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Clinical Neurophysiology
journal homepage: www.elsevier.com/locate/clinph
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-
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
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
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
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
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.
3. Results
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
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
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*
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
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
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)
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
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
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
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
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
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
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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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
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