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Clinical Neurophysiology xxx (2013) xxxxxx

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Clinical Neurophysiology
journal homepage: www.elsevier.com/locate/clinph

Correlation of risk-taking propensity with cross-frequency


phaseamplitude coupling in the resting EEG
Jaewon Lee a,b,c, Jaeseung Jeong a,
a

Department of Bio and Brain Engineering, Korea Advanced Institute of Science and Technology (KAIST), Daejeon 305-701, South Korea
Neuropsychiatry Research Laboratory, Department of Psychiatry, Gongju National Hospital, Chungcheongnam-do 314-200, South Korea
c
Addiction Brain Center, Eulji Addiction Institute, Gangnam Eulji Hospital, Seoul 135-010, South Korea
b

a r t i c l e

i n f o

Article history:
Accepted 7 May 2013
Available online xxxx
Keywords:
Cross-frequency phaseamplitude coupling
(CFPAC)
Risk-taking propensity (RTP)
Barrett impulsiveness scale (BIS)
Domain-specic risk-taking (DOSPERT)
scale

h i g h l i g h t s
 The cross-frequency phaseamplitude coupling may be successfully adapted to the scalp resting EEG.
 There are signicant correlations between cross-frequency phaseamplitude couplings and the mea-

sures of risk-taking propensity.


 It is suggested that the cross-frequency phaseamplitude coupling could be a promising indicator for

diagnosing the tendency to take risks.

a b s t r a c t
Objective: Recent evidence has suggested that the weak inhibitory inuence of the prefrontal cortex on
the subcortical structures may be responsible for risk-taking behaviour. The aim was to determine the
possibility that this weakness in top-down control is reected in changes in the cross-frequency
phaseamplitude coupling (CFPAC) in the electroencephalography (EEG).
Methods: Nineteen-channel EEGs were recorded from 50 healthy volunteers with their eyes closed before
risk-taking propensity was assessed by behavioural measures, the domain-specic risk-taking (DOSPERT)
scale and the Barrett impulsiveness scale (BIS). Correlation analyses between the CFPACs and the behavioural measures were performed.
Results: The CFPACs were negatively correlated with the risk-taking DOSPERT and BIS scores in frontal
(Fp2) and centroparietal (C3, C4 and P4) regions. By contrast, the CFPACs were positively correlated with
the risk-taking DOSPERT and BIS scores in the right hemisphere (T8 and P8).
Conclusions: We suggest that frequent risk-taking behaviour is closely associated with the reduced interference of the cortical control network on the reward-oriented system. The CFPAC, which reects the
degree of interactions among functional systems, provides information about an individuals risk-taking
propensity.
Signicance: The CFPAC may be a useful neurophysiological indicator of an individuals tendency towards
risk-taking behaviours, which thus potentially contributes to evaluating the severity of the psychiatric
diseases exhibiting abnormal risk-taking behaviours.
Published by Elsevier Ltd. on behalf of International Federation of Clinical Neurophysiology.

1. Introduction
Risk-taking propensity (RTP) is generally dened as an individuals tendency to perceive or interpret potentially risky situations
and to take endurable risks but avoid excessive risks (Byrnes,
1998; Garon and Moore, 2004; Halpern-Felsher and Cauffman,
2001; Mann et al., 1989; Steinberg and Scott, 2003). A wide variety
Corresponding author. Address: Brain Dynamics Laboratory, Department of Bio
and Brain Engineering, KAIST, 373-1 Kuseong-dong, Yuseong-gu, Daejeon, South
Korea. Tel.: +82 42 350 4319; fax: +82 42 350 4310.
E-mail address: jsjeong@kaist.ac.kr (J. Jeong).

of behaviours qualify as risky. Among these are behaviours that involve highly undesirable real-world risks, such as alcohol abuse,
tobacco use, unsafe sexual activity, dangerous driving, interpersonal aggression and even more serious delinquent and criminal
behaviours; these behaviours have been the major focus of
researchers and clinicians interested in the neurobiology of RTP
(Boyer, 2006).
To date, the studies on impulsive risky behaviour have focussed
on the neural correlates of either the cognitive control system
(Eshel et al., 2007; Van Leijenhorst et al., 2006) or the reward-processing system (Ernst et al., 2005; Galvan et al., 2006; Polezzi et al.,
2010; Van Leijenhorst et al., 2010). Both systems are closely related

1388-2457/$36.00 Published by Elsevier Ltd. on behalf of International Federation of Clinical Neurophysiology.


http://dx.doi.org/10.1016/j.clinph.2013.05.007

Please cite this article in press as: Lee J, Jeong J. Correlation of risk-taking propensity with cross-frequency phaseamplitude coupling in the resting EEG.
Clin Neurophysiol (2013), http://dx.doi.org/10.1016/j.clinph.2013.05.007

J. Lee, J. Jeong / Clinical Neurophysiology xxx (2013) xxxxxx

to RTP, but recently, the interaction between the two systems has
received more attention. For instance, it has been postulated that
high RTP in adolescents originates from differences in the development patterns of reward- and control-related circuitry that might
lead to an imbalance in the adolescent brain (Casey et al., 2008;
Ernst et al., 2006; Galvan et al., 2006; Steinberg et al., 2008). Recently, RTP has been investigated in the context of interactions between reward-related and control-related brain regions (Van
Leijenhorst et al., 2010).
Reward processing is associated with activation of the ventral
medial prefrontal cortex, orbitofrontal cortex, ventral striatum
and amygdala (Bjork et al., 2004; Cohen et al., 2009; Ernst et al.,
2005; Eshel et al., 2007; Galvan et al., 2006; May et al., 2004).
Reward processing is essential for motivation, volition and goal-directed behaviour of humans. However, the dysfunctional processing of reward is also frequently associated with behavioural
problems such as addiction, impulsivity and risk-taking (Paulus,
2007; Steinberg, 2007). It is supposed that reward processing is
mediated by more complex mechanisms associated with the functional interaction between various reward-related brain regions
(Camara et al., 2008). For instance, the reward system recognises
some stimuli as liking and produces pleasure and positive affect.
On the contrary, in other cases, the same stimuli are accepted as
wanting and produce incentive motivation. It is quite differently
processed in the reward-related brain regions, and it gives us an insight into understanding the aetiology of addiction or eating disorders (Berridge and Robinson, 1995; Berridge et al., 2009; Camerer,
2006; Davis et al., 2009; Finlayson et al., 2007; Litman, 2005; Robinson et al., 2005).
On the other hand, it has been suggested that cognitive control
processing is associated with the dorsal anterior cingulate cortex,
the lateral (dorsal and ventral) prefrontal cortex (Eshel et al.,
2007; Van Leijenhorst et al., 2006), the anterior insular cortex (Wager and Barrett, 2004), the inferior frontal junction (Brass et al.,
2005) and the posterior parietal cortex (Andersen et al., 1997; Constantinidis and Steinmetz, 1996). Some of these regions are parts of
the frontostriatal system known as the corticosubcortical circuit
(CSC). It is generally accepted that the sub-regions of this circuit
do not function independently but rather work together towards
specic functions such as executive control processing (Gazzaniga
et al., 1998). Undoubtedly, risk-taking behaviour is based in the
CSC, where interaction between the reward-related and control-related brain regions begins. This idea is supported by various studies that have reported increased risk-taking behaviours in subjects
with prefrontal cortex disruptions caused by, for example, traumatic brain injury (Bechara et al., 1996), transcranial direct current
stimulation (Fecteau et al., 2007), repetitive transcranial magnetic
stimulation (Knoch et al., 2006) and the interference of alcohol
(Lane et al., 2004).
Since Robinson (1999, 2000) originally suggested that different
EEG rhythms might reect different corticosubcortical projections, several studies have focussed on the relationship between
the EEG spectra and the CSC (Honk and Schutter, 2005; Knyazev
and Slobodskaya, 2003; Schutter and Honk, 2004; Schutter et al.,
2006). It has been suggested that the crosstalk in the CSC manifests
in the coupling of slow and fast wave activities and that this is
likely the result of descending inhibition (DI), by which the cortical
system executes inhibitory control over the subcortical brain structure (Jackson, 1958). Thus, cognitive inhibitory control in the cortical system possibly alters the degree of cross-frequency
coupling between slow and fast oscillations. Therefore, we hypothesised that an individuals RTP would be revealed by differences in
the degree of cross-frequency coupling observed in resting scalp
EEG.
The cross-frequency coupling between slow and fast oscillations can allow for even more complex corticosubcortical

interactions (Buzsaki and Draguhn, 2004; Steriade, 2001) and has


been examined by EEG (Canolty et al., 2006; Jensen and Colgin,
2007; Palva et al., 2005; Schack et al., 2002; Shils et al., 1996).
Especially, recent studies on the human neocortex have demonstrated that the power of fast oscillations (30150 Hz) is modulated by the phase of slow oscillations (18 Hz) (Canolty et al.,
2006; Jensen and Colgin, 2007). From a theoretical point of view,
there are several ways in which the cross-frequency interactions
might occur, such as amplitudeamplitude, phaseamplitude and
phasephase interactions. So far, the cross-frequency amplitude
amplitude coupling has been investigated by many researchers
interested in the corticosubcortical interaction related to the hormone level (Miskovic and Schmidt, 2009; Schutter and van Honk,
2005; van Peer et al., 2008), anxiety (Knyazev, 2011; Knyazev
et al., 2005, 2006; Miskovic et al., 2010; Miskovic et al., 2011a,b),
emotion (Schutter and Knyazev, 2012) and obsessivecompulsive
disorder (Velikova et al., 2010). To our knowledge, there is a lack
of studies that investigate the corticosubcortical interaction using
the phaseamplitude interaction. Moreover, the cross-frequency
phaseamplitude coupling (CFPAC) reported by Canolty et al.
(2006) is of interest among clinical psychiatrists because of its potential as a neurophysiological measure of corticosubcortical
interactions (Jensen and Colgin, 2007).
The aim of the present study was to determine whether or not
the CFPAC in resting EEGs is correlated with self-reported measures of RTP. To this end, the Korean versions of the Domain-Specic Risk-Taking (DOSPERT) Scale (Hong et al., 2010) and the
Barrett impulsiveness scale (BIS) (Chung and Lee, 1997) were used
as behavioural measures of RTP. Studies that have investigated the
intra-individual stability of resting EEGs have demonstrated the
stability of resting EEG traces over a period of years (Kondacs
and Szabo, 1999). Moreover, because RTPs are rather long-standing
behavioural tendencies and would also be the result of sustained
corticosubcortical interactions, we used resting EEG when the
subjects eyes were closed in order to capture individual dispositional differences in RTP.
2. Materials and methods
2.1. Subjects
A total of 50 healthy volunteers (21 females; aged
33.0 7.8 years; Edinburgh laterality quotient, 87.9 30.8) were
recruited using an online advertisement in Gongju, South Korea.
None of the participants were taking any medications and all had
completed at least 12 years of education (14.9 1.9 years). In addition, each participant signed an informed consent form before the
experiment. This study was approved by the Institutional Review
Board (IRB) of the Gongju National Hospital (Gongju, South Korea)
and was performed in accordance with the Declaration of Helsinki
(World Medical Association: Ethical Principles for Medical Research Involving Human Subjects, 1964).
2.2. Risk-taking and impulsivity scales
The DOSPERT Scale, a self-reported psychometric scale, allowed
us to assess the conventional risk attitudes (i.e., the reported level
of risk-taking) and the perceived risk attitudes (i.e., the willingness
to engage in a risky activity as a function of its perceived riskiness).
The scale comprises ve commonly encountered content domains:
ethical, nancial, health/safety, social and recreational (Blais and
Weber, 2006; Weber et al., 2002). The DOSPERT generates two
scores: one for the risk attitude, which is called the risk-taking
score, and the other for the perceived risk attitude, which is called
the risk-perception score. These scores provide integrative

Please cite this article in press as: Lee J, Jeong J. Correlation of risk-taking propensity with cross-frequency phaseamplitude coupling in the resting EEG.
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information about the ve domains described above. In general,


the greatest risk takers exhibit high risk-taking scores and low
risk-perception scores. We used the Korean version of the 30-item
version of the DOSPERT (Hong et al., 2010). In addition, the Korean
version of the BIS standardised by Chung and Lee (1997), a widely
used and well-validated self-report measure of RTP, was used. It includes 23 items that can be scored to yield three factors such as
attentional, motor and non-planning impulsiveness. High scores
indicate a greater tendency towards impulsive risk-taking in decision making and various social situations.
2.3. Experimental procedures
After the subjects arrived at the laboratory at Gongju National
Hospital, they were screened for neurological or psychiatric conditions. The use of alcohol was carefully screened for using a digital
breath alcohol concentration (BAC) calculator (Alcoscan AL9000,
Sentech, Seoul, South Korea) and self-report questionnaires. Those
subjects with 0% BAC and a history of consuming fewer than ve
alcoholic beverages per week were allowed to participate in the
experiment. First, each subject was seated in a comfortable chair
in a dimly lit room and instructed to relax and keep movements
to a minimum. The resting EEG was recorded over 3 min with
the subjects eyes closed. Next, the subjects lled out the DOSPERT
and BIS self-report questionnaires. The subjects were debriefed at
the end of the experiment.
2.4. EEG recording and pre-processing

band at the signicance level 0.05 were removed. Finally, the absolute powers were averaged over all of the time windows and frequency bands for further analysis.
2.6. CFPAC analysis
We employed the synchronisation index (SI) proposed by Cohen
(2008) to assess the cross-frequency interactions between the lowfrequency (18 Hz) phase and the power of the gamma (3080 Hz)
oscillations. Briey, the SI is a phase coherence measurement between the phase of the upper (gamma) power time series and
the phase of the lower time series (synchronisation index:
P
SI 1n nt0 ei ult  uut ; n, the number of time points; uut , the
phase of the upper frequency power time series at time point t;
and ult , the phase of the lower frequency time series at time point
t) (Cohen, 2008). To avoid distortions of the phase value during ltering, we used the two-way, least-squared nite impulse response
lter (eeglt.m) included in the EEGLAB toolbox (Delorme and
Makeig, 2004). In addition, 1000-ms time windows with an 800ms overlap and 3-Hz windowing for each of the ve gamma subfrequencies were used for the subjects. The gamma power time
series was extracted as the squared magnitude of ft, which is
the analytic signal obtained from the Hilbert transform (power
time series: pt realft2 imagft2 ). The phases of the two
time series were extracted from the Hilbert transform


(phase arctan imagft
). The SI value is a complex number, and
realft
its magnitude (SIm) reects the extent to which the phases are synchronised (0 = completely desynchronised; 1 = perfectly synchronised). The outliers were also removed in the same way as described
for the spectral analysis. Finally, the SIm values were averaged over
all of the time windows and each of the ve gamma sub-frequency
windows for further analyses. We investigated the two different
CFPACs: delta-phase gamma-power coupling (DGC) and the theta-phase gamma-power coupling (TGC).

The EEG recording was conducted from the scalp using a SynAmps2 direct current (DC) amplier and a 10/20 layout 64-channel
Quik-Cap electrode placement system (Neuroscan Inc., NC, USA).
The EEGs were recorded from 19 electrode sites (Fp1, Fp2, F7, F3,
Fz, F4, F8, T7, C3, Cz, C4, T8, P7, P3, Pz, P4, P8, O1 and O2) based
on a standard international 10/20 system at a sampling rate of
1000 Hz. We used the linked mastoid for reference and two additional bipolar electrodes to measure the horizontal and vertical
eye movements. The impedance of each electrode was kept below
10 kO throughout the EEG recording session.
We used Matlab 7.0.1 (MathWorks, Natick, MA, USA) and the
EEGLAB toolbox (Delorme and Makeig, 2004) to pre-process and
analyse the EEG recordings. First, the EEG data were downsampled
to 250 Hz. Next, the EEG data were detrended and mean-subtracted to remove the DC component. A 1-Hz high-pass lter and
a 60-Hz notch lter were applied to remove the eye and electricity
noise. Independent component analysis (ICA) was also performed
to eliminate eye-blink and muscle artefacts. For the analysis,
>2 min of artefact-free EEG data were selected from the 3-min
recording of each subject based on visual inspection by clinical
psychiatrists and EEG experts.

The Matlab 7.0.1 statistical toolbox was used for the statistical
analyses. All values of the RTP measures (the DOSPERT and BIS)
were expressed as the mean and the standard deviation (SD). Students t-tests were used to test for gender differences in the age,
education and the RTP measures (the DOSPERT and BIS). Statistical
signicance was dened as p < 0.05. We used a correlation analysis
to compare the linear relationship between the RTP measures and
the EEG data. We adjusted for gender, age and education using the
Pearsons partial correlation method. The partial correlation coefcients and the associated p-values were determined. To improve
clarity, the topographical plots of the partial correlation coefcients and p-values were used to represent the correlation results.

2.5. Power-spectrum analysis of the EEG

3. Results

Seven frequency bands were dened for further analyses: delta


(14 Hz), theta (48 Hz), slow alpha (810 Hz), fast alpha
(1013.5 Hz), beta (13.530 Hz), slow gamma (3058 Hz) and fast
gamma (6280 Hz). For the cross-frequency coupling analyses, the
slow gamma and fast gamma frequencies were divided into ve
sub-bands: 35-Hz gamma (3039 Hz), 45-Hz gamma (4049 Hz),
55-Hz gamma (5058 Hz), 65-Hz gamma (6269 Hz) and 75-Hz
gamma (7080 Hz). We investigated the power spectra of the
EEG data for each subject using the short-time Fourier transform
spectrogram.m function of the signal processing toolbox in Matlab. Time windows of 1000 ms with an 800-ms overlap and the
Hamming window were used for the spectral analysis. The outliers
that were far from the spectral value distribution of each frequency

To assess the characteristics of impulsive, risk-taking behaviours in the subjects, we measured the DOSPERT and BIS scores.
The demographic features and the ndings are presented in Table
1. The Cronbachs alphas for the DOSPERT and BIS are 0.7186 and
0.7827, respectively. To determine whether the risk-taking behaviours were gender-dependent or not, we compared the values of
the DOSPERT and BIS between the male and female subjects. The
statistical analyses of the gender differences in the DOSPERT and
BIS values revealed no signicant differences between the groups
except in the DOSPERT risk-taking scores. The risk-taking DOSPERT
scores were signicantly higher for the male subjects than the female subjects (t(48) = 2.01, p < 0.01). To assess the possible relationship with the absolute powers of resting EEGs, we estimated

2.7. Statistical analysis

Please cite this article in press as: Lee J, Jeong J. Correlation of risk-taking propensity with cross-frequency phaseamplitude coupling in the resting EEG.
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Table 1
The characteristics of the demographic data and the measures of risk-taking
propensity in the subjects.
Mean S.D.

Total
(n = 50)

Male
(n = 29)

Female
(n = 21)

Age (years)
Education (years)
Edinburgh laterality quotient
BIS score
The DOSPERT risk-perception
score
The DOSPERT risk-taking score

33.0 7.8
14.9 1.9
91.4 17.6
26.0 7.0
102.1 12.1

31.8 7.4
15.0 1.8
94.9 12.5
26.1 8.2
100.7 11.0

34.8 8.2
14.9 2.1
86.5 22.2
25.9 5.1
104.0 13.4

72.0 15.9

78.1 16.1*

63.7 11.3*

S.D., Standard deviation; BIS, Barrett impulsivity scale; DOSPERT, domain-specic


risk-taking scale.
*
p-Value < 0.05.

the partial correlations, corrected for gender, age and education,


between the DOSPERT and BIS values and the 12 power spectra
(seven frequency bands + ve gamma sub-bands) of the resting
EEGs from the subjects. The topographical representations of each

of the Pearsons partial correlation coefcients and the associated


p-value are presented in Fig. 1.
From the results of partial correlation analyses, we found that,
as a whole, the power spectra of EEGs were positively correlated
with BIS scores at central and occipital regions and with DOSPERT
risk-taking scores at parietal and occipital regions. However, in the
case of DOSPERT risk-perception scores, the negative correlations
dominated at central and occipital regions. The partial correlation
analyses indicated signicant positive partial correlations between
the Cz electrode and the BIS scores (45 Hz) and negative partial
correlations between the central (C4 and Fz) and parietooccipital
(P8) regions and the DOSPERT risk-perception scores. However, no
signicant partial correlations were observed between the DOSPERT risk-taking scores and the power spectra. The signicant statistical results are presented in Table 2.
To investigate whether RTP correlates with the CFPAC of resting
EEGs, we also examined the partial correlations corrected for gender, age and education between the DOSPERT and BIS values and
the two CFPACs (DGC and TGC) of the resting EEGs in the subjects.

Fig. 1. Topographical representations of the Pearsons partial correlations, corrected for gender, age, and education, between the absolute powers and the BIS and DOSPERT
scores. On the left is the topography of the Pearsons partial correlation coefcients, and on the right is the topography of the associated p-values. The scale for each
topography pair corresponds to the color bar in the two enlarged samples above. r, Pearsons partial correlation coefcient; p, p-value; DOSPERT, domain-specic risk-taking
scale; BIS, Barrett impulsiveness scale.

Please cite this article in press as: Lee J, Jeong J. Correlation of risk-taking propensity with cross-frequency phaseamplitude coupling in the resting EEG.
Clin Neurophysiol (2013), http://dx.doi.org/10.1016/j.clinph.2013.05.007

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Table 2
The electrodes show the signicant (p < 0.05) partial correlation (adjusted for gender,
age and education) between the power spectrum and the measures of risk-taking
propensity.
Risk-taking
measure

Electrode location
(type of power
spectra)

BIS score

Cz (45 Hz)

DOSPERT
risk-perception score

C4 (delta)
P8 (delta)
Fz (slow gamma)
C4 (fast gamma)
Fz (35 Hz)
Fz (45 Hz)
C4 (65 Hz)
C4 (75 Hz)

Table 3
The electrodes show the signicant (p < 0.05) partial correlation (adjusted for gender,
age and education) between the CFPACs and the measures of risk-taking propensity.
Risk-taking
measure

Electrode location (type of


CFPAC and gamma band)

Pearsons
partial
correlation
coefcient

p-Value

p-Value

0.319

0.027

BIS score

0.297
0.332
0.302
0.316
0.292
0.288
0.302
0.326

0.040
0.021
0.037
0.028
0.044
0.047
0.037
0.024

F8 (TGC 35 Hz)
T7 (TGC 35 Hz)
Fp2 (DGC 75 Hz)
F3 (DGC 75 Hz)
T8 (DGC 75 Hz)
P4 (DGC 75 Hz)
C4 (TGC 75 Hz)

0.340
0.312
0.391
0.312
0.298
0.461
0.387

0.0183
0.0310
0.0059*
0.0307
0.0394
0.0009*
0.0065*

DOSPERT riskperception
score

C4 (DGC 35 Hz)
F3 (TGC 45 Hz)
P8 (TGC 45 Hz)
P8 (TGC 55 Hz)
P4 (TGC 65 Hz)
F8 (TGC 75 Hz)

DOSPERT risktaking score

F7 (DGC 35 Hz)
C3 (DGC 45 Hz)
T8 (DGC 45 Hz)
P8 (DGC 45 Hz)
Fp1 (DGC 55 Hz)
O1 (DGC 55 Hz)
Pz (DGC 65 Hz)
T8 (DGC 75 Hz)

Pearsons partial
correlation
coefcient

BIS, Barrett impulsivity scale; DOSPERT, domain-specic risk-taking scale.

Fig. 2 presents the topographical representations of each of the


Pearsons partial correlation coefcients and the associated p-values between the measures of RTP and the CFPAC on resting EEGs.
We found that the BIS score was negatively correlated with DGC
and TGC. The signicant ndings were revealed mainly in DGC
(75 Hz) and TGC (35 and 75 Hz) in frontal (Fp2, F8 and F3), central
(C4) and temporoparietal (T7 and P4) regions. However, the positive partial correlation between the BIS score and DGC (75 Hz) was
found in the right temporal (T8) region. Regarding the DOSPERT
score, positive partial correlations were found in the frontal (F3
and F8) and centroparietal (C4, P4 and P8) regions between the
risk-perception score and CFPACs. In addition, negative partial correlations were observed in the frontal (Fp1 and F7), central (C3),
temporoparietal (T8, P8 and Pz) and occipital (O1) regions
between DGC and the risk-taking score. Further, the signicant positive partial correlations were found in the right temporal (T8 and
P8) regions between DGC (45 Hz) and the risk-taking score. The

0.304
0.298
0.312
0.294
0.346
0.294
0.289
0.376
0.315
0.355
0.297
0.263
0.307
0.346

0.0356
0.0396
0.0307
0.0422
0.0161
0.0428
0.0463
0.0084*
0.0289
0.0132
0.0403
0.0184
0.0340
0.0159

CFPAC, cross-frequency phase amplitude coupling; BIS, Barrett impulsivity scale;


DOSPERT, domain-specic risk-taking scale; TGC, thetagamma coupling; DGC,
deltagamma coupling.
*
p-Value <0.01.

signicant statistical results are presented in Table 3. The scatter


plots of the four signicant (p < 0.01) partial correlations are presented in Fig. 3.

Fig. 2. Topographical representations of the Pearsons partial correlations, corrected for gender, age, and education, between the cross-frequency couplings (CFPACs) and the
BIS and DOSPERT scores. On the left is the topography of the Pearsons partial correlation coefcients, and on the right is the topography of the associated p-values. The scale
of the topography pairs corresponds to the color bar enlarged in the two center examples. r, Pearsons partial correlation coefcient; p, p-value; DOSPERT, domain-specic
risk-taking scale; BIS, Barrett impulsiveness scale.

Please cite this article in press as: Lee J, Jeong J. Correlation of risk-taking propensity with cross-frequency phaseamplitude coupling in the resting EEG.
Clin Neurophysiol (2013), http://dx.doi.org/10.1016/j.clinph.2013.05.007

J. Lee, J. Jeong / Clinical Neurophysiology xxx (2013) xxxxxx

Fig. 3. Scatter plots of the Pearsons partial correlations corrected for gender, age, and education between the mean of the SIm values with the BIS and DOSPERT measures. (a)
The partial correlation of the SIm DGC values (45 Hz) and the risk-taking DOSPERT score at C3. (b) The partial correlation of the SIm DGC values (75 Hz) with the BIS scores at
Fp2. (c) The partial correlation of the SIm DGC values (75 Hz) with the BIS scores at P4. (d) The partial correlation of the SIm TGC values (75 Hz) with the BIS scores at C4. SIm,
magnitude of the synchronization index; r, Pearsons partial correlation coefcient; p, p-value; DOSPERT, domain-specic risk-taking scale; BIS, Barrett impulsiveness scale;
TGC, theta-phase gamma-amplitude coupling; DGC, delta-phase gamma-amplitude coupling.

4. Discussion
In the current study, we have demonstrated that high RTP assessed by the DOSPERT Scale and BIS is closely associated with
low degrees of CFPACs in the EEG in the frontal (Fp2) and centroparietal (C4, P4 and C3) regions. By contrast, the high degrees
of CFPACs in the right temporal and parietal lobe (T8 and P8) are
related to high risk-taking scores. Otherwise, comparing the methods for EEG analysis, the spectral analyses had a weakened power
to demonstrate signicant differences between the absolute powers and the measures of RTP. This nding implicates that frequent
risk-taking behaviour is reected in the EEG potentially measuring
the reduced interference of the cortical control network in the subcortical regions. We suggest that CFPAC of the EEG, which likely reects the degree of interactions among functional systems, can be a
useful tool for quantifying individuals risk-taking propensity.
Clearly, unlike spectral analysis, the CFPAC mainly uses the
phase information from EEG oscillations. The conceptual framework for the difference between the phase and amplitude of EEG
oscillations has been outlined in detail by Klimesch et al. (2007).
The idea is that the phase represents the timing of neuronal
activity, whereas the amplitude indicates the extent of task

involvement of the relevant neurons in the ongoing EEG (Klimesch


et al., 2007). The discrepancy in our ndings between the CFPAC
and spectral analysis might come from this dissimilar point of view
about the method for neuronal activity. Another intriguing difference between the two methods is that the correlation coefcients
of the CFPAC exhibit more local alterations than the spectral analysis in our topographic ndings. In the case of DGC (75 Hz) of the
BIS as shown in Fig. 2, the topographic patterns of the partial
correlation coefcient vary considerably. This is likely because
the CFPAC might serve as a mechanism to transfer information
from large-scale brain networks to the local cortical processing regions (Jensen and Colgin, 2007). Taken together, these ndings
suggest that the degree of CFPAC may differ across various local
brain areas. Furthermore, the CFPAC measures the amount of timing information from the interacting functional systems across
multiple spatiotemporal scales, unlike the spectral results, which
describe the amount of excitation of the functional neuronal system. Recently, our studies using the CFPAC of scalp EEG have
shown the similar characteristics of CFPAC in different tasks (Park
et al., 2013, 2011).
Our results indicate that the topographic features of the correlation vary across the RTP measures. This variation possibly results

Please cite this article in press as: Lee J, Jeong J. Correlation of risk-taking propensity with cross-frequency phaseamplitude coupling in the resting EEG.
Clin Neurophysiol (2013), http://dx.doi.org/10.1016/j.clinph.2013.05.007

J. Lee, J. Jeong / Clinical Neurophysiology xxx (2013) xxxxxx

from dissimilar properties in each RTP measure that might focus on


different neuronal systems involved in RTP. The assessment of RTP
is limited, and its degrees are varied depending on the type of measures. All of our measures assess different aspects of RTP (Boyer,
2006; Reynolds et al., 2006). The DOSPERT reects the social aspects of RTP (Weber et al., 2002). The scale directly measures
RTP across a number of everyday, real-life situations, such as
investing in stocks, buying a lottery ticket, bungee jumping, engaging in unsafe sex and drunk driving (Harrison et al., 2005). Furthermore, previous work has shown that the risk-taking DOSPERT
scores are negatively correlated with the risk-perception DOSPERT
scores. Unlike DOSPERT, the BIS reects the emotional and affective aspects of RTP, including aggression, depression and impulsivity. However, a number of previous studies have demonstrated
meaningful correlations among these measures of RTP (Hong
et al., 2010; Lejuez et al., 2002).
As expected, the DOSPERT risk-taking and BIS measurements
were negatively correlated with CFPACs, mainly in the frontal
and centroparietal regions. These ndings suggest that increased
interactions between the functional neuronal systems in the frontal and centroparietal regions would be associated with the tendency to avoid risk. This result may be related to the top-down
inhibitory control mechanisms underlying decision-making processes that address risky environments and situations. This could
be evidence for DI (i.e., higher systems inhibiting the lower), which
was proposed by Jackson (1958). A number of studies have demonstrated the key role of the prefrontal and frontal cortex in inhibitory control of behaviour, reward processing and decision
making (Badre, 2008; Brass et al., 2005; Byrnes, 1998; Cole and
Schneider, 2007; Logan, 1994; Reuter and Kathmann, 2004; Van
Leijenhorst et al., 2006, 2010). Recently, Cole and Schneider
(2007) suggested that a set of brain regions, including the dorsolateral prefrontal and posterior parietal cortex, forms a cognitive control network of anatomically distinct component-processing brain
regions that interact in a tightly coupled fashion to implement cognitive control of a variety of tasks (Cole and Schneider, 2007). In
addition, the association between our ndings and DI is supported
by the observation that patients with traumatic brain injuries or
other pathologies affecting the PFC show a tendency towards risky
and impulsive decision making and an apparent disregard for the
negative consequences of their actions (Bechara et al., 1996; Rahman et al., 2001). Moreover, this observation appears to be particularly true for patients with right-sided lesions (Clark et al., 2003;
Tranel et al., 2002). We found meaningful negative correlations between the CFPAC and the BIS measurements in the right frontal
(Fp2) region. The importance of the right frontal lobe in inhibitory
control has been well demonstrated experimentally in previous
works on repetitive transcranial magnetic stimulation and transcranial direct current stimulation-induced functional disinhibition
of the right prefrontal cortex (Fecteau et al., 2007; Knoch et al.,
2006).
On the one hand, we found signicant positive correlations between the CFPAC and the measures of RTP in the right temporal
(T8) and parietal (P8) lobes. From the perspectives of the brain
behaviour relationship for impulsivity and risk-taking, violent
and impulsive behaviour could be categorised as impulsiveemotional or controlledinstrumental (Vitiello and Stoff, 1997).
Impulsiveemotional behaviour occurs suddenly in reaction to
threat within the context of increased impulsivity and emotionality. Controlledinstrumental behaviour, on the other hand, manifests itself as a relatively non-emotional display of aggression
directed at obtaining the goal. According to the result from the
neuropsychological studies for impulsivity, it appears that impulsiveemotional behaviour is closely associated with the greater
right-hemisphere activation, particularly in temporal regions and
connections to limbic and hypothalamic structures, which are

important in the expression and regulation of emotion (Knyazev


et al., 2002; Raine, 2002; Scarpa and Raine, 2000). A previous study
for the psychological differences between left and right temporal
lobe epilepsy has shown that the patients with right temporal lobe
epilepsy were more impulsive and more externalised aggressive
responses than those with left temporal lobe epilepsy (McIntyre
et al., 1976). The patient with temporal lobe epilepsy involuntarily
feels the unexpected phenomena, called experiential phenomena,
of the nonspecic irritation from seizure discharges such as perceptual hallucinations or illusions, memory ashbacks, forced thinkings or emotions (Gloor et al., 1982). It is suggested that the
exaggeration of the emotional function of the right temporal lobe
results in affective instability and emotional expressiveness (McIntyre et al., 1976). Therefore, it is supposed that the positive correlations between the CFPAC and the measures of RTP found in the
right temporal (T8) and parietal (P8) regions are closely related
to the overexpression of the impulsiveemotional function of the
right hemisphere.
So far, many studies for RTP have investigated the neural substrate of risk-taking during the performance of a decision-making
task that might have directly tapped into some of the neurocognitive operations presumed to be involved in mediating risk-taking
behaviours in real-world situations. However, the result of the
present study comes from the analysis of EEG for the resting
eyes-closed condition. How can the resting EEG effectively express
the neural information for RTP? In the present study, there were
several reasons for using the resting EEG for examining RTP. First,
as mentioned in the Introduction section, the RTP for a long-standing trait is explained by the individual state of equilibrium or balance between the reward-related and cognitive control-related
functional networks of the brain (Casey et al., 2008; Steinberg,
2007). From the result of a recent study using functional magnetic
resonance imaging (MRI), the highest global brain connectivity was
found in both the cognitive control network (Cole and Schneider,
2007) and the default mode brain network, the so-called resting
state brain network (Cole et al., 2010). Further, it is thought that
the quantitative EEG (QEEG) for the resting state often provides
valuable information about the balance between large-scale functional brain networks such as the cognitive control network (Cantor, 1999; Prichep and John, 1992). Consequently, it is supposed
that two different types of EEG (resting and during task) might
be evaluating different aspects of RTP, so that the risk-taking decision task mainly assesses reward processing, whereas the resting
EEG mainly reects the cognitive control ability. Second, the research ndings for the default mode brain network have shown
that the resting state is temporally anti-correlated with the task
state (Broyd et al., 2009; Cole et al., 2010). Moreover, a close association between task performance and the strength of anti-correlation has been suggested (Fox et al., 2005). In essence, a healthy
resting state promotes better task performance. It is suggested that
the resting state might reect the performance of the risk-taking
decision task to some degree. Finally, considering the clinical
implication, it is more benecial to use resting than during task
in terms of applicability, time and simplicity.
The most signicant limitation of the present study is that we
could not control the false positives arising from multiple comparisons. To our knowledge, there is no previous study regarding the
differences in topographical pattern between spectral analysis
and CFPAC. We thought that it is meaningful to compare the detailed topographical pattern and characteristic of various frequencies between two different analyses (spectral and cross-frequency
coupling) for the resting EEG. Hence, the design of the analysis of
the present study was complex and involved many comparisons.
However, this is also the studys weak point. Therefore, the results
should be interpreted with caution as preliminary ndings and require further replication.

Please cite this article in press as: Lee J, Jeong J. Correlation of risk-taking propensity with cross-frequency phaseamplitude coupling in the resting EEG.
Clin Neurophysiol (2013), http://dx.doi.org/10.1016/j.clinph.2013.05.007

J. Lee, J. Jeong / Clinical Neurophysiology xxx (2013) xxxxxx

Additionally, we could not exclude the possible confounding


factors of personality traits, intelligence and psychological symptoms such as anxiety and depression. Many previous studies have
focussed on the relationships among these factors, and specic frequency oscillations have been frequently reported as having a close
relationship with various factors, such as personality traits, intelligence and symptoms of anxiety and depression (Chi et al., 2005;
Lutzenberger et al., 1992; Thatcher et al., 2005; Thibodeau et al.,
2006). In addition, various scales and tasks have been presented
to measure RTP and impulsivity recently. It is our weak point that
we used the limited type of scales or tasks for measuring RTP.
Although the CFPAC is not specic to RTP, and thus should be
interpreted with caution, the present study suggests that the
CFPAC in resting EEGs can be used as a potential novel neurophysiological indicator of RTP. We suggest that the CFPAC is likely to be
useful for assessing RTP in individuals who have social, criminal or
health problems and patients with neurological and psychiatric
diseases who are driven to take excessive risks that lead to negative consequences.

Acknowledgments
The authors thank Sujin Kim, Kyung Hee Kim, So Yul Kim,
Yul-mai Song and Young Sung Kim (Neuropsychiatry Research Laboratory, Gongju National Hospital, Chungcheongnam-do, South
Korea) for their valuable help with this study. This work was supported by the Chung Moon Soul Research Center for Bio Information and Bio Electronics (CMSC) in KAIST and a Korea Science and
Engineering Foundation (KOSEF) Grant provided by the Korean
government (MOST) (No. R01-2007-000-21094-0 and No.
M10644000028-06N4400-02810; No. 20090093897 and No. 2009
0083561).

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