European Journal of Neuroscience

European Journal of Neuroscience, Vol. 38, pp. 37783785, 2013

doi:10.1111/ejn.12375

COGNITIVE NEUROSCIENCE

Effects of transcranial direct current stimulation on risky

decision making are mediated by hot and cold
decisions, personality, and hemisphere
hler and Claus Lamm
rgen Pripfl, Renate Neumann, Ulla Ko
Ju
Social, Cognitive and Affective Neuroscience (SCAN) Unit, Faculty of Psychology, University of Vienna, A-1010 Vienna, Austria
Keywords: cognitive control, hemispheric specialization, impulsivity, risk-taking, tDCS

Abstract
Previous results point towards a lateralization of dorsolateral prefrontal cortex (DLPFC) function in risky decision making. While
the right hemisphere seems involved in inhibitory cognitive control of affective impulses, the left DLPFC is crucial in the deliberative processing of information relevant for the decision. However, a lack of empirical evidence precludes definitive conclusions.
The aim of our study was to determine whether anodal transcranial direct current stimulation (tDCS) over the right DLPFC with
cathodal tDCS over the lDLPFC (anodal right/cathodal left) or vice versa (anodal left/cathodal right) differentially modulates risktaking in a task [the Columbia Card Task (CCT)] specifically engaging affect-charged (Hot CCT) vs. deliberative (Cold CCT) decision making. The facilitating effect of the anodal stimulation on neuronal activity was emphasized by the use of a small anode
and a big cathode. To investigate the role of individual differences in risk-taking, participants were either smokers or non-smokers.
Anodal left/cathodal right stimulation decreased risk-taking in the cold cognition version of the task, in both groups, probably by
modulating deliberative processing. In the hot version, anodal right/cathodal left stimulation led to opposite effects in smokers
and non-smokers, which might be explained by the engagement of the same inhibitory control mechanism: in smokers, improved
controllability of risk-seeking impulsivity led to more conservative decisions, while inhibition of risk-aversion in non-smokers
resulted in riskier choices. These results provide evidence for a hemispheric asymmetry and personality-dependent tDCS effects
in risky decision making, and may be important for clinical research on addiction and depression.

Introduction
Making the right decisions in a complex environment that is full of
seductive as well as frightening options requires careful weighing of
risks and benets, and a sound regulation of affective impulses.
Recent evidence suggests that the prefrontal cortex (PFC) is a
pivotal area for deliberative processing (Weber et al., 2004;
Krawczyk, 2012; Minati et al., 2012b) as well as cognitive inhibitory control (Cohen, 2005; Ochsner & Gross, 2005; Knoch et al.,
2008; Goldstein et al., 2009; Dolcos et al., 2011; Mitchell, 2011;
Ridderinkhof et al., 2011).
Some neuroimaging (Ernst et al., 2002; Schonberg et al., 2012)
and brain-stimulation studies (Knoch et al., 2006; Fecteau et al.,
2007a) suggest that the right dorsolateral PFC (rDLPFC) may be
particularly critical to exert cognitive control on affective impulses
and therefore to limit the inuence of affect in risky decisionmaking behavior in healthy participants. Observations in substance
abuse disorders that are related to impaired risky decision-making
behaviors (for review, see Murphy et al., 2012) further support the
idea of a lateralization of DLPFC function in risky decision making

Correspondence: Dr J. Prip, as above.

E-mail: juergen.prip@univie.ac.at
Received 21 June 2013, revised 27 August 2013, accepted 3 September 2013

(Cservenka & Nagel, 2012). Smokers, for example, who reliably differ from non-smokers in traits affecting cognitive control like impulsivity and sensation seeking (Baker et al., 2004; Ryan et al., 2013),
and who behave highly risky in a variety of real-life situations
(Hersch & Viscusi, 1998), show lower rDLPFC activity in cognitive
control tasks than non-smoking controls (Nestor et al., 2011).
However, the interpretation of these ndings in terms of cognitive
control is problematic because the tasks commonly used to study
risky decision-making behavior did not allow for a clear separation
between affect-charged and deliberative processes (Figner et al.,
2009). Hence, some authors have interpreted rDLPFC activity during risky decision making in terms of deliberative thinking (Rao
et al., 2008; Mohr et al., 2010), although evidence for the involvement of the DLPFC in deliberative processing is most prominent for
the left (l)DLPFC in healthy (see Vallar & Bolognini, 2011; for
review) as well as clinical populations (see Demirtas-Tatlidede
et al., 2013, for review).
We assessed hemispheric transcranial direct current stimulation
(tDCS) effects on risky decision making by means of placing a
small-sized anodal electrode over the rDLPFC with a big-sized cathode over the lDLPFC (anodal right/cathodal left) and vice versa (i.e.
small anode left/big cathode right). Different sizes of electrodes
were used for two reasons: rst to improve focality of anodal tDCS;
and second to maximize the facilitating neuronal effect of the anode

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DLPFC and risk-taking 3779

and to minimize the inhibitory effect of the cathode (see Materials
and methods: tDCS). The experimental task we used [Columbia
Card Task (CCT); Figner et al., 2009] was specically designed to
assess risky decision making under differential involvement of deliberative vs. affective processes. Furthermore, by including a group
of smokers and non-smokers, we aimed to assess if individual
differences in risk-taking propensity can be attributed to lateral PFC
functions.

Materials and methods

Participants
Forty healthy university students participated in the study. Students
received course credits for participation, independent of their performance in the CCT. Four participants had to be excluded for incomplete behavioral data. The remaining sample consisted of 18
smokers (age: mean  SD, 22.4  2.5 years; 10 females) and 18
non-smokers (21.0  1.5 years; 15 females). Smokers had been
smoking at least 10 cigarettes per day for at least 1 year, and had a
mean score of 2.44  1.4 in the Fagerstrom Test for Nicotine
Dependence (Heatherton et al., 1991). Participants were all righthanded, as assessed by the Edinburgh Handedness Inventory (Oldeld, 1971), with normal or corrected-to-normal vision, and had
been screened for the absence of present or past neurological or psychiatric conditions and use of psychoactive medication. All were
naive to the goals of the experiment, and gave informed written
consent. The study was conducted in conformity to the Declaration
of Helsinki and approved by the ethics committee of the University
of Vienna.
Experimental design
In a within-subjects design, each participant joined three tDCS sessions with different stimulation conditions [anodal electrode placed
over the lDLPFC with the cathode placed over the rDLPFC (anodal
left/cathodal right), anodal electrode placed over the rDLPFC with
the cathode placed over the lDLPFC (anodal right/cathodal left), and
sham stimulation], with at least 1 week between sessions. The
sequence of stimulation conditions was counterbalanced across
participants. For sham stimulation, electrode positions of both verum
stimulations (anodal left/cathodal right, anodal right/cathodal left)
were balanced across participants. The sequence of the tasks, i.e. the
Hot and Cold version of the CCT (see below), was counterbalanced
across participants, but task order was kept constant within participants for the three sessions to avoid confounding task order effects
with stimulation conditions.
After electrode application, participants were seated in a comfortable chair in a sound-attenuated, dimmed room equipped with
an intercom to the experimenter. Before starting the stimulation,
participants were given a training session to familiarize them with
the CCT, which was presented on a 19-Zoll-CRT-Monitor placed
at a 60-cm viewing distance. Participants were instructed to sit
quietly with their eyes open for the rst 5 min of stimulation, after
which task presentation started. Stimulation of the verum sessions
was terminated after 15 min. Processing of the tasks lasted a few
(35) minutes longer, depending on the individual reaction times.
Note that verum post-stimulation effects have been documented to
last at least for 1 h (Nitsche & Paulus, 2001). After electrode
removal, participants had to answer a questionnaire about the
adverse effects of brain stimulation (based on Brunoni et al.,
2011).

CCT
In the CCT, participants are instructed to maximize their game
scores during each game round by choosing how many cards they
would like to draw out of a total of 32 hidden gain or loss cards.
An optimal strategy to maximize the total score needs to take into
account three factors, which are orthogonally varied trial by trial: (a)
probability of a loss (pL = 1 or 3 loss cards); (b) gain amount
[GA = 10 (low) or 30 (high) points per gain card]; and (c) loss
amount (LA = 250 or 750 points). In the 24 rounds of the Hot
task version of the game, participants make stepwise incremental
decisions by turning only one card at a time with immediate feedback provided after each choice. At any point in each round, participants can choose to stop their card selection (thus obtaining the
rounds payoff), or continue to choose cards until a losing card is
selected (which leads to a subtraction of the LA in that round, and
ends the round). This dynamic nature in which risk increases over
time within a trial is similar to other risk-taking tasks like the Balloon Analogue Risk Task (Lejuez et al., 2002), which has also been
used in previous tDCS studies (e.g. Fecteau et al., 2007b; Boggio
et al., 2010a). The position of loss cards was randomized for each
round and not xed (as in Figner et al., 2009), in order to avoid the
impression of rigged feedback (for details, see Figner et al., 2009).
In the Cold task version of the game, decisions are not made stepwise and there is no immediate feedback. Instead, participants are
asked to indicate only the number of cards (from 0 to 32) they
would like to turn over on a given trial. Players receive feedback on
their performance only at the very end of the whole CCT session,
by means of a summary score after the last of the 24 rounds.
According to Figner et al. (2009), the number of cards chosen,
independent of the game factors, represents an index of risk-taking,
while the number of cards chosen as a function of the game factors
represents an index of information use. It is crucial to note that the
two versions of the CCT elicit different decision-making processes.
The Hot CCT elicits higher emotional arousal, as indexed by electrodermal activity, is positively correlated with the motivationalaffective construct need-for-arousal, and has been shown to elicit
strategies predominantly based on affect-charged decision-making
behavior. The Cold CCT, in contrast, elicits strategies predominantly
based on mathematical calculations and reasoning, and has been
shown to be independent from impulsive personality characteristics
(Figner et al., 2009). Hence, risk-taking in the Hot CCT is more
strongly inuenced by affective processes, while deliberative decision-making processes prevail in the Cold CCT.
tDCS
Anodal tDCS was delivered over three sintered Ag/AgCl electrodes
(sized 5.3 cm in total), which were connected by an electrode
splitter cable (1 to 3) to the anodal output of a battery-driven, constant-current stimulator (DC-STIMULATOR PLUS, neuroConn
GmbH, Erlangen, Germany). Small electrodes were used for anodal
stimulation to improve the focality of tDCS (Marshall et al., 2004;
Nitsche et al., 2007; Datta et al., 2009; Faria et al., 2009; Miranda
et al., 2009; Minhas et al., 2010). Positions F1, F3 and AF1 according to the international 1020 electrode system (Jasper, 1958) were
used for left hemisphere anodal stimulation (anodal left/cathodal
right hitherto). For right hemisphere anodal stimulation (anodal
right/cathodal left), electrodes were positioned at F2, F4 and AF2.
Electrodes were positioned and kept in place by using an elastic
and individually tted electroencephalogram (EEG)-cap (EASYCAP
Ges.m.b.H., Herrsching, Germany). The 7 9 5 cm cathodal reference

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European Journal of Neuroscience, 38, 37783785

3780 J. Prip et al.

electrode was centered contralateral at positions F3 and F4, respectively, with the short side running in parallel to the imaginary Cz-Fz
connecting line. Stimulation electrodes were lled with degassed
electrode gel (Electro-Cap International, Eaton, USA), and the skin
under the electrodes had been cleaned with alcohol and slightly
scratched to decrease skin resistance (Bauer et al., 1989). This
method assured electrode impedance values of 3 kO, as individually measured by an impedance meter (Ing. Zickler Ges.m.b.H.,
Pfaffstatten, Austria). At the side of the surface sponge electrode the
skin was only cleaned with alcohol, but not scratched, as this might
have created unwanted focal cathodal stimulation effects.
A direct current of 0.45 mA intensity, resulting in an anodal current density of 0.085 mA/cm, was induced for 15 min in the verum
sessions, and for 30 s with 30 s fade-in and 30 s fade-out in the
sham session. Modeling studies showed that 0.45 mA delivered over
an electrode size of about 5 cm induces a comparable current intensity at the surface of the cortex to 1 mA over a 35 cm electrode
(Miranda et al., 2009). At the cathode a direct current density of
0.013 mA/cm was induced. Because a minimum current density of
0.017 mA/cm was previously shown to be necessary to modify
motor cortex excitability by tDCS (Nitsche & Paulus, 2000), current
density at the reference electrode might be considered as functionally irrelevant.
Assessment of personality characteristics
Participants had to answer questionnaires assessing cognitive control-related personality characteristics [Barratt Impulsiveness Scale
(BIS11), Patton et al., 1995; Substance Use Risk Prole Scale
(SURPS), Woicik et al., 2009; BIS/BAS scale, Carver & White,
1994] and one additional question concerning risk-aversion: It
frightens me when I have to make decisions which involve risk
(four-point scale: strongly disagree; disagree; agree; strongly agree).
Data analysis
The main outcome measures were the number of cards chosen. To
account for differences in the procedures and the interpretation of
the game parameters, the Hot and Cold versions of the CCT were
analysed using separate statistical analyses. Linear mixed models
with restricted maximum likelihood estimation were used to control
for heteroscedasticity and to include time-dependent covariates,
which was necessary because of the within-subject design (Gueorguieva & Krystal, 2004; McCulloch & Searle, 2005; Heck et al.,
2011). For the two versions of the CCT we evaluated the withinsubjects xed factors stimulation condition (sham, anodal left, anodal right), GA (low, high), LA (low, high) and pL (low, high);
the between-subjects xed factor smoking group [smokers (S),
non-smokers (NS)] and the random factor subjects in a full-factorial
model. For the Hot version the number of cards chosen in the Cold
CCT and the number of negative feedbacks were introduced as
time-dependent covariates, to control for the inuence of deliberative processing and negative feedback, respectively. Schwarzs
Bayesian criteria (Schwarz, 1978) were used to determine the besttting variancecovariance structure, which was determined to be
Diagonal. Bonferroni corrected post hoc tests were used to examine
interactions and omnibus main effects. Signicance was evaluated at
P < 0.05. All post hoc values are reported following correction for
multiple comparisons. All data are reported as means  SE. Group
differences in personality characteristics were assessed by means of
independent t-tests. Each dichotomized scale (absent, present) of the
adverse effects questionnaire was subjected to a Chi-square test to

compare smoking groups and a Cochran-Q test comparing the three

stimulation conditions. Statistical analyses were performed using
IBM SPSS Statistics 20 (IBM, Chicago, IL, USA).

Results
Adverse effects
The frequencies of reported adverse effects did neither differ
between the three stimulation conditions nor between smokers and
non-smokers, except that more non-smokers reported itching sensations during anodal left stimulation (61% vs. 22%). The three most
frequently reported adverse effects were sleepiness (56%), tingling
(45%) and itching (32%).
Questionnaire data
As for the questionnaire data, smokers scored higher in the SURPS
subscales
Impulsivity
(S = 10.3  1.5;
NS = 8.8  1.9;
t34 = 2.525, P = 0.016) and Sensation Seeking (S = 17.8  2.6;
NS = 14.7  2.1; t34 = 3.947, P < 0.001), and in the BIS11 total
score (S = 67.3  7.2; NS = 57.9  8.6; t34 = 3.592, P = 0.001).
Non-smokers scored higher in the SURPS Anxiety Sensitivity subscale (S = 10.8  2.9; NS = 12.8  3.0; t34 = 2.047, P = 0.048),
the inhibition scale (BIS) of the BIS/BAS scale (S = 19.5  4.3;
NS = 22.7  3.9; t34 = 2.319, P = 0.027) and the risk-aversion
scale (S = 2.2  0.5; NS = 2.9  0.7; t34 = 3.370, P = 0.002).
Cold CCT
Analysis of the Cold CCT revealed a signicant main effect for
stimulation condition (F2,351 = 4.330, P = 0.014). Bonferroni
post hoc tests showed that anodal left/cathodal right (P = 0.014) but
not anodal right/cathodal left (P = 1.000) stimulation resulted
in decreased risk-taking compared with sham stimulation (Fig. 1).

Fig. 1. Risk-taking (as indicated by the number of cards chosen in the risky
gamble) in the Cold CCT, averaged across smokers and non-smokers.
Anodal left/cathodal right stimulation over the DLPFC led to a decrease in
risk-taking, in comparison to sham stimulation; whereas anodal right/cathodal
left stimulation had no effect. Left: anodal left/cathodal right; right: anodal
right/cathodal left.

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DLPFC and risk-taking 3781

Further signicant main effects revealed that the number of chosen cards was higher for trials with high GA (F1,556 = 95.339,
P < 0.001), low LA (F1,556 = 381.664, P < 0.001) and lower pL
(F1,556 = 506.338, P < 0.001).
In addition, there were signicant interactions for GA 9 pL
(F1,556 = 9.976, P = 0.002) and LA 9 pL (F1,556 = 17.903,
P < 0.001). However, none of the interactions with stimulation condition was signicant (all P-values > 0.1). This pattern of ndings
for the gamble factors reveals that information about risk conditions
was appropriately used by participants, but that information use was
not modulated by tDCS stimulation.
Further signicant interactions were found for smoking
group 9 GA (F1,556 = 5.090, P = 0.024) and smoking group 9 pL
(F1,556 = 9.333, P = 0.002). Bonferroni post hoc tests showed that
smokers took higher risks than non-smokers under conditions of
high GA (P = 0.037), as well as under conditions of low pL
(P = 0.027). All other main effects and interactions were non-significant (all P-values > 0.08), including the interaction group 9 stimulation (P = 0.318).
Hot CCT
The analysis of the Hot condition revealed neither a signicant main
effect for smoking group nor for stimulation condition (all P-values
> 0.195), but a signicant interaction of stimulation condition 9 smoking group (F2,361 = 6.324, P = 0.002). Bonferroni post
hoc tests revealed that smokers showed a decrease in risk-taking
during anodal right/cathodal left compared with sham stimulation
(P = 0.046), whereas non-smokers showed the opposite pattern, i.e.
an increase in risk-taking under anodal right/cathodal left compared
with sham stimulation (P = 0.031). Furthermore, compared with
non-smokers, smokers took signicantly higher risk during the sham
condition (P = 0.010), but not during anodal left/cathodal right or
anodal right/cathodal left stimulation (all P-values > 0.1; Fig. 2).
Note that when conducting an analysis without covariates the results
were essentially identical (stimulation condition 9 smoking group:
F2, 352 = 7.245, P = 0.001).

Fig. 2. Risk-taking in the Hot Columbia Card Task (CCT). Smokers and
non-smokers showed the opposite pattern: compared with sham stimulation,
anodal right/cathodal left tDCS resulted in lower risk-taking in smokers but
higher risk-taking in non-smokers. In addition, the two groups differed in
their baseline risk-taking behavior during sham stimulation, where smokers
showed higher risk-taking than non-smokers. Left: anodal left/cathodal right;
right: anodal right/cathodal left.

In the Hot CCT, signicances of main effects and interactions of

the gambling factors, i.e. GA (F1,556 = 46.229, P < 0.001), LA
(F1,556 = 54.783, P < 0.001), pL (F1,683 = 296.130, P < 0.001) and
GA 9 pL (F1,515 = 17.402, P < 0.001), were similar to the Cold
version except for LA 9 pL, which was very close to the chosen
signicance threshold though (F1,519 = 3.162, P = 0.076).
Furthermore, signicant interactions were found for smoking
group 9 LA (F1,510 = 5.336, P = 0.021), smoking group 9 pL
(F1,515 = 5.811, P = 0.016) and smoking group 9 GA 9 LA
(F1,510 = 4.005, P = 0.046). Bonferroni post hoc tests revealed that
in the Hot CCT smokers showed particularly higher risk-taking than
non-smokers in conditions that combine high GA with low LA
(P = 0.015), and on a trend level in conditions with low pL
(P = 0.058). In analogy to the Cold CCT these patterns were not
affected by the type of stimulation (P-values > 0.1).

Discussion
We used two different versions of a risky decision-making game,
and investigated whether anodal left/cathodal right or anodal right/
cathodal left tDCS over the DLPFC inuences the risky choices
made in this game in two different groups (S vs. NS). To improve
focality and emphasize the facilitating effect of anodal stimulation, a
small-sized anode and a big-sized cathode were used. Our results
demonstrate that tDCS over the DLPFC affects risky decision making, and that these effects are modulated by the stimulated hemisphere, the type of task and the group. Briey, anodal left/cathodal
right stimulation decreased risk-taking in the cold cognition version of the task, in both groups, while in the hot version, anodal
right/cathodal left stimulation decreased risk-taking in smokers and
increased it in non-smokers.
In terms of their general behavior, participants acted in line with
theoretical predictions and previous observations using similar task
setups (Figner et al., 2009). Most importantly, information use was
as expected in both the Cold and the Hot CCT, because higher GA,
lower LA and a lower pL all resulted in a higher number of cards
chosen (i.e. risks taken). However, the difference in cards chosen
between the Hot and Cold CCT was reversed and smaller in our
study than reported in Figner et al. (2009). This can be explained
by the fact that Figner et al. (2009) used a xed feedback strategy,
i.e. the game was programmed in a way that loss cards would only
be presented at the very end of a game round (i.e. the last card, or
if more than one loss card was included the last possible card). To
maintain the impression of playing a game of chance, Figner et al.
interspersed a few loss trials in which a xed loss was incurred,
independently of the participants choice. This procedure implies the
possibility that participants detect the rigged nature of the feedback.
Therefore, the position of loss cards was fully randomized in our
version of the Hot CCT, and this may have resulted in fewer cards
chosen than in the Cold CCT. The ndings of Huang et al. (2013)
further support this interpretation. They used the Warm CCT,
which provides feedback at the trial by trial level, rather than the
card by card level, to avoid participants detecting the rigged nature
of feedback. This manipulation on the feedback strategy of the Hot,
respectively, Warm CCT resulted, in agreement with our observations, in more cards turned over on average in the Cold CCT than
in the Warm CCT, but with the Warm CCT still arousing stronger
emotions (Huang et al., 2013). When comparing information use of
smokers and non-smokers, similar patterns could be observed for
the two versions of the CCT. For instance, smokers took higher
risks than non-smokers when pL was low (Hot and Cold CCT),
when there was much to win (Cold CCT), and in trials that

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3782 J. Prip et al.

combined high wins with low LA (Hot CCT). However, these decision patterns were not affected by the type of stimulation.
The results of the Cold CCT, in which more cautious decisions
were obtained after anodal left/cathodal right but not anodal right/
cathodal left stimulation in both groups, are in agreement with our
hypothesis. The Cold CCT has been shown to elicit strategies predominantly based on mathematical calculations, and does not correlate with the need-for-arousal construct (Figner et al., 2009). Thus,
decision making in the Cold CCT is said to be independent from
personality characteristics, such as impulsivity or sensation seeking
(Figner et al., 2009). This assumption ts well with the lack of
baseline differences in risk-taking between smokers and non-smokers
in the Cold CCT. We attribute the decrease in risk-taking after anodal left/cathodal right stimulation over the DLPFC in both groups to
a modication of deliberative reasoning and stimulus processing.
This interpretation is supported by results showing that particularly
stimulation with the anode placed over the lDLPFC results in the
modication of executive processes that play a major role in deliberative processing, such as working memory (Keeser et al., 2011b),
probabilistic reasoning (Hecht et al., 2010) and planning (Dockery
et al., 2009). A recent study by Xue et al. (2012) further supports
this interpretation. Based on functional magnetic resonance imaging
(fMRI) data showing the left DLPFC being strongly activated in
strategic decision making, subsequently applying anodal tDCS over
this region resulted in modication of the decision-making strategy.
Our hypothesis concerning the effect of tDCS on affect-charged
risky decisions (as assessed by the Hot CCT) could partly be conrmed. As expected, we did not nd signicant modulation of risktaking by anodal left/cathodal right stimulation over the DLPFC in
either group. More importantly, anodal right/cathodal left stimulation
decreased risk-taking, but only seen in smokers, whereas non-smokers showed increased risk-taking. When interpreting this opposite
effect on risk-taking for smokers and non-smokers, differences in
baseline risk behavior need to be taken into account. Comparing the
baseline level of risk-taking, i.e. risk-taking during sham stimulation,
smokers showed signicantly higher risk-taking than non-smokers in
the Hot CCT. This is in agreement with previous ndings (e.g.
Hersch & Viscusi, 1998; Lejuez et al., 2003; Hakes & Viscusi,
2007; Anderson & Mellor, 2008). Furthermore, and as predicted,
these differences in risk-taking were accompanied by individual differences in personality characteristics (e.g. Fields et al., 2009; Ryan
et al., 2013): while smokers scored higher in impulsivity (SURPS,
BIS11) and sensation seeking (SURPS), non-smokers showed higher
behavioral inhibition (BIS scale), anxiety sensitivity (SURPS) and
risk-aversion.
Based on this pattern of ndings, the opposing tDCS effects in
the two groups might be explained by the engagement of the same
inhibitory control mechanism associated with rDLPFC (Knoch
et al., 2006). In smokers, with their higher impulsivity and sensation
seeking, increased cognitive control of affective impulses leads to a
reduction of risky decisions. In the risk-averse and more loss-sensitive non-smokers, on the other hand, cognitive control might act
upon and inhibit the inuence of bottom-up aversive impulses
signaling to be careful in risky choices hence resulting in less conservative and therefore more risky decisions. Two lines of evidence
support this interpretation: rst, it has been shown that low sensation
seekers, as the non-smokers in our study, display enhanced anxious
anticipation of negative consequences. For example, indicators of
anticipatory aversive affect, such as fear-potentiated startle responses
to unpredictable stimuli, are increased in low sensation seekers
(Lissek et al., 2005). This suggests a stronger bottom-up engagement
of aversive physiological and affective responses in unpredictable

situations, such as risky decisions. Second, it has been shown that

stimulation by means of anodal right/cathodal left tDCS over the
DLPFC can boost response condence during risky decisions in
healthy risk-averse participants (Minati et al., 2012a), and this has
been attributed to strengthened cognitive control (Camchong et al.,
2007).
Concerning the often reported risk-seeking propensity of smokers,
our results support the longstanding idea in psychology that resisting
temptations reects competition between impulses and self-control
(Hofmann et al., 2009). Strengthening self-control by means of
increasing rDLPFC activation helps smokers to stie risk-seeking
impulsivity. However, our data do not allow concluding that
increased risk-taking of smokers is due to maladaptive cognitive
control (Feil et al., 2010; Goldstein & Volkow, 2011). Our results
rather show that different personality characteristics, i.e. smokers
being risk-seekers and non-smokers scoring not only lower in sensation seeking and impulsivity but also higher in risk-aversion and
anxiety sensitivity, are responsible for the observed differences in
risk-taking between groups.
It might be argued that general differences in the cognitive processes and task demands engaged by the Hot and Cold CCT, termed
learning demands by Figner et al. (2009), might be an alternative
explanation for the reported results. For instance, the Hot CCT
requires participants to keep track of the increasing probability of
losing with each card they have turned over. This might involve
higher demands on working memory, which has also been associated with DLPFC function. However, what speaks against this alternative explanation is the fact that smokers and non-smokers showed
effects in opposite directions in the Hot CCT contradicting a general effect attributable to modulation of working memory function.
Furthermore, neither Figner et al. (2009) nor Huang et al. (2013)
found any evidence for differential learning demand effects for the
Cold and Hot CCT versions in their studies.
As the Cold CCT was designed to trigger mainly deliberative
decision making (Figner et al., 2009), but not exclusively, it could
also be argued that the Cold CCT is not completely free of affective
processes. This could make it difcult to separate deliberative from
affective processing in the two versions of the CCT. However, those
versions of the CCT that have been designed to engage affective
processes (i.e. the Hot CCT and the Warm CCT) indeed seem to
arouse stronger emotions during decision making than the Cold
CCT, as shown in previous behavioral studies (Figner et al., 2009;
Huang et al., 2013). Furthermore, the study by Figner et al. (2009)
demonstrated that the Cold CCT elicits strategies predominantly
based on mathematical calculations and reasoning, while strategies
to solve the Hot CCT are predominantly based on affect-charged
decision-making behavior, as shown by self-reported decision strategies. While Huang et al. (2013) could not replicate these differences
in strategies when comparing the Warm CCT with the Cold CCT,
this might have been due to limitations of the self-report measures
used, according to the authors. Thus, although minor affective
processing might have been induced during playing the Cold CCT,
results of the Cold CCT of our study are more plausibly explained
in terms of involvement and modication of deliberative processes.
It should further be noted that cognitive inhibitory control or
cognitive control is necessary for a variety of impulsive behaviors
(for an overview, see Ohmura et al., 2012), like impulsive action
(e.g. Go/No Go task or stop-signal-reaction-time task; e.g. Logan
et al., 1997; Steinbeis et al., 2012); impulsive choice (e.g. delay
discounting; e.g. Cho et al., 2012); risky behavior (for review, see
Boyer, 2006); or substance craving (e.g. George & Koob, 2011;
Hayashi et al., 2013). Our study refers to cognitive control in risky

2013 Federation of European Neuroscience Societies and John Wiley & Sons Ltd
European Journal of Neuroscience, 38, 37783785

DLPFC and risk-taking 3783

behavior, i.e. limiting the inuence of affect in risky decision making. Cognitive control in other impulsive behaviors might be based
on partly overlapping (for review, see Cohen & Lieberman, 2010),
but probably not identical, brain mechanisms. Comparing, for example, the effects of high-frequency repetitive transcranial magnetic
stimulation (rTMS) over the lDLPFC (with rDLPFC not studied) on
delay discounting and risky decision making [Risky Choices Gambling Task (RCGT)] in the same sample (smokers and non-smokers), signicant modication of delay discounting compared with
sham stimulation was observed, but there was neither a difference
between the active and sham rTMS condition for risky decision
making nor for cigarette consumption (Sheffer et al., 2013). Using
the same risk task, i.e. the RCGT, Knoch et al. (2006) found that
inhibiting activity by rTMS over the right, but not over the left,
DLPFC modulates risky decision making, which is in agreement
with our observations in particular because the RCGT measures
mainly affect-charged risky decision making with little strategic
planning. Together, these ndings speak against a domain general
cognitive inhibitory control mechanism within the DLPFC and for a
prominent role of the rDLPFC for cognitive control of affective
processes in risky decision making.
It has also been proposed that non-invasive brain-stimulation
treatment effects of addiction are linked to shifts in decision making
related to the role of the DLPFC in impulsivity control (e.g. Boggio
et al., 2010b; for review, see Fecteau et al., 2010). However, as our
study did not assess craving and the effects of the specic electrode
setting used in our study have never been explored for the potential
to modify craving, testing this hypothesis is not within the scope of
this study.
In general, the spatial resolution of tDCS is known to be limited.
To improve spatial specicity and emphasize the facilitating effect
of the anodal stimulation, we used small EEG electrodes focused
over the DLPFC, and a large sponge electrode was placed contralateral with the intention to make the cathode functionally ineffective
(Marshall et al., 2004; Nitsche et al., 2007; Datta et al., 2008;
Minhas et al., 2010). Nevertheless, the exact distribution of the
electric eld generated by tDCS is not known (Datta et al., 2009;
Dmochowski et al., 2011; Faria et al., 2011), and cathodal functional ineffectiveness of current densities below 0.017 mA/cm as
used in this study (0.013 mA/cm) has only been shown for the
motor cortex (Nitsche & Paulus, 2000) but not for other regions.
Further studies, in particular ones providing information on the
precise neural effects, such as combinations of tDCS with fMRI, are
therefore necessary to clarify the inuence of such electrode settings
on DLPFC activity and whether other areas were also stimulated
and therefore might contribute to the observed effects (Keeser et al.,
2011a). The specic stimulation protocol used, particularly the
combination of small-sized EEG electrodes with a big-sized sponge
electrode, and the consideration of personality characteristics in our
study might also explain some disparity to results of other studies
dealing with risky decision making and non-invasive brain stimulation of the DLPFC (Fecteau et al., 2007a,b).
We show that anodal right/cathodal left tDCS over the DLPFC
predominantly modulates regulation of affective impulses, and the
opposite electrode setting, i.e. anodal left/cathodal right stimulation,
mainly inuences deliberative processing of risky decision-making
behavior. Upregulating the activity of the rDLPFC seems to increase
cognitive control of affective impulses. However, the direction of
effects on risk-taking when strengthening cognitive control depends
on the valence of affective impulses: improved controllability of
risk-seeking temptations leads to more conservative decisions vs.
inhibition of risk-averse apprehensiveness results in riskier choices.

These ndings are relevant for mechanistic models of decision making, and suggest that individual differences, the type of decisions
and hemispheric variability need to be taken into account in such
models. Our results also provide further insights into the development of interventions using non-invasive brain stimulation to treat
psychiatric disorders associated with decision-making problems,
such as addiction or depression.

Acknowledgements
This study was nancially supported by the MMI-CNS research cluster (University of Vienna and Medical University of Vienna), by funds of the Oesterreichische Nationalbank (Anniversary Fund, project number: 14350) and the
Austrian Science Fund (P22813). The authors are grateful to Bernd Figner
for providing the software of the Columbia Card Task (CCT). The authors
declare no competing nancial interests.

Abbreviations
BIS, Barratt Impulsiveness Scale; CCT, Columbia Card Task; DLPFC, dorsolateral prefrontal cortex; EEG, electroencephalogram; fMRI, functional magnetic resonance imaging; GA, gain amount; LA, loss amount; lDLPFC, left
dorsolateral prefrontal cortex; NS, non-smoker; PFC, prefrontal cortex; RCGT,
Risky Choices Gambling Task; rDLPFC, right dorsolateral prefrontal cortex;
rTMS, repetitive transcranial magnetic stimulation; S, smoker; SURPS, Substance Use Risk Prole Scale; tDCS, transcranial direct current stimulation.

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