, which is
a partial 5-HT1A receptor agonist. Compared with DZP, it does not
affect g-aminobutyric acid receptors and has anxioselective action,
lacking sedative, muscle relaxing motor impairment, and anticonvulsive effects (Taylor, 1998; Cohn et al., 1989). In this study, BSP was
administered to decrease the subjective level of tension but, in contrast to diazepam, was not expected to inuence the level of energy
or alertness.
The effect of benzodiazepines on the spontaneous EEG power
is well established. Results show a consistent increase in b- or high
b-power, along with a decrease in u- and low a-activity. The pattern
of EEG activity after benzodiazepines is similar to that associated
with an alert state, while behavioral and subjective measures show
decreased activity and more drowsiness (Coenen and Van Luijtelaar,
1991). However, in the low frequencies, an increase in d over the
right temporoparietal region has been observed, which could be
related to a deactivation of the posterior emotional system (Yamadera et al., 1997). Conversely, BSP causes a shift in EEG frequency
toward low frequencies, from a to u, which is more pronounced in
the posterior than in the anterior sites (McAllistereWilliams et al.,
2007). An enhancement of low-frequency activity (delta and theta)
with a decrease in either whole b or only high b has been reported.
There are some inconsistencies concerning a-power, which is decreased or unchanged, depending on the study (Bond et al., 1983;
Holland et al., 1994; Murasaki et al., 1989).
The aim of the present study was to determine the relationships between subjective qualities of emotional state and the way the
cortical emotional systems cooperate with each other. This cooperation is inferred from synchronization measures of the EEG
recorded from cortical emotional areas. The drugs introduced in the
study are intended to modify the subjective state. It is hypothesized
that changes in the subjective state will be reected in specic
changes of synchronization levels. These activities could then be
considered as neural correlates of experiential aspects of subjective
states. The distinction in emotional specialization of cortical areas
(valence vs. nonspecic arousal) suggests a measurement of the
emotional state on the following dimensions: energetic arousal,
tension arousal, and valence. It is expected that the increase in
the scores, which are strongly linked with emotional arousal
(i.e., tension and negative valence), will be associated with
a heightened level of synchronization between prefrontal and right
290

temporoparietal areas in the higher frequencies. Conversely, changes

in energetic arousal are thought to be associated with a deactivation
pattern, that is, with a low-frequency synchronization, at both short
(within an area) and long (between areas) ranges.

MATERIALS AND METHODS

Subjects
Fifty-two student volunteers (25 women and 27 men), aged 19
to 32 years (mean, 22.8 years), participated in the study. All of them
were healthy, not experiencing any chronic diseases, and medication
free, and this information was based on a questionnaire lled in
during the recruitment process.

Mood Assessment
The current emotional/activation state was assessed by the
computer version of the UMACL (Matthews et al., 1990) in the
Polish adaptation of Gory

nska (2001). It consists of 29 adjectives
describing subjective state rated on a 4-point scale. As a result, it
yields scores on three subscales: EA, TA, and hedonic tone (HT).

EEG Recording and Quantification

The resting EEG signal was measured and recorded with
a BioSemi ActiveTwo device (BioSemi B.V., NL), equipped with 32
preamplied active electrodes. The sampling frequency was 256 Hz
with 24-bit analog-to-digital converters. The extended 10-20 system
for electrode placement, with averaged reference, was used. The
following electrodes, localized over the prefrontal and temporoparietal emotional systems, were selected: frontal (Fp1, Fp2, AF3, AF4,
F7, and F8) and right temporoparietal (T8, C4, CP2, CP6, P4, and
P8). Electrode impedances were kept in a recommended range
during the whole recording. An off-line ocular artifact rejection
algorithm based on the method of Gratton et al. (1983) was then
applied to the EEG signal using data from additional electrooculogram electrodes. For synchronization analysis, 16-second EEG segments (4,096 samples) recorded just before the subjective assessment
were taken. Using digital lters (24 dB/octave slope), the whole
spectrum was divided into the following frequency bands: a-1 (8
to 10 Hz), a-2 (10 to 12 Hz), b-1 (13 to 15 Hz), b-2 (16 to 24 Hz),
and b-3 (25 to 30 Hz). The data were not normalized. Separately for
each frequency band, the SL index was calculated for all electrode
pairs, using the following parameters: lag 10 samples, embedding
vector dimension in phase space 10, v1 100, v2 400, p ref
0.05 (Stam and Van Dijk, 2002). Apart from the SL analysis, to
check the effects of drug inuence on EEG power, 60-second segments of the EEG signal were divided into 2-second overlapping
epochs for which power spectral density (mV2/Hz) was calculated
and averaged across the epochs and then aggregated into the
above-mentioned frequency windows. Because of skewness of
the data distribution, spectral values were log-transformed (Gasser
et al., 1982).

Procedure
The experimental procedure was approved by the Bioethical
Committee of the Jagiellonian University. Before the experiment, all
subjects were given basic information about the procedure and asked
to sign a written consent. Subjects were randomly assigned to one of
three groups in which different substances were administered orally
in accordance with a double-blind procedure: CTRdcontrol with
Copyright 2011 by the American Clinical Neurophysiology Society

Journal of Clinical Neurophysiology  Volume 28, Number 3, June 2011

placebo, DZPddiazepam (2 mg), and BSPdbuspirone (5 mg). The

number of subjects in the particular groups was 20, 16, and 16,
respectively. The experiment was performed in a soundproof and
electrically shielded cabin. All instructions were displayed on
a 1999 LCD screen. The procedure started with an idle 4-minute
period with a blank computer screen, which was intended for adaptation to the measurement conditions, followed by the computer
version of the UMACL. Then, the substance was administered, followed by a -hour period required for the drugs to take effect
(Besser and Duncan, 1967; McAllistereWilliams et al., 2007). During this time, subjects were allowed to read newspapers. After this
waiting period, 1 minute of spontaneous EEG with eyes open was
recorded, followed immediately by a second UMACL assessment.

Data Analysis
To check that after randomization, the balance between
genders in the experimental groups was maintained, a nonparametric
x2 test was used. Premedication subjective scores were checked
using a multivariate analysis of variance test to ensure no differences
between the groups. To determine whether the pharmacologic modication of mood was effective, the inuence of medication type on
differential subjective scores (before medication minus after medication) was analyzed using one-way multivariate analysis of variance
with planned contrasts: DZP versus CTR 1 BSP for the EA scale
(decreased activation effect), CTR versus DZP 1 BSP for the TA
scale (the effect of tension reduction), and CTR versus DZP 1 BSP
for the HT scale (the control group was checked against the medication groups). The effect of the drugs on EEG power was veried
using an analysis of variance with planned contrasts testing b-increase
in the DZP group versus the CTR group and a-decrease in the BSP
group versus the CTR group.
Before the main analyses, a baseline (predrug) EEG check
was conducted using a series of multivariate analysis of variance
tests to nd any group differences in baseline synchronization level.
None of the parameters (neither Wilks L nor Hotellings trace)
reached signicance level. This result conrmed that no pretreatment
group differences existed.
Within each of the EEG frequency bands, the associations
between scores on the subjective scales and synchronization
magnitudes between all combinations of electrodes were checked
using Pearsons r correlation coefcient. Positive correlation here
means an increased synchronization level related to higher subjective
scores, while negative correlation reects decreased synchronization
in the same conditions. Because of multiple hypothesis testing, additional correction of P levels was applied using the false discovery
rate procedure, which, apart from controlling experimentwise error
rate, can preserve relative high statistical power (Benjamini and
Hochberg, 1995). The P levels reported are corrected values.

EEG Synchronization and Emotional State

anxiolytics decreased the level of tension. No effect for the HT scale

was observed (F1,49 0.85; P 0.362; 2-tailed test). Changes in
subjective scores within the groups are shown in Table 1.
Spectral analysis of EEG power after diazepam revealed an
increase in b-3 log power in the DZP compared with the CTR group
in the regions of interest (mean log power mV2, 20.09 and 0.14,
respectively; t48 1.71; P 0.047; 1-tailed test). This group difference was not observed before drug administration. No signicant
spectral power effects were found for buspirone comparisons.

Synchronization and Subjective Scores

Control Group
In medication-free conditions, numerous negative correlations
within the frontal area were apparent between tension scores and SL
in the a-frequency range (8 to 12 Hz) (Fig. 1; Table 2). The lower
the EA estimation, the more pronounced was a-synchronization
within and between the hemispheres. Estimation of negative valence
(HT) was correlated with increased SL between T8 and many frontal
sites in most of the frequency range (8 to 30 Hz). However, the
higher the frequency, the fewer of these effects were preserved. Instead, associations with the centroparietal CP2 electrode became
apparent in the b-3 frequency range. In other words, more negative
emotional state was related to heightened level of frontoparietal
synchronizations. No correlations were found between EA estimation and SL level.

Diazepam Group
In the DZP group, positive correlations with EA between C4
and right frontal (Fp2) as well as posterior CP2 electrodes were
observed in the higher b-band. The HT scores were negatively correlated with the SL level between right posterior and frontal electrodes, and this effect was apparent for a-band as well as for the high
b-band; however, in lower frequencies, more signicant effects were
observed (Fig. 2; Table 3).

Buspirone Group
After BSP intake, EA estimation was found to be positively
correlated with SL levels between centroparietal and prefrontal areas
over the whole frequency range (8 to 30 Hz), and also with the left
frontal area in the lower frequencies (8 to 15 Hz). Some effects
within the centroparietal area were also visible. The C4 electrode
seemed to be the center of these effects and increased its functional
dependencies with both frontal and centroparietal sites in conditions

TABLE 1. Differences Between Pre- and Postmedication

Subjective Scores for the Three Scales (EA, TA, and HT) Within
Each Group
Scores

RESULTS
Effect of the Drugs

Scale

The x2 statistic showed no signicant disturbance of gender

distribution between experimental groups (x2(2) 0.121; P 0.94).
The multivariate analysis of variance test run on premedication subjective scores showed no between-group differences (Wilks L
0.93; F6,94 0.60; P 0.73). The effects of drug type using planned
comparisons were found signicant for the EA scale (F1,49 4.74;
P 0.034; 2-tailed test) and nearly signicant for the TA scale (F1,49
3.50; P 0.067; 2-tailed test). As expected, diazepam decreased
the level of energy compared with the remaining groups, and both

EA

Copyright 2011 by the American Clinical Neurophysiology Society

TA

HT

Group

Minimum

Maximum

CTR
DZP
BSP
CTR
DZP
BSP
CTR
DZP
BSP

211
210
213
24
25
27
23
23
21

10
4
8
9
3
7
8
7
10

Mean
1.11
23.44
21.00
0.50
21.44
21.22
3.83
2.50
3.56

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M. Wyczesany et al.

FIG. 1. Dashed lines link pairs of electrodes for which negative correlations between subjective scores and the SL were observed in
the CTR group.
of rising energy estimation. Such increase in synchronization related
to high EA scores was also seen in the case of short-distance effects
within the centroparietal area. For the highest frequencies (especially
b-3; 24 to 30 Hz), TA scores were positively correlated with synchronizations between the T8 electrode and some frontal and right
posterior electrodes. Also, in these highest frequencies, additional
effects with SL between left frontal and posterior area could be
observed. The HT scores were again negatively correlated with SL
level between right temporoparietal and frontal electrodes in bfrequencies; however, the effects in the right centroparietal region
were found for the higher b-band (24 to 30 Hz) (Fig. 3; Table 4).

DISCUSSION
Functional connectivity estimation measures can be confounded by common sources present in the EEG signal. It is an
effect of scalp volume connectivity as well as the inuence of
reference electrodes, which causes the potential from relatively focal
sources to be spread across the scalp, with magnitude decreasing
together with distance between the given electrodes (Barry et al.,
2005). Scalp volume conductance, as the rst source of possible
spurious effects, can especially increase detections of short-distance
synchronizations. Therefore, these effects should be interpreted with
caution. Conversely, long-distance functional connections, which
were our primary interest, are considered to be relatively weakly
sensitive to this problem (Handy, 2009). Additionally, because we
are inferring about cortical areas that are located relatively close to
the skull (and not deep, subcortical structures), the uncertainty introduced by volume conduction is further diminished. Thus, we
assume that our data are sufcient to draw conclusions about synchronizations between the regions of interest, with special caution
for within-area (short-distance) effects. However, in the case of longdistance synchrony, a problem of reference electrodes can still be
meaningful. This inuence was limited here by using an averaged
reference system. It should also be noted that these volume conduction and reference effects would be expected to affect all our subjects
similarly, so that any observed group differences cannot be attributed
to these sources.
292

The modication of the subjects emotional state by the use of

the drugs was successful, as reected in the subjective scores. The
UMACL used here was also previously found useful in registering
changes caused by medication (Holland et al., 1994).
Although the whole EEG frequency spectrum seems to be
affected by anxiolytic action, our primary interest was to investigate
changes in activation of emotion-related areas associated with
subjective states. For this purpose, a- and b-frequencies were chosen
as bands that allow relatively clear functional interpretation in terms

TABLE 2. Signicant r Coefcients Between Subjective Scales

and the SL in the CTR Group
Band
TA
a-1

a-2

HT
a-1

a-2

b-1
b-3

Electrodes

Fp2/AF4
Fp2/F7
Fp2/F8
F7/F8
Fp1/F7
Fp1/F8
Fp2/AF4
Fp2/F7
F7/F8

20.59*
20.52
20.48
20.59*
20.50
20.49
20.53
20.54*
20.51

Fp1/T8
AF3/T8
F7/T8
Fp1/T8
AF3/T8
F7/T8
Fp1/T8
F7/T8
AF3/CP2
F7/T8

20.62
20.59
20.68
20.59
20.59
20.69
20.58
20.69
20.63
20.70

P # 0.05. *P # 0.01; all P levels are adjusted by the False Discovery Rate
procedure.

Copyright 2011 by the American Clinical Neurophysiology Society

Journal of Clinical Neurophysiology  Volume 28, Number 3, June 2011

EEG Synchronization and Emotional State

FIG. 2. The lines connect the pairs of electrodes for which correlations between subjective scores and the SL were observed in the
DZP group. Solid lines represent positive correlations, while dashed lines represent negative correlations.

of cortical activity. Moreover, a- and b-activity results from our

previous experiments can provide a context for comparison and interpretation. In contrast, the presence of low-frequency rhythms can
be observed in conditions of both increased and decreased cortical
arousal (Klimesch, 1999). This lack of a straightforward relationship
for d, and especially u, makes the interpretation of experimental
effects more difcult and ambiguous.
The general hypothesis assuming stable and specic relationships between EEG characteristics and subjective scales received
partial, but rather good, support. Salient similarities between the
groups were observed for the HT and EA, which may suggest their
more universal character.
Negative correlation of the HT scores and the SL between
right temporoparietal centers (temporal T8 and posterior CP2 and
C4) were similar in all three conditions. Because of the bipolar
characteristics of the HT scale, this effect can be considered as
a positive correlation between cortical synchronization and the
negative affect, in the sense that the more negative is the estimation
of emotional state, the higher is the level of functional bindings
between parietal and temporal centers of synchronization. Moreover,
this effect is in accordance with the initial hypothesis, predicting
increased cortical associations in emotional conditions. However,
another conclusion, which is suggested by the data, is not fully
compliant with the theory. It is shown here that the temporoparietal
area characteristics differ for positive versus negative valence of
the emotional state, while theory of Heller claims that this area is
valence unspecic, that is, related to both positive and negative
emotional arousal. There are some similar discrepancies found in the
literature with regard to the posterior activation and its role in
emotional processing. Some experimental procedures show activation in both positive and negative conditions, as predicted by Heller
(Goldin et al., 2005; Lane et al., 1997; Lang et al., 2001), but other
studies show specicity of activation, depending on the valence
(Davidson et al., 1990; George et al., 1995). It is possible that the
negative emotional state, especially in laboratory conditions, could
be generally more arousing than the positive. As a consequence, it
seems easier to provoke in experimental procedures a higher
Copyright 2011 by the American Clinical Neurophysiology Society

negative emotional state, which is reected in sensitivity of the

temporoparietal system to negative stimulation. However, data supporting this post hoc explanation are lacking, suggesting that the
valence-unspecic nature of activation of the temporoparietal area
as a whole is questionable.
The analysis of the focus of synchronization delivers more
information concerning the posterior emotional system. Interestingly, two distinct centers can be distinguished on the basis of their
activation pattern in different conditions. The rst of these,
a temporal center focused in the T8 electrode, formed a center of
synchronizations with most frontal sites, showing increased synchronizations in conditions of negative valence estimation. Another
center could be observed over the right posterior sites (CP2 and C4).
Two distinct centers with different characteristics, according to

TABLE 3. Signicant r Coefcients Between Subjective Scales

and the SL in the DZP Group
Band
EA
b-2
b-3
HT
a-1

a-2

b-3

Electrodes

Fp2/C4
C4/CP2
Fp2/C4

0.73
0.52
0.51

Fp1/CP6
AF3/C4
AF3/CP2
F7/C4
AF3/C4
AF3/CP2
F7/C4
Fp2/C4
AF4/CP2

20.60
20.69
20.72
20.73
20.62
20.68
20.66
20.74
20.50

P # 0.05; *P # 0.01; all P levels are adjusted by the False Discovery Rate
procedure.

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Journal of Clinical Neurophysiology  Volume 28, Number 3, June 2011

FIG. 3. The lines connect the pairs of electrodes for which correlations between subjective scores and the SL were observed in the
BSP group. Solid lines represent positive correlations, while dashed lines represent negative correlations.

subjective dimensions and frequencies, suggest that the right parietal

and temporal cortex is not a single unitary emotional system. Instead,
it may be composed of different subsystems related to different
aspects of emotional processing. Moreover, the present data allow us
to generalize that, despite possible functional heterogeneity, the
whole right temporoparietal area seems to have important functional
connections with the frontal area, especially visible in the negative
emotional state. This observation can be considered as further
support for distinguishing the described cortical emotional areas.
Positive correlation of the EA scores with synchronization
between bilateral frontal and parietal areas (focused mostly in the C4
derivation), as well as local synchronizations within the parietal
cortex, was observed in the buspirone group. In the diazepam group,
only a small subset of these synchronizations was signicant;
however, the C4 electrode was still a center of synchronization.
The effects are very similar across the whole frequency range
examined. According to the theoretical background, the right
parietotemporal area can be related to experience of unspecic
energy. Our data would focus this area, especially in the right
parietal region. Conversely, it can be noted that temporal lobe SL
level was not related to EA estimation, which is another argument in
favor of a functional dissociation between right temporal and parietal
cortex. The EA dimension is weakly related to emotional arousal,
and this can be linked with the absence of temporal synchronizations. It can be hypothesized on the basis of the outcomes that the
posterior area is more related to unspecic emotional arousal, as
described by model of Heller, while the temporal area activity is
related to negative emotional arousal. However, the reason why
294

the drug groups differ according to the effect size, as well as why the
effect is absent in the control group, remains unclear.
Contrary to the hypothesis, the TA scores in the control group
were not correlated with the level of synchronization between the
frontal and posterior areas. Instead, changes were limited to the
frontal area, where synchronization decreased with increasing
tension. It is noticeable that this effect was visible only for the
low frequencies, particularly those covering the a-frequencies.
This activity has traditionally been considered as one of the basic
brain integrating rhythms, originating in thalamic pacemaker cells
(Skinner et al., 2000). Despite the newer data suggesting distinction
of several functional rhythms in this frequency range with possibly multiple generators (Basar et al., 1997), a-power is usually
considered as an index of cortical deactivation (Barry et al., 2009;
DiFrancesco et al., 2008) and is negatively correlated with fMRI
BOLD (Blood-Oxygen-Level Dependence) signal (Laufs et al.,
2006). In agreement with these ndings, the present observation of
a decreased a-synchronization in tension conditions may reect
a more active cortex. However, after medication, these low-frequency associations with tension are not observed, and the reason
behind this is not completely clear.
Quite different effects related to tension estimation were
found in the BSP group. Increase in synchrony between the temporal
T8 site and the frontal region was accompanied by some synchronizations within parietal areas at high frequencies. This effect,
although predicted by the theory, could be seen only in the BSP
group. It reects an enhancement of communication between the
temporal lobe and the frontal and right posterior areas. The right
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Journal of Clinical Neurophysiology  Volume 28, Number 3, June 2011

TABLE 4. Correlations Between Subjective Scales and the SL

in the BSP Group
Band
HT
b-2

b-3

TA
b-2
b-3

EA
a-1

a-2

b-1

b-2

Electrodes

Fp2/T8
AF4/T8
F8/T8
Fp1/P4
Fp1/P8
Fp2/T8
AF4/T8
F7/P8
F8/T8

20.65
20.64
20.73
20.50
20.49
20.72*
20.76*
20.66
20.77*

F7/T8
F8/T8
T8/CP2
T8/P4
AF3/C4
AF3/P8
AF4/T8
F7/P8
F8/T8

0.55
0.67
0.53
0.62
0.53
0.55
0.56
0.74*
0.69

C4/CP2
C4/CP6
C4/P4
C4/P8
Fp1/C4
Fp2/C4
AF3/C4
F7/C4
Fp2/C4
AF3/C4
C4/CP2
C4/CP6
C4/P4
C4/P8
CP6/P4
P4/P8
Fp1/C4
Fp2/C4
AF3/C4
F7/C4
C4/CP2
C4/CP6
C4/P8
CP6/P4
P4/P8
Fp1/C4
Fp2/C4
AF3/C4
F7/C4
AF3/C4
F7/C4
Fp2/C4
C4/CP2
C4/P4
C4/P8
CP2/P8
CP6/P4
P4/P8

0.60
0.75*
0.66*
0.76*
0.77*
0.67
0.80*
0.75*
0.67
0.80*
0.64*
0.74*
0.61
0.79*
0.84*
0.75*
0.81*
0.76*
0.82*
0.74*
0.61
0.64
0.71*
0.85*
0.74*
0.76
0.72
0.67
0.73
0.67
0.73
0.73
0.54
0.52
0.52
0.61*
0.80*
0.71*

Copyright 2011 by the American Clinical Neurophysiology Society

EEG Synchronization and Emotional State

TABLE 4. (Continued )
Band
b-3

Electrodes

C4/CP2
CP2/P8
CP6/P4
P4/P8
Fp2/C4
Fp2/CP6

0.52
0.57
0.70*
0.56
0.67
0.67

*P # 0.05; all P levels are adjusted by the False Discovery Rate procedure.

temporal area is known to be important in the control of emotional

and autonomic arousal, which is related to TA estimation (Kuniecki
et al., 2002). The action of BSP is mainly located in the limbic
structures (Taylor, 1998), as well as the raphe nuclei that activate
serotonin release related to positive mood (Flory et al., 2004). The
limbic system has bilateral projections to the medial part of the prefrontal cortex, which is related to conscious awareness of anxiety
state and its inhibiting modulation (Miller et al., 2005). Increased SL
level between the frontal and temporal lobe may be an effect of
enhanced inhibiting action of the frontal lobe on the emotional
circuits. This interpretation, however, is speculative and requires
further investigation.

CONCLUSIONS
The main hypothesis concerning a stable relationship between
subjective measures of emotional state and cortical EEG synchronization patterns received substantial support. The obtained results
can be interpreted as increased cooperation of both the prefrontal and
the posterior emotional areas in conditions of increased negative
valence as well as increase in both kinds of affective arousal:
energetic and tension. Especially the valence dimension (HT), but
also EA, showed similar results in different groups. In the case of the
former, data analysis revealed two centers of synchronization, which
are possibly functionally distinct but together form the postulated
right temporoparietal emotional area. It was speculated that the
parietal center is especially related to unspecic arousal, while
the temporal center is associated with negative emotional arousal.
The presented results suggest that combining subjective measures
with nonlinear synchronization methods can be a valuable tool for
inferring functional cortical dependences in emotional processes.

REFERENCES
Barry RJ, Clarke AR, Johnstone SJ, et al. Adjusting EEG coherence for interelectrode distance effects: an exploration in normal children. Int J Psychophysiol 2005;55:313e321.
Barry RJ, Clarke AR, Johnstone SJ, et al. Electroencephalogram theta/beta ratio
and arousal in attention-decit/hyperactivity disorder: evidence of independent processes. Biol Psychiatry 2009;66:398e401.
Basar E, Schrmann M, Basar-Eroglu C, Karakas S. Alpha oscillations in brain
functioning: an integrative theory. Int J Psychophysiol 1997;26:5e29.
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical
and powerful approach to multiple testing. J R Stat Soc B Met 1995;57:
289e300.
Besser GM, Duncan C. The time course of action of single doses of diazepam,
chlorpromazine and some barbiturates as measured by auditory utter fusion
and visual icker fusion thresholds in man. Br J Pharmacol Chemother
1967;30:341.

295

M. Wyczesany et al.

Journal of Clinical Neurophysiology  Volume 28, Number 3, June 2011

Bond A, Lader M, Shrotriya R. Comparative effects of a repeated dose regime of

diazepam and buspirone on subjective ratings, psychological tests and the
EEG. Eur J Clin Pharmacol 1983;24:463e467.
Calmels C, Holmes P, Jarry G, et al. Variability of EEG synchronization prior to
and during observation and execution of a sequential nger movement. Hum
Brain Mapp 2006;27:251e266.
Coenen AM, Van Luijtelaar EL. Pharmacological dissociation of EEG and behavior: a basic problem in sleep-wake classication. Sleep 1991;14:464.
Cohn JB, Rickels K, Steege JF. A pooled, double-blind comparison of the effects
of buspirone, diazepam and placebo in women with chronic anxiety. Curr
Med Res Opin 1989;11:304e320.
Davidson RJ, Ekman P, Saron CD, et al. Approach-withdrawal and cerebral
asymmetry: emotional expression and brain physiology. I. J Pers Soc Psychol
1990;58:330e341.
Demaree HA, Everhart DE, Youngstrom EA, Harrison DW. Brain lateralization of
emotional processing: historical roots and a future incorporating dominance. Behav Cogn Neurosci Rev 2005;4:3.
DiFrancesco MW, Holland SK, Szaarski JP. Simultaneous EEG/functional
magnetic resonance imaging at 4 tesla: correlates of brain activity to spontaneous alpha rhythm during relaxation. J Clin Neurophysiol 2008;25:
255e264.
Flory JD, Manuck SB, Matthews KA, Muldoon MF. Serotonergic function in the
central nervous system is associated with daily ratings of positive mood.
Psychiatry Res 2004;129:11e19.
Gasser T, Bcher P, Mcks J. Transformations towards the normal distribution of
broad band spectral parameters of the EEG. Electroencephalogr Clin Neurophysiol 1982;53:119e124.
George MS, Ketter TA, Parekh PI, et al. Brain activity during transient sadness
and happiness in healthy women. Am J Psychiatry 1995;152:341.
Goldin PR, Hutcherson CA, Ochsner KN, et al. The neural bases of amusement
and sadness: a comparison of block contrast and subject-specic emotion
intensity regression approaches. Neuroimage 2005;27:26e36.
Gootjes L, Bouma A, Van Strien JW, et al. Attention modulates hemispheric
differences in functional connectivity: evidence from MEG recordings. Neuroimage 2006;30:245e253.
Gory

nska E. Polska adaptacja Przymiotnikowej Skali Nastroju. In: Ciarkowska W,
Matczak A, (Eds). R_znice indywidualne: Wybrane badania inspirowane
Regulacyjna Teoria Temperamentu Profesora Jana Strelaua. Interdyscyplinarne Centrum Genetyki Zachowania, University of Warsaw; Warszawa,
Poland, 2001:155e164.
Gratton G, Coles MG, Donchin E. A new method for off-line removal of ocular
artifact. Electroencephalogr Clin Neurophysiol 1983;55:468e484.
Handy TC (Ed). Brain signal analysis: advances in neuroelectric and neuromagnetic methods. MIT Press; Cambridge, 2009.
Heller W. Neuropsychological mechanisms of individual differences in emotion,
personality, and arousal. Neuropsychology 2009;7:476e476.
Heller W, Nitschke JB. The puzzle of regional brain activity in depression and
anxiety: the importance of subtypes and comorbidity. Cogn Emotion
1998;12:421e427.
Holland RL, Wesnes K, Dietrich B. Single dose human pharmacology of buspirone. Eur J Clin Pharmacol 1994;46:461e468.
Klimesch W. EEG alpha and theta oscillations reect cognitive and memory
performance: a review and analysis. Brain Res Brain Res Rev 1999;29:
169e195.

296

Kuniecki M, Urbanik A, Sobiecka B, et al. Central control of heart rate changes

during visual affective processing as revealed by fMRI. Acta Neurobiol Exp
(Wars) 2002;63:39e48.
Lane RD, Reiman EM, Ahern GL, et al. Neuroanatomical correlates of happiness,
sadness, and disgust. Am J Psychiatry 1997;154:926e933.
Lang PJ, Bradley MM, Fitzsimmons JR, et al. Emotional arousal and activation of
the visual cortex: an fMRI analysis. Psychophysiology 2001;35:199e210.
Laufs H, Holt JL, Elfont R, et al. Where the BOLD signal goes when alpha EEG
leaves. Neuroimage 2006;31:1408e1418.
Matthews G, Jones DM, Chamberlain AG. Rening the measurement of mood: the
UWIST mood adjective checklist. Br J Psychol 1990;81:17e42.
McAllister-Williams RH, Massey AE, Fairchild G. Repeated cortisol administration attenuates the EEG response to buspirone in healthy volunteers: evidence
for desensitization of the 5-HT1 A autoreceptor. J Psychopharmacol
2007;21:826e832.
Mehta AK, Ticku MK. An update on GABAA receptors. Brain Res Brain Res Rev
1999;29:196e217.
Micheloyannis S, Vourkas M, Bizas M, et al. Changes in linear and EEG measures
as a function of task complexity: evidence for local and distant signal synchronization. Brain Topogr 2003;15:239e247.
Miller LA, Taber KH, Gabbard GO, Hurley RA. Neural underpinnings of fear and
its modulation: implications for anxiety disorders. J Neuropsychiatry Clin
Neurosci 2005;17:1e6.
Molnr M, Boha R, Czigler B, et al. The acute effect of low-dose alcohol on
working memory during mental arithmetic. II. Changes of nonlinear and
linear EEG-complexity in the theta band, heart rate and electrodermal activity.
Int J Psychophysiol 2009;73:138e142.
Murasaki M, Miura S, Ishigooka J, et al. Phase I study of a new antianxiety drug,
buspirone. Prog Neuropsychopharmacol Biol Psychiatry 1989;13:137e144.
Olkkola KT, Ahonen J. Midazolam and other benzodiazepines. Handb Exp Pharmacol 2008;182:335.
Rulkov NF, Sushchik MM, Tsimring LS, Abarbanel HD. Generalized synchronization of chaos in directionally coupled chaotic systems. Phys Rev E Stat
Phys Plasmas Fluids Relat Interdiscip Topics 1995;51:980e994.
Skinner JE, Molnar M, Kowalik ZJ. The role of the thalamic reticular neurons in
alpha- and gamma-oscillations in neocortex: a mechanism for selective perception and stimulus binding. Acta Neurobiol Exp (Wars) 2000;60:123e142.
Stam CJ, Van Dijk BW. Synchronization likelihood: an unbiased measure of
generalized synchronization in multivariate data sets. Phys Nonlinear
Phenom 2002;163:236e251.
Taylor D. Buspirone, a new approach to the treatment of anxiety. FASEB J
1988;2:2445e2452.
Varela F, Lachaux JP, Rodriguez E, Martinerie J. The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2001;2:229e239.
Wyczesany M, Kaiser J, Coenen A. Subjective mood estimation co-varies with spectral power EEG characteristics. Acta Neurobiol Exp (Wars) 2008;68:180e192.
Wyczesany M, Kaiser J, Barry RJ. Cortical lateralization patterns related to selfestimation of emotional state. Acta Neurobiol Exp (Wars) 2009;69:526e536.
Wyczesany M, Kaiser J, Coenen A. Associations between self-report of emotional
state and the EEG patterns in affective disorders patients. J Psychophysiol
2010;24:33e40.
Yamadera H, Kato M, Tsukahara Y, et al. Zopiclone versus diazepam effects
on EEG power maps in healthy volunteers. Acta Neurobiol Exp (Wars)
1997;57:151e155.

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