Acx 065
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Abstract
Objective: Decision-making in the Iowa Gambling Task (IGT) has been intensively studied regarding both the “hot” and “cold” compo-
nents. The ventromedial prefrontal cortex is a key region involved in processing somatic marker information, though recent findings suggest
dorsolateral regions are also important. The dorsolateral prefrontal cortex is also known as a substrate of executive functions—the cold com-
ponent of decision-making. However, there is contradictory evidence about the role of executive functions, as well as the hot component of
decision-making—emotional intelligence. Previous findings suggest that patients with right frontal lobe lesions find decision-making more
problematic in IGT. The goal of this study is to replicate previous findings on IGT performance in patients with dorsolateral lesions com-
pared to controls.
Methods: We obtained data from patients with right frontal lobe tumors (n = 12), localized in the dorsolateral prefrontal cortex, and
healthy controls (n = 21) who undertook the IGT, Wisconsin Card Sorting Test (WCST), Mayer–Salovey–Caruso Emotional Intelligence
Test (MSCEIT), and D-KEFS Color-Word Interference Test.
Results: The performance in the IGT, WCST, and EI tests is impaired in the clinical group. At the subgroup level, we found patients had
lower EI scores regarding the ability to use “emotions for thinking facilitation”. However, we found an interaction between the EI scores
regarding the ability “the perception and identification of emotions” and the performance on WCST only in the patient group.
Conclusion: This study raises the possibility of identifying components of EI which could be helpful in understanding the impairment of
patients with right dorsolateral lesions.
Keywords: Iowa Gambling Task; Right frontal lobe tumor; Tumor patients; Executive functions; Lateral prefrontal cortex; Emotional intelligence
Introduction
This work investigates an intriguing and extensively studied process—decision-making. Research on decision-making
under uncertainty reveals important characteristics of human behavior as a holistic act and distinguishes quantitative specifics
of human behavior from animal behavior. If decision-making is evaluated through the prism of making the right choice, of
picking one option among several, then this choice could be explained as a result of calculations of gains and losses (the
“cold” component of decision-making) with emotional reactions having an affect on the desirability of each option (the “hot”
component of decision-making). While cold decision-making is related to cognitive and rational processes, hot decision-
making is associated with emotional and affective processes (Brand, 1985; Damasio, 1994; Shafir, Simonson, & Tversky,
1993). Hot components, such as affective and emotional reactions, help humans to act in situations requiring immediate
action, while cold components such as the rational determination of risks and the benefits of each possible action are more
valuable in stable situations (Séguin, Arseneault & Tremblay, 2007). These two factors or types of thinking are also referred
© The Author 2017. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
doi:10.1093/arclin/acx065 Advance Access publication on 19 July 2017
O. Zinchenko, E. Enikolopova / Archives of Clinical Neuropsychology 32 (2017); 1026–1036 1027
to as System 1 and System 2 theoretical components, respectively (Kahneman, 2003). Executive functions (EF), such as plan-
ning, cognitive flexibility and working memory are thought to be linked to the “cold” part of decision-making. We could
assume that the “cold” component of decision-making could be measured on tests with emotionally neutral stimuli, such as
the Stroop Test or Wisconsin Card Sorting Test (Roiser et al., 2013). In contrast, the “hot” component of decision-making, as
mentioned before, involves the processing of emotionally significant information, such as gain–loss comparison and reward
anticipation in the Iowa Gambling Task (IGT).
Initially IGT was tested in patients with ventromedial prefrontal lesions who made significantly more disadvantageous de-
cisions compared to controls (Bechara, Damasio & Damasio, 2000a, 2000b; Bechara, Damasio, Damasio & Anderson, 1994).
These patients, who ignore the long-term consequences of their actions, are insensitive to the emotions of others and unable
to learn after making errors, so consequently they show risky behavior. Bechara and colleagues (1994) suggests a “somatic
marker hypothesis” to explain the origins of this behavior: “somatic markers” are the interoceptive signals associated with
subliminal emotions, which help to guide the decision-making process. Physiological changes, experienced for the first time
Our study recruited two participant groups consisting of 12 patients with right frontal lobe tumors and 21 healthy controls
(2:3 study design). Participants were recruited from the Moscow Burdenko Institute of Neurosurgery prior to tumor surgery.
All patients suffered from convexital brain tumors in the right hemisphere, mostly localized in the lateral prefrontal cortex
region, and diagnosed by neurological and neuroimaging assessment. Patients were examined 1–2 days after their admission
to hospital, before surgery. The visits were done in Russian language. Data about the site of lesions were collected by review-
ing patient records and confirmed by the neurologist. Participants of the control group were recruited by e-mail and social net-
works from the Lomonosov Moscow State University and related institutions. Participants in the sample were native Russian
speakers, with at least 1 year of higher (post-secondary) education and were at least 18 years of age. Exclusion criteria were:
left-handedness or ambidextrous (screened by the neuropsychological assessment by Luria’s battery and Annett’s question-
naire of functional asymmetry), other neurological diseases (e.g. epilepsy, aneurism), aphasia and agnosia symptoms, psychi-
• Luria’s Neuropsychological battery (Luria, 1973). This battery includes neuropsychological probes to assess a variety
of cognitive functions: attention, perception of different modalities, handedness, memory, and EF. A questionnaire
about sociodemographic characteristics was included.
• IGT (Bechara et al., 1994). A computerized version of IGT was used (PEBL free software, http://pebl.sourceforge.
net/). The participant is instructed to pick up a card from four decks of cards over the course of 100 trials. Two of
these decks are advantageous (C and D) because they consist of cards with small losses and high long-term gains,
while two others (A and B) are disadvantageous due to the probability of receiving a high monetary loss once every
10 trials. Performance in IGT was assessed by a set of different measures: The total score as a parameter of general
productivity is calculated by subtracting the number of disadvantageous deck selections from the number of advanta-
geous selections (C + D) – (A + B) as well as the partial performance of sets of 20 trials (0–20, 20–40, 40–60,
60–80, 80–100). We also calculated the quantity of choices to access preferences for each deck across all four decks.
The partial performance in blocks of 20 trials has been performed in order to examine the ability to learn about
advantageous and disadvantageous decks using somatic markers from early trials (0–20) to final trials (80–100). The
scores for the performance on the IGT for five consecutive blocks of 20 cards are calculated by subtracting the num-
ber of advantageous selections (decks C, D) from the number of disadvantageous selections (decks A, B). The learn-
ing curves have been created to represent the process of learning.
• WCST (Heaton, Chelune, Talley, Kay, & Curtis, 1993) provides information about cognitive reasoning and flexibil-
ity, and the set-shifting of the participant. It also can be used for the assessment of the level of brain damage to the
prefrontal cortex. Raw scores were used in the analysis (percentage errors and perseverative errors).
• D-KEFS Color-Word Interference Test (Delis, Kramer, Kaplan & Holdnack, 2004) is a part of the Delis–Kaplan
Executive Function System Test to measure the ability to inhibit an automatic verbal response, which typically occurs
in patients with prefrontal cortex damage. It is significantly different from previous versions of the Stroop Test
because of the introduction of a new “inhibition and switching” section. T-scores were used in the analysis.
• Mayer–Salovey–Caruso Emotional Intelligence Test (MSCEIT v.2.0), Russian adaptation (Mayer, Salovey &
Caruso, 2002; Sergienko & Vetrova, 2009). Mayer and Salovey (Mayer & Salovey, 1997; Salovey & Mayer, 1990)
model emotional intelligence as a set of skills to evaluate, express and regulate one’s emotions. The evaluation of
one’s emotions is divided into verbal and non-verbal subcomponents, while the assessment of others’ emotions in-
cludes non-verbal perception and empathy. A later edition of their model (Mayer et al., 2002, 2003) includes four do-
mains which develop in ontogenesis: the perception and identification of emotions (Sections A and E), the use of
emotions for thinking facilitation (B and F), the understanding and analysis of emotions (C and G), and conscious
emotional control and regulation for personal growth and the improvement of interpersonal communication (D and H).
Our participants were asked to complete Sections A, B, E, F, but because of fatigue, complexity of the task (imagine a
situation and evaluate a role of imaginary emotion) and duration of the study not all patients completed Sections B
O. Zinchenko, E. Enikolopova / Archives of Clinical Neuropsychology 32 (2017); 1026–1036 1029
Table 1. (continued)
Age Gender Years of Hemisphere Tumor type and localization Group Time when tumor was
(1-male, schooling diagnosed (months
2- female) (university before operation and
education) current study)
15 22 2 3 — — Control —
16 18 2 1 — — Control —
17 31 1 5 — — Control —
18 48 2 5 — — Control —
19 45 2 5 — — Control —
20 27 1 5 — — Control —
21 33 1 5 — — Control —
M(SD) 29.86(11.70) 1.43(0.51) 3.95(1.36)
Statistical Analyses
The normality of data distribution within groups was assessed with Shapiro–Wilk criteria because of small sample size. In
spite of the small sample size, the data was normally distributed. All variables included in the analysis were derived from nor-
mally distributed populations (all ps > .05).
Parameters related to IGT performance (total score, performance per block and deck preferences) were analyzed through
MANOVA with Shidak post-hoc test for multiple comparisons to access between group differences. Significance was con-
sidered at α = 0.05. The relationships between behavioral measures were analyzed with linear regression analysis. To evaluate
the effect of EI on IGT performance and WCST, a sum of scores from the “perception and identification of emotions” section
(A and E) was used as an independent variable, while total score, performance per block, preference per deck in IGT and
“percentage errors” and “perseverative errors” in WCST were used as the dependent variables. The Pearson correlation was
used while correlation analysis was also implemented. SPPS 22 has been used to analyze the data.
Results
The whole set of data included in the analysis (group descriptive statistics, F, p-values, effect size) is presented in Table 2.
Descriptive Statistics
Statistical analyses did not identify significant differences in sociodemographic characteristics between groups (age:
F(1,31) = 0.920, p = .345; education: F(1,31) = 0.641, p = .430; gender: F(1,31) = 1.021, p = .320). The control and clinical
groups did not differ in regards to clinical variables (no comparisons were significant at p < .05).
We also perform descriptive statistics for the subgroup analysis to control there are no differences in subsets of controls
and patients ((age: F(1,18) = 3.074, p = .097, gender: F(1,18) = 0.900, p = .355, years of education (university): F(1,18) =
2.021, p = .173)). The control and clinical groups did not differ in regards to clinical variables (no comparisons were signifi-
cant at p < .05).
The differences in decision-making performance in IGT were firstly assessed by total scores using the formula (C + D) –
(A + B). The performance per block for general decision-making performance was calculated for each 20 trials in all three
groups across the task using the formula (C + D)–(A + B). Also a parameter of preference per deck was calculated for each
deck separately. The MANOVA test was applied with Shidak post-hoc correction (see Table 2 for whole analysis).
O. Zinchenko, E. Enikolopova / Archives of Clinical Neuropsychology 32 (2017); 1026–1036 1031
M SD
Wisconsin Card Sorting Test
Percentage errors 9.476 .004 0.234 1 28.9133 14.97841
2 16.9238 7.49359
Perseverative errors 7.614 .010 0.197 1 18.3550 10.21497
2 11.0171 5.12921
Not perseverative errors 3.779 .061 0.109 1 10.3850 8.56953
2 5.4005 6.11715
Iowa Gambling Task
Selections Deck A 0.801 .378 0.025 1 17.0833 5.55073
A total score. The results of MANOVA indicated a significant difference between healthy controls [M(SD) = 26.8571
(24.67850)] and the clinical group: [M(SD) = 10.3333(14.21480)] (F(1,31) = 4.488, p = .042, partial n2 = 0.126) (see
Table 2).
Performance per block. MANOVA across two groups indicated a significant difference in performance in the block 20–40
(F(1,31) = 4.337; p = .046, partial n2 = 0.123) (see Table 2). This suggest that clinical group in the beginning of the game
shows significantly lower performance than healthy controls (M(SD) = 2.6667(2.99495), M(SD) = 7.0476 (6.8882)).
Preference per deck. Table 2 shows the results of statistical analysis across two groups for their preferences measured as a
number of selections for each deck. This suggests that selections from disadvantageous deck B (F(1,31) = 5.238, p = .029,
partial n2 = 0.145) significantly differ between the clinical group (M(SD) = 27.7500(5.7068)) and healthy controls (M(SD) =
21.3333(8.66795)).
1032 O. Zinchenko, E. Enikolopova / Archives of Clinical Neuropsychology 32 (2017); 1026–1036
Learning curves. Fig. 1 shows repeated-measures ANOVA results across two groups for their performance through five
blocks of IGT. No significant differences were found for clinical group (F(2,141,23,546) = 1.35, p = .289, partial n2 =
0.107). However, the IGT performance through five blocks differed significantly in control group (F(4,80) = 9.748, p = .000,
partial n2 = 0.328). Post-hoc analysis with Shidak correction has been applied. A performance between first and all next
blocks differed significantly (p < .05), while all next comparisons (2–3, 3–4, 4–5) were not significantly different.
MANOVA revealed a significant difference between the clinical group and healthy controls in branches of parameters,
such as Percentage errors (F(1,31) = 9.476, p = .004, partial n2 = 0.234) and perseverative errors (F(1,31) = 7,614, p = .01,
partial n2 = 0.197) (see Table 2). This suggests that participants from the clinical group made more errors then healthy con-
Wisconsin Card Sorting Test and Iowa Gambling Task. To evaluate the possible interaction between the WCST and IGT
parameters, first a correlation analysis with the Pearson correlation was implemented to access the direction and strength of
the relationship between IGT and WCST significantly differed variables between groups (WCST percentage errors and per-
severative errors, selections from Deck B, performance in block 20–40 and overall score in IGT). Second, if any variables ap-
peared to be related, linear regression analysis was implemented to evaluate the percentage of one variable dispersion that
could be predicted by another.
No significance was found in correlation and regression analyses of statistically differed parameters between groups
(WCST Percentage errors and perseverative errors, selections from Deck B, performance in block 20–40 and overall score in
IGT).
D-KEFS Color-Word Interference Test. No significant differences in overall performance and correlations with performance
in the Iowa Gambling Task were observed.
Emotional intelligence. Mayer–Salovey–Caruso Emotional Intelligence Test (MSCEIT v.2.0)—Both groups completed
Sections A and E in MSCEIT, while only 6 out of 12 patients and 14 out of 21 controls completed Sections B and F.
MANOVA revealed no significant differences between subgroup of healthy controls and the clinical group in scores and
frequencies in emotional perception and identification (Sections A and E). There is a significant difference between overall
frequencies in Sections B and F (F(1,18) = 5,508, p = .031, partial n2 = 0.234) between controls (M(SD) = 0.3914(0.04418))
Fig. 1. Learning curves (Iowa Gambling Task) for clinical and control groups.
O. Zinchenko, E. Enikolopova / Archives of Clinical Neuropsychology 32 (2017); 1026–1036 1033
and the clinical group (M(SD) = 0.3133(0.10801)) and overall scores (F(1,18) = 4.440, p = .049, partial n2 = 0.198) between
controls (M(SD) = 6.9286(1.68543)) and the clinical group (M(SD) = 4.500(3.56371)).
Emotional intelligence and performance in the Wisconsin Card Sorting Test—In patients group there is a significant effect of
scores in Sections A and E (beta = –0.661, p = .019, R2-corrected =0.381) on percentage errors in WCST, while there is no
such effect in healthy controls (p = .315).
No other significant effects were found.
Emotional intelligence and performance in the Iowa Gambling Task—No effects of scores in Sections A and E were found
on significantly differed between groups parameters of IGT.
Subgroup analyses. We performed a separate analysis for subjects who completed Sections B and F in MSCEIT to reveal the
possible influence of emotions on the thinking process, as the authors of MSCEIT initially proposed the value for these scales.
A total score. The results of MANOVA indicated a significant difference between healthy controls [M(SD) = 30.2857
(26.6355)] and the clinical group: [M(SD) = 5.3333(15.2665)] (F(1,18) = 4,.531, p = .047, n2 = 0.201)
Performance per block. MANOVA across two groups indicated a significant difference in performance in the block 80–100
(F(1,18) = 5.121; p = .036, n2 = 0.221) between healthy controls [M(SD) = 10.4286(7.7331)] and the clinical group: [M(SD) =
0.666(11.2190)], while a difference between groups in block 20–40 approaches significance (F(1,18) = 3.896; p = .064, n2 =
0.178).
Preference per deck. The selections from disadvantageous deck B (F(1,18) = 5.262, p = .034, n2 = 0.226) significantly differ
between the clinical group (M(SD) = 29.6667(4.6332)) and healthy controls (M(SD) = 20.2143(9.5125)).
Emotional intelligence and performance in the Iowa Gambling Task. A linear regression analysis revealed no interaction/
influence of frequencies converted from overall scores in Sections B and F on selection from deck B in clinical subgroup.
Wisconsin Card Sorting Test performance. There were no significant differences between clinical subgroup and healthy con-
trols in different parameters of WCST.
Emotional intelligence and performance in the Wisconsin Card Sorting Test. A linear regression analysis revealed no influ-
ence of frequencies converted from overall scores in Sections B and F on WCST parameters significantly differed across
groups.
Discussion
The current study assesses decision-making under uncertainty in patients with right dorsolateral prefrontal cortex tumors
compared to healthy controls and revealed the significant impairment in EF and IGT performance and EI in the clinical group.
Moreover, this study sought to replicate the findings of poor performance in IGT in patients with dorsolateral prefrontal cortex
lesions (Manes et al., 2002) because of the contradictory findings of Bechara and colleagues (1994; 2000a, 2000b). This pres-
ent study is also the first to obtain data on the Mayer–Salovey–Caruso Emotional Intelligence Test (MSCEIT v.2.0) from a
clinical sample with tumor lesions.
We found that total IGT scores and performance per second block (20–40) differed significantly between the group of pa-
tients with dorsolateral lesions and the control group. According to the learning curves obtained, both control and clinical
groups started to display positive total score from block 2 (20–40). A preference for disadvantageous deck B is more common
in the clinical group compared to the control group. The former results are consistent with previous findings (Cardoso et al.,
2014) obtained for a frontal stroke lesions group. This indicates that patients with dorsolateral prefrontal cortex lesions lose
1034 O. Zinchenko, E. Enikolopova / Archives of Clinical Neuropsychology 32 (2017); 1026–1036
the ability to learn to avoid disadvantageous decks, though nothing could be said about their sensitivity to advantageous
decks. This means that patients prefer immediate large rewards and are not able to evaluate the long-term consequences of
their actions—compare worse outcome in Deck B preferences and better outcome in advantageous decks with a long-term
perspective. A significant difference in IGT performance in block 20–40 also shows that patients choose a disadvantageous
strategy more often at first trials then healthy controls.
Does an impairment of the “cold” component or “hot” component result in such behavior? Brand, Recknor, Grabenhorst,
and Bechara (2007) suggest that two different mechanisms underlie the IGT performance: decisions under uncertainty in the
first trials and decisions under risk in the latter trials. Thus, an impaired “cold” component should have a higher affect on IGT
performance in the first trials and no affect in the latter trials. To address this question, we performed regression analysis to
investigate the possible interaction between EF tests, EI measurements and IGT performance. In the current study, we did not
see any significant interaction with regard to regression analysis between WCST parameters and IGT performance per block,
though we expect that it could be reproducible in larger samples (for instance, n = 97 in the study by Brand and colleagues
Limitations
The main limitation of the neuropsychological methodology used in this study is that we performed all visits in Russian
and measures were then translated. Here we present preliminary results of the influence of emotional intelligence on some
O. Zinchenko, E. Enikolopova / Archives of Clinical Neuropsychology 32 (2017); 1026–1036 1035
parameters of cognitive tests, especially Sections B and F of MSCEIT. We expect that the latter will be confirmed with
increasing sample size. Since T-scores were used in the analysis of the D-KEFS Color-Word Interference Test, we expect cul-
tural differences in the normative sample compared to the study sample to be an additional limitation of the study. However,
patients were not tested specifically to evaluate mood/emotional status and it could be a confounding variable as only patients
who voluntarily agreed to participate and were neutral were asked to take part in the study. Despite the small sample size,
which could be a limitation, we checked for group differences to be sure that the main and subgroup analysis were statistically
correct. Moreover, neither the main groups nor subgroups differ for any sociodemographic variable.
Funding
During the data analysis and writing of this paper OZ was supported by the Russian Academic Excellence Project “5-100”.
Acknowledgments
The authors gratefully acknowledge Dr Sveltana Buklina, MD, PhD for supervision of the current work during data collec-
tion and observation.
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