Epilepsy & Behavior 60 (2016) 158–164

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Epilepsy & Behavior

journal homepage: www.elsevier.com/locate/yebeh

Decision-making in patients with temporal lobe epilepsy: Delay

gratification ability is not impaired in patients with
hippocampal sclerosis
Patricia Rzezak b,c,d,⁎, Ellen Marise Lima c, Fabricio Pereira b, Ana Carolina Gargaro e, Erica Coimbra e,
Silvia de Vincentiis a,b,c,d, Tonicarlo Rodrigues Velasco e, João Pereira Leite e,
Geraldo F. Busatto b,c, Kette D. Valente a,b,c,d
a
Laboratory of Clinical Neurophysiology,Psychiatry Department,University of São Paulo (USP) School of Medicine,São Paulo, SP, Brazil
b
Laboratory of Neuroimaging in Psychiatry (LIM 21),University of São Paulo (USP) School of Medicine,São Paulo, SP, Brazil
c
Group for the Study of Cognitive and Psychiatric Disorders in Epilepsy — Clinics Hospital,University of Sao Paulo (USP),Brazil
d
Center for Interdisciplinary Research on Applied Neurosciences (NAPNA),University of Sao Paulo (USP),Brazil
e
Ribeirao Preto School of Medicine,Department of Neurosciences and Behavior,University of Sao Paulo (USP),Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Background: Decision-making abilities have rarely been examined in patients with temporal lobe epilepsy related
Received 26 August 2015 to hippocampal sclerosis (TLE-HS). We aimed to investigate the ability to delay gratification, a decision-making
Revised 18 April 2016 subdomain, in patients with intractable TLE-HS and to verify the association of delay gratification performance
Accepted 19 April 2016 and cool executive function tests.
Available online 18 May 2016
Methods: We evaluated 27 patients with TLE-HS (mean age: 35.46 [±13.31] years; 7 males) and their cognitive
performance was compared with that of 27 age- and gender-matched healthy controls (mean age: 35.33
Keywords:
Decision-making
[±12.05] years; 7 males), without epilepsy and psychiatric disorders. Patients were assessed using the delay
Epilepsy discounting task (DDT) and tests of attention, shifting, inhibitory control, and concept formation. Results were
Temporal lobe correlated with clinical epilepsy variables such as age of onset, epilepsy duration, AED use, history of status epi-
Delay discounting lepticus, febrile seizures, and the presence of generalized seizures. Statistical analysis was performed using one-
Executive functions way ANCOVA with years of education as a confounding factor.
Hippocampal sclerosis Results: Patients and controls demonstrated similar performance on DDT, showing similar discount rate (p =
0.935) and probability rate (p = 0.585). Delay gratification was not related to cool executive function tests
(Digit Span, Stroop Color Test, Trail Making Test, Wisconsin Card Sorting Test, and Connors' CPT). History of status
epilepticus, presence of generalized seizures and higher seizure frequency, age at onset, and epilepsy duration
had a significant impact on DDT.
Conclusion: Patients with intractable TLE-HS showed unimpaired delay gratification abilities, being able to accept
a higher delay and a lower amount of chance for receiving a higher reward in the future. Clinical variables related
to the epilepsy severity impacted the performance on delay gratification. Impairment on cool aspects of executive
function was unrelated to this decision-making domain.
© 2016 Elsevier Inc. All rights reserved.

1. Introduction aspects of EF related to planning, cognitive flexibility, and inhibition —

It is well established that patients with temporal lobe epilepsy (TLE)
may present deficits in executive functions (EF). Executive functions is
an umbrella term for several cognitive subfunctions, including working
memory, inhibitory control, decision-making, and task-switching [1]. At
present, most studies in epilepsy have focused on the most traditional
⁎ Corresponding author at: University of São Paulo, Laboratory of Clinical
Neurophysiology, Department of Psychiatry, R. Dr. Ovídio Pires de Campos, 785 - Caixa
Postal 3671, CEP 01060-970 São Paulo, SP, Brazil.
E-mail address: patriciarzezak@gmail.com (P. Rzezak).
the cool domains of EF. The so-called cool EF are often associated with
lateral prefrontal cortex (PFC) and are elicited by relatively abstract,
decontextualized tasks [2–4].
Hot domains of EF are defined as those observed in emotionally and
motivationally significant situations since they involve meaningful, self-
relevant rewards or punishments [5]. One of the most studied hot EF
abilities across neurological and psychiatric disorders is decision-
making. The ventromedial PFC is frequently associated with this ability
[6]. In addition, limbic structures, such as the amygdala, are assumed to
be essential for the generation of an automatic emotional state, which is
implicated in response to a gain/loss in the context of decision-making

http://dx.doi.org/10.1016/j.yebeh.2016.04.042
1525-5050/© 2016 Elsevier Inc. All rights reserved.
 P. Rzezak et al. / Epilepsy & Behavior 60 (2016) 158–164
[7]. Emerging evidence suggests that damage to medial temporal lobes
impairs performance on decision-making tasks when choice is influ-
enced by representations of previous experiences [8,9]. It is reasonable
to believe that medial temporal lobe-based memory functions may be
implicated in the decision-making processes. Nevertheless, these find-
ings are controversial as some studies demonstrated that patients
with amnesia with lesions to the medial temporal lobes had a normal
performance on a decision-making paradigm [10].
The investigation of decision-making abilities in patients with TLE
with lesions located in mesial temporal structures, such as TLE caused
by hippocampal sclerosis (TLE-HS), may corroborate the importance
of these structures to this subdomain of hot EF. Although there might
be an overlap between brain regions that participate in decision-
making and those related to TLE-HS, this cognitive domain has seldom
been investigated in these patients.
It is relevant to have in mind that decision-making is not a unidi-
mensional construct, and the type of decision-making ability can vary
according to the precision and predictability of the knowledge of the
possible outcomes of a decision (i.e., decision under ambiguity [“implic-
it”] and under risk [“explicit”] conditions) or the tendency to discount
future rewards (i.e., delay discounting). Dual-process models of
decision-making suggest that risk-taking decisions can be made by
affective or cognitive controlled systems. The first one is automatic,
effortless, fast, and emotional while the second is deliberative, con-
trolled, slow, neutral, and reflective [11–13]. Different brain regions
are involved in each of these types of decision-making. The neural cor-
relates underlying the affective system are thought to be the amygdala
and the striatum. On the other hand, the ventromedial PFC, dorsolateral
PFC, the anterior cingulate, and the hippocampus are thought to be
implicated in the reflective system [14]. Thus, one may assume that
according to the type of decision-making paradigm, and the system
required to perform this task, different brain regions may be activated.
The reflective system is assumed to have a more pronounced
relationship with cool EF. Brand et al. [15] suggested that cool EF are
important in risk-taking decisions because they are crucial for the cate-
gorization of information and options, the implementation of strategies,
and the integration of feedback.
Delay discounting is a type of decision-making characterized by a
depreciation of the value of a long-term reward with an overvaluation
of a short-term recompense. Therefore, the value of a reward is time-
related, considering the time that this reward takes to be delivered.
Delay discounting is widely used as a measure of impulsiveness. In pa-
tients with impulse control impairment, higher rates of delay
discounting are documented since these subjects prefer to sacrifice
long-term greater rewards in favor of smaller rewards that are available
immediately [16].
Emerging evidence suggests that patients with TLE have worse per-
formance on decision-making tasks in which consequences and their
probabilities are “implicit” (decision-making under ambiguity or
feedback-based decision-making) [17]. In this context, the decision
maker has to initially figure out the options' qualities by processing
feedback of previous decisions [18–21]. On the other hand, patients
with TLE usually show similar performance compared with controls in
tasks of decision-making when information is “explicit” about the po-
tential consequences of different options and their subsequent probabil-
ities [18,19,21]. Therefore, there is some evidence that these patients
may show impairments in some decision-making domains and not in
others [18–21]. To the best of our knowledge, delay gratification abilities
have not been investigated in patients with TLE-HS. Moreover, it is still
not clear whether a delay discounting paradigm, with no feedback of
the consequence of a decision, may be influenced by cool EF impair-
ments in patients with epilepsy. The delay discounting paradigm does
not offer an immediate reward or punishment related to the decisions,
and does not require updating previous choices before deciding be-
tween immediate and delayed gratifications. Thus, we assume that it
is more related to the affective system and may not be influenced by
159
cool EF. Based on the hypothesis that delay gratification may be more
related to the affective system, but not to the reflective system, we
predicted that patients with TLE-HS would show similar performance
when compared with healthy subjects in a delay gratification task, and
that the cool EF performance would not be correlated to delay
discounting performance.
2. Methods
2.1. Participants
Patients with TLE-HS were followed in the Outpatient Epilepsy Clinic
in Clinics' Hospital — University of São Paulo. All subjects signed an in-
formed consent form approved by the local Ethics Committee. Patients
and controls were enrolled in a protocol that included neurological,
psychiatric, and neuropsychological evaluations. In addition, patients
underwent a neurophysiological (including electroencephalogram
[EEG] and video-EEG) and neuroimaging study with 3 Tesla magnetic
resonance imaging (MRI — Intera Achieva, Philips). Epilepsy clinical
information was obtained from the patient and a relevant other in an
interview, close to the time of the neuropsychological assessment.
Patients and controls were interviewed by a psychiatrist, using a
structured clinical interview, the Structured Clinical Interview for
Diagnostic and Statistical Manual of Mental Disorders (DSM-IV-TR)
Axis I Disorders (SCID-I/P) [22] for the assessment of the presence of
any psychiatric disorders. After this evaluation, patients and controls
with major psychiatric disorders (major mood disorders, generalized
anxiety disorder, conversive/dissociative disorders, or psychosis) were
excluded.
Patients with prior history of neurosurgery (including epilepsy
surgery), drug intoxication, previous or current history of substance
abuse, lack of adherence to treatment, and IQ scores lower than 70
(obtained from Block Design and Vocabulary subtests of the Wechsler
Adult Intelligence Scale 3rd Edition — WAIS-III) were not included in
the current study. Finally, patients with other lesions, such as dual pa-
thology, previous history of stroke, or any other neurological disorder
were excluded from this study.
For each selected patient with TLE-HS, an age- and gender-matched
control participant was included. In order to match participants by age,
we considered an age difference between subjects of no more than five
years.
2.1.1. Patients with TLE-HS
Forty-three patients with TLE were enrolled after neurological and
psychiatric evaluation. Four patients with TLE were excluded because
of lack of confirmation of hippocampal sclerosis in 3.0 T MRI, one for in-
complete neuropsychological assessment, and one with an IQ lower
than 70.
Our final sample consisted of 27 patients with TLE-HS who were
candidates with refractory epilepsy. All patients were evaluated before
the surgical procedure. These patients had an unequivocal diagnosis of
TLE-HS according to MRI. The epileptogenic zone was determined by
EEG and long-term inpatient video-EEG for surgical purposes.
This group was composed of twenty females and seven males.
Participants had a mean age of 35.46 years old (SD: 13.31, ranging
from 16 to 58 years old), average length of education of 10.44 years
(SD: 3.02, ranging from 4 to 16 years), and showed mean estimated IQ
(based on Vocabulary and Block Design subtests of WAIS-III) of 93.19
(SD: 13.05, ranging from 74 to 129). Eight patients (29.6%) had a history
of status epilepticus, ten patients (38.1%) had a history of febrile sei-
zures, and three patients (12.5%) were seizure-free at the time of clinical
evaluation. Of the remaining patients, seizure semiologies were as fol-
lows: dyscognitive seizures (seven patients); generalized tonic-clonic
seizures GTC (one patient); autonomic and dyscognitive seizures (five
patients); autonomic, dyscognitive and GTC (five patients); autonomic
and GTC (four patients); and dyscognitive and GTC (one patient).
160 P. Rzezak et al. / Epilepsy & Behavior 60 (2016) 158–164
Mean age at epilepsy onset was 13.52 years (SD: 9.34; ranging from 1 to
40 years). Mean duration of epilepsy was 22.52 years (SD: 13.19; rang-
ing from 3 to 54 years). Seven patients were on monotherapy, and eigh-
teen were on polytherapy. Clinical data were not available for two
patients.
2.1.2. Group of healthy controls
Twenty-seven healthy volunteers with no history of neurological or
psychiatric disorders were also evaluated. Twenty subjects (61.5%)
were female, and seven were male, with a mean age of 35.33 years
(SD: 12.05, ranging from 18 to 55 years). Average length of education
was 13.22 years (SD: 3.07, ranging from 8 to 23 years), and mean esti-
mated IQ was 111.00 (SD: 14.97, ranging from 86 to 138).
2.2. Procedures
2.2.1. Delay discounting task (DDT)
Participants were evaluated with a computerized delay discounting
task (DDT). This task consisted of a series of choices between two possi-
bilities: 1) to earn a certain amount of money immediately or 2) to re-
ceive R$ 1000 after a defined period of time. The amount of money
varied among twenty alternatives (1; 5; 10; 20; 40; 60; 80; 100; 150;
300; 450; 600; 750; 900; 920; 940; 960; 980 or 990 Brazilian Reais)
whereas the period of time had seven delay options (1 day, 1 month,
6 months, 1 year, 5 years, 10 years, or 50 years). Choices were made
within a set of pairwise combinations (amount of money and time
delay variables) that totaled 140 trials.
Participants were also evaluated under the Probability Discounting
Test (PDT). This task is very similar to the previous one, but here, all
trials reward the participant immediately. Subjects have to choose be-
tween earning for sure an amount of money or taking a probability of
gaining R$ 1000. The variable “amount of money” varied identically to
the DDT whereas there were seven alternatives for the “probabilistic
variable” (5%, 10%, 30%, 50%, 70%, 90%, and 95%). Pairwise permutations
(amount of money and probabilistic with both variables) also summed
140 trials.
The delay discounting task was translated to Portuguese, and the
task was implemented according to Rachlin et al. [23]. All data collection
and management software were executed in Matlab Version r2012a
(MathWorks, Natick, Mass). The ranges of delays and cash values tested
have been explored in previous studies [23,24]. The 280 trials of both
discounting tests were presented in a single session in a random
order. The elapsed time to make each choice was not limited, and partic-
ipants were not instructed as to how quickly they should respond.
2.2.2. Executive function tests
The following neuropsychological evaluation was designed to
investigate cool EF of patients with TLE-HS. This protocol was based
on previously published literature in patients with TLE [25–29].
1. Digit Span Forward and Backward [30] — auditory attention (Digit
Forward) and working memory abilities (Digit Backward). The raw
scores of Digit Forward and Backward were used separately.
2. Stroop Color Test [31] — selective attention, mental flexibility, and in-
hibitory control. Only the score (total time) of the last presentation
(Stroop III), which requires higher inhibitory control, was included
in the analyses, as previously done by others [32,33].
3. Trail Making Test [32] — complex visual scanning, visual search speed,
visual attention, mental flexibility, and task-switching. An index score
was obtained by discounting the time to complete Part A from Part B.
In that way, an actual value of task-switching is obtained [32,33].
4. Wisconsin Card Sorting Test [34] — abstract behavior, set-shifting,
response inhibition, and mental flexibility. Here, we considered the
number of categories achieved, the number of perseverative
responses, number of nonperseverative errors, and number of fail-
ures to maintain the set.
5. Connors' CPT [35] — vigilance and inhibitory control abilities.
Numbers of omission and commission errors were used for this test.
2.3. Data analysis
Demographical variables, such as age, years of education, and IQ
scores, were compared between groups using Student t-tests. In relation
to our primary outcome, for each individual, a hyperbolic discount rate
(k, amount of time that the subject accepted to delay his/her gratifica-
tion for receiving a higher reward) and probability rate (h, amount of
chance that the subject agreed to gamble for receiving a higher reward)
were estimated from their choice data in the DDT. Because the k and h
parameters were not normally distributed (Kolmogorov–Smirnov
Z = 1.57; p = 0.015 and Z = 1.23; p = 0.096, for k and h scores in
the patient group, respectively), the distributions of these parameters
were normalized by using the natural log transformation. This proce-
dure was previously used by others in similar studies using this task
[17]. To compare performance on DDT and other executive function
tests, we applied analysis of covariance (ANCOVA), using years of formal
education as a covariate. Our patient group had fewer years of formal
education than controls (t(53) = −3.30; p = 0.002). Education attain-
ment might have an impact in executive function as previously demon-
strated by Cutler et al. [36]. For this reason, education was considered as
a covariate. We used Pearson's correlation coefficient to identify associ-
ations between DDT scores and results of executive functions tests in
patients with TLE-HS. In addition, we explored associations between
the task parameters (log(k) and log(h)), and TLE-HS clinical variables
(i.e., age at onset, epilepsy duration, number of AEDs, presence of gener-
alized seizures, seizure frequency, history of status epilepticus, and his-
tory of febrile seizures) in patients using a series of Student t-tests for
categorical variables and Pearson's correlation analysis for continuous
variables. All reported probability values are two-tailed with the signif-
icance set at p = 0.05. A tendency towards significance was adopted
when the p-value was between 0.050 and 0.100. A conservative thresh-
old of p = 0.001 was used for correlation analysis in order to decrease
the chance of error due to multiple comparisons. The Stata 12.0 was
used for the statistical analyses.
3. Results
3.1. Demographic and clinical characteristics of the sample
Patients with TLE-HS and healthy controls had similar age [t(53) =
1.67; p = 0.102]. On the other hand, patients with TLE-HS had fewer
years of formal education [t(53) = −3.30; p = 0.002] and had lower es-
timated IQ scores [t(53) = − 4.61; p b 0.001] than healthy subjects
(Table 1).
3.2. Performance on delay discounting task
No significant differences between patients with TLE-HS and con-
trols were observed either in the discounting rate (Log (k); F(1,52) =
0.01; p = 0.935) or in the probability rate (Log (h); F(1,52) = 0.31;
p = 0.583) of the delay discounting task (Table 2). To further explore
this lack of differences between groups, the same analysis was done
Table 1
Sociodemographic description of the two samples.
TLE-HS group mean Control group mean t p
(SD) (SD)
Age 35.46 (13.31) 35.33 (12.05) 0.04 0.971
Education 10.44 (3.02) 13.22 (3.07) −3.30 0.002⁎
IQ 93.19 (13.05) 111.00 (14.97) −4.61 b0.001⁎
⁎ Statistical significance at p b 0.05.
 P. Rzezak et al. / Epilepsy & Behavior 60 (2016) 158–164 161

Table 2 3.5. Impact of clinical epilepsy variables on the delay gratification ability
Between-group comparisons in delay gratification and cool executive function tests, using
education as a covariate.
Significant impact of epilepsy variables in DDT scores were observed
TLE-HS group mean Control group mean F p for the following variables: presence of generalized seizures (yes[mean]
(SD) (SD) versus no[mean] on Log DDT probability: −0.17 versus 0.35; t = −2.51;
Log (k) −1.70 (5.91) −1.76 (4.25) 0.00 0.935 p = 0.023), seizure frequency (frequent[mean] versus
Log (h) 1.20 (4.24) 1.44 (3.40) 0.31 0.583 unfrequent[mean] on DDT probability: 0.02 versus 0.07; t = − 2.09;
DDT 0.05 (0.07) 0.03 (0.02) 0.94 0.338
p = 0.057); history of status epilepticus (yes[mean] versus no[mean]
PDT 2.06 (2.30) 1.90 (1.78) 0.01 0.934
Digit Forward 6.58 (2.23) 8.11 (2.08) 2.02 0.162 on Log DDT probability: − 0.12 versus 0.25; t = − 1.89; p = 0.076),
Digit Backward 4.29 (2.18) 6.22 (2.49) 4.34 0.043⁎ and seizure control (yes[mean] versus no[mean] on Log DDT delay:
Stroop Test 38.17 (14.69) 32.23 (42.18) 0.01 0.954 −2.34 versus − 1.68; t = −1.75; p = 0.096). Longer duration of epilep-
TMT 120.96 (107.62) 33.41 (20.90) 8.58 0.005⁎ sy was related to Log of DDT (r = 0.42; p = 0.066) and to DDT probabil-
WCST cat 2.71 (1.85) 2.88 (1.56) 0.13 0.719
WCST PR 19.17 (17.07) 8.85 (8.50) 2.37 0.130
ity (r = 0.46; p = 0.042). Earlier age of onset was related to DDT delay
WCST NPE 14.50 (9.30) 13.22 (7.31) 0.09 0.771 scores (r = 0.041; p = 0.067).
WCST FS 0.54 (0.78) 0.38 (0.70) 0.36 0.554
CPT om 16.10 (19.97) 3.07 (4.66) 6.25 0.016⁎ 4. Discussion
CPT com 14.25 (6.06) 9.19 (5.85) 8.21 0.006⁎

Legend: Log (d): discount rate; Log (h): probabilistic rate; TMT: Trail Making Test; WCST: In the present study, we demonstrated that patients with TLE-HS
Wisconsin Card Sorting Test; WCST cat: number of categories achieved; WCST PR: number have similar performance on an “explicit” decision-making task com-
of perseverative responses; WCST FS: number of failures to maintain set; CPT: Connors'
Continuous Performance Test; CPT om: number of errors of omission; CPT com: number
pared with healthy subjects with neither neurological nor psychiatric
of errors of commission. conditions. To the best of our knowledge, this is the first study to inves-
⁎ Statistical significance at p b 0.05. tigate delay gratification abilities in an etiological homogeneous group
of patients with TLE determined by HS. Despite the lack of hot EF impair-
ments, our patients showed the already described cool EF deficits. As a
without the normalization of DDT. Differences between groups secondary goal, we also demonstrated that cool EF performance is not
remained nonsignificant. related to delay gratification abilities, but some clinical epilepsy
variables may negatively impact the ability to postpone an immediate
reward considering a greater recompense in the future.
3.3. Performance in cool executive function tests Our work is in agreement with previous studies reporting that pa-
tients with TLE have preserved decision-making abilities under risk con-
Patients with TLE-HS showed worse performance on the Digit Back- ditions [18,19,21]. Different tests were used in these studies, and
ward (F(1,52) = 4.24; p = 0.043) and Trail Making Test (F(1,52) = although they were all designed to measure “explicit” decision-making,
8.58; p = 0.005), and made a higher number of omission (F(1,52) = they require different aspects of risk-taking behaviors. Delazer et al. [19]
6.25; p = 0.016) and commission errors (F(1,52) = 3.42; p = 0.006) and Bonatti et al. [21] applied the Probability-Associated Gambling Task
in the Connors' Continuous Performance Test. These findings show a (PAG). In this task, subjects have to choose between a safe small amount
more pronounced impairment in concentration, inhibitory control, of loss/win prize or to take the risk and gamble for a higher gain/loss.
task-switching, mental flexibility, and working memory. No other The chance of winning by gamble is available. Labudda et al. [18], on
significant differences were observed in cool executive function tests the other hand, used the Game of Dice Task (GDT). In this paradigm,
(Table 2). subjects must guess which number will be thrown before a die is rolled.
They can choose between different options associated with a predefined
gain/loss probability, and the rules of the game are explicit. Both tasks
3.4. Correlation between delay gratification scores and cool EF tests deliver a feedback after each trial, and the subject has the possibility
to adjust an ongoing behavior considering the amount of money that
No significant correlation was demonstrated between either the he gained/lost and the probability of a later negative reward.
discounting rate or the probability rate with the cool executive function The DDT is a relatively different task. It is a monetary delay gratifica-
tests in the group of patients with TLE-HS (Table 3). Similar results were tion task that measures individual's preferences between smaller-but-
obtained after replicating this analysis with nonnormalized DDT scores. immediate rewards versus larger-but-postponed or smaller-but-with a
greater probability of success rewards. Subjects are instructed to re-
spond quickly, and no feedback regarding the success of his/her re-
Table 3
Correlation between delay gratification and cool executive function tests in TLE-HS group. sponses is given. It provides an estimate for individual discount and
probability rates, reflecting how rapidly a reward loses subjective
Log (d) Log (h)
value as a function of how long a person must wait to receive it or the
r p r p chance of receiving it [37]. In real life, this ability is related to resisting
Digit Forward 0.08 0.701 0.09 0.675 temptation in favor of long-term goals, which is an important aspect
Digit Backward −0.06 0.768 0.07 0.757 of social competence and economic gain.
Stroop Test −0.11 0.596 −0.05 0.817 Impairment on delay gratification is usually related to impulsive-
TMT 0.14 0.505 −0.19 0.379
ness, and has been widely documented in patients with impulsive con-
WCST cat 0.08 0.704 0.05 0.834
WCST PR 0.29 0.180 0.03 0.880 trol impairment, such as patients with bipolar disorder [38], substance
WCST NPE −0.23 0.284 0.18 0.428 abuse [39], pathological gambling [40], and ADHD [41].
WCST FS 0.32 0.140 0.36 0.102 Differently than GDT and PAG, in DDT, feedback of responses and
CPT om −0.13 0.582 0.05 0.844
amount of money gained/lost are not provided, and subjects do not
CPT com −0.47 0.033 −0.27 0.232
have the opportunity to adjust their behavior accordingly. In the context
Legend: Log (d): discount rate; Log (h): probabilistic rate; TMT: Trail Making Test; WCST: of the dual-system theory of decision-making, it is reasonable to
Wisconsin Card Sorting Test; WCST cat: number of categories achieved; WCST PR: number
of perseverative responses; WCST FS: number of failures to maintain set; CPT: Connors'
suppose that the emotional feedback route is more involved with DDT
Continuous Performance Test; CPT om: number of errors of omission; CPT com: number while the cognitive feedback route is more so used in GDT and PAG. Re-
of errors of commission. sponses in DDT tend to be automatic, effortless, fast, emotional, and
162 P. Rzezak et al. / Epilepsy & Behavior 60 (2016) 158–164
associative while in the other tasks, subjects use information related to
feedback (e.g., amount of money won or lost and what the new overall
capital is) in controlled cognitive processes such as rethinking strategies
and probabilities [13,42,43].
Labudda et al. [18] suggested that patients with TLE show good per-
formance in decision-making under “explicit” conditions because they
can use information about the contingencies of the task to generate,
monitor, and modify advantageous decision-making strategies. We
added to the current literature by demonstrating that patients with
TLE showed similar performance when compared with healthy subjects
not only on tasks that require mostly the reflective system, but also on
those tasks requiring the impulsive system of decision-making under
risk.
Currently, epilepsy is seen as a connectivity disorder. In this context,
there is a consensus that neuropsychological studies need to address
more than memory and language impairments. Patients with TLE-HS
have cognitive deficits that are often related to other brain areas besides
the temporal lobes [26–28,44]. Our study is in agreement with previous
data [4,28,44–46] that demonstrated that adult patients with TLE-HS
show pronounced impairment in some domains of EF represented by
inhibition, shifting, mental flexibility, and working memory — cool EF.
Brand et al. [15] suggest that cool EF are important for decision-
making under risk because they guide the categorization, development,
and application of strategies, and are necessary for the integration of
feedback. Indeed, several studies demonstrated that patients with
executive dysfunction (measured with similar tests as the ones used
in the present study — WCST, Tower of London/Hanoi, Trail Making
Test, Color Word Interference Test) choose more high-risk options
with negative consequences in the GDT, the PAG task, and in the Cam-
bridge Gambling Task [47–50]. The only study that specifically evaluat-
ed the relationship of cool and hot EF in TLE demonstrated a correlation
between cool EF, such as set-shifting, cognitive flexibility, and categori-
zation with GDT [15]. According to these authors, an impaired mental
flexibility and inhibition underlies a worse decision-making behavior
[51].
In our study, cool EF impairments were not related to hot executive
performance. One possible explanation for our different results relies
on the dual-process theory of decision-making. Based on this, some
studies demonstrated that deliberative decision-making usually relies
on cool EF whereas decision-making tasks related to affective processes
have been shown to be relatively independent of cool EF [52].
Delay gratification is related to the ability to postpone an immediate
reward in favor of long-term goals. This ability is usually related to
cognitive control processes [53]. A key component of cognitive control
is the ability to suppress or override competing attentional and behav-
ioral responses (inhibitory control) [54,55]. In this scenario, someone
could expect a positive correlation between DDT scores, Stroop Color
Test, and Conners' CPT commission errors. On the other hand, a number
of strategies, including making choices based on intuition (i.e., a “gut
feeling”) or consideration of economic factors (i.e., interest, inflation)
were reported by subjects evaluated with a delay discounting paradigm
[56]. It is reasonable to believe that these strategies rely on different
cognitive processes, with the second being more related to cool EF. In
an “intuition–strategy” scenario, vigilance and concentration may be
more required than cool EF, which could explain our findings. Neverthe-
less, CPT omission errors were not related to DDT scores, which speak
against the possible explanation that vigilance impairments could influ-
ence DDT scores in patients with TLE-HS. In order to corroborate this as-
sumption, future studies should investigate the strategy used by
patients with TLE-HS to solve DDT.
It is also relevant to discuss the impact of some clinical aspects of
epilepsy severity and worse performance on delay gratification.
Although, we evaluated an etiologically homogeneous group of patients
with TLE-HS, there were within-group differences considering seizure
control and use of AEDs. Patients with early onset epilepsy and worse
seizure severity (seizure frequency and occurrence of GTC seizures)
had a worse performance on DDT. These results may point to the pres-
ence of clinical subgroups with distinct degrees of severity in all aspects,
as already demonstrated in TLE and other syndromes [25,27,57]. The
analysis of a larger sample is indeed necessary in order to establish pre-
dictors of worse performance on cognitive aspects as well as to establish
more suitable interventions for distinct groups.
The importance of mesial temporal lobe damage to decision-making
has been proposed in studies with patients with amnesia. Emerging
evidence suggests that damage to the mesial temporal lobes impairs
performance on decision-making tasks under ambiguity (e.g., Iowa
Gambling Task) [8,9,58], suggesting that memory processes play a role
in shaping decisions. Nevertheless, previous research established that
hippocampal damage does not affect delay discounting performance,
as patients with amnesia with damage to mesial temporal lobes dis-
count the value of delayed rewards similarly to healthy subjects
[10,56]. Our findings of similar DDT performance in patients with TLE-
HS, with lesions to the mesial temporal structures, corroborate the
lack of an association between damage to hippocampus and
surrounding tissue and delay of gratification.
Some strengths of the present study must be emphasized. First, our
patient group was composed of patients with TLE with a well-defined
etiology (restricted to mesial temporal lobe structures), with no current
major psychiatric disorders, and inclusion of presurgical patients solely.
Secondly, our experimental and control groups were closely matched by
gender and age. There is evidence that gender may influence decision-
making abilities in individuals with no current or past neurological or
psychiatric conditions. Although this finding is generally observed
when subjects are under ambiguous risk conditions [59,60], the rela-
tionship of gender and DDT performance has been less studied. Thus,
we decided to be conservative in control group selection and minimize
the chance of gender differences jeopardizing data interpretation.
Besides, age has a well-studied impact in risk-taking abilities. It is sup-
posed to be low in childhood, increase during adolescence and young
adulthood, and decrease again in adults [12]. As our patient sample
was composed of subjects with different age ranges, subtle differences
in DDT performance could be related to the above-mentioned develop-
mental trajectory of decision-making; thus, matching patients with
controls by age range was implemented.
Some limitations of this study should also be considered. Firstly, dif-
ferences in intellectual functioning between patients and controls were
not included in the data analysis. Some studies demonstrated the im-
pact of intelligence on decision-making abilities in people without neu-
rological or psychiatric disorders [61]. In our analysis, we had to choose
between the covariation for IQ scores or years of education, as these two
factors are highly intercorrelated. As lower IQ scores are an underlying
feature of epilepsy [62,63], but lower educational attainment is not,
we chose to correct for the latter. The work of Davis et al. [64], demon-
strated a highly significant effect of education on the IGT. As the level of
education increased, performance to improve more rapidly and reached
a higher eventual positive score. Therefore, education should be used as
a stratification or matching variable in case–control research, using de-
cision-making tests, as stated by the authors. An exploratory analysis
without correcting for education attainment did not show different re-
sults in DDT performance, but showed differences in the cool EF com-
parison between groups. Future studies that investigate the impact of
intelligence on delay gratification abilities in patients with TLE-HS
with different IQ ranges should help to further explore this relationship.
Another aspect that could not be explored in this study is reaction time
differences between groups. Faster response times can be an indication
of a more automatic response. Due to time constraints and considering
that patients usually have a slower reaction time, all pairs of decisions
were read aloud by the examiner, and patients' responses were marked
by her. Studies using a shorter version of DDT, with less pairs of choices,
considering reaction times are warranted to further explore this possi-
ble strategy that might be used by patients with TLE. Finally, although
we examined a homogeneous group of patients with very restrictive
 P. Rzezak et al. / Epilepsy & Behavior 60 (2016) 158–164
inclusion and exclusion criteria, we analyzed a small sample size. One
may pose the question about the impact of some AEDs on impulsive-
ness. Indeed, this may represent another limitation. However, merely
three of our patients were using topiramate, an AED that can decrease
impulsive behavior and therefore potentially have an impact on the
finding of a lack of an association between TLE-HS and “explicit”
decision-making impairment [65].
Decision-making ability, a cognitive process that allows the individ-
ual to compare values between the immediate and delayed consump-
tion of a determined commodity [56], was not impaired in patients
with TLE-HS. These findings allow us to make some assumptions re-
garding risk-taking behaviors of these patients. Despite other cognitive
deficits, these patients are probably able to postpone an immediate
reward in view of a greater reward in the future. In conclusion, our find-
ings corroborate previous data showing that patients with TLE-HS pres-
ent impairments on mental flexibility, inhibition, and complex attention
subdomains, but have decision-making behavior under explicit
situation spared, despite the presence of refractory epilepsy.
Acknowledgments
Dr. Vincentiis received grants from Foundation for Research Support
of the State of São Paulo (FAPESP 13/11361-4). Dr. Rzezak received a
grant from Foundation for Research Support of the State of São Paulo
(FAPESP 12/09025-3; 12/13065-0). Dr. Valente received grants from
the Brazilian Research and Development Council (CNPQ 307262/
2011-1) and Foundation for Research Support of the State of São
Paulo (FAPESP 13/11361-4; 12/09025-3; FAPESP 12/09025-3). Dr.
Busatto received grants from the Foundation for Research Support of
the State of São Paulo (FAPESP 12/09025-3 AND 2012/50329-6). Dr.
Leite received grants from the Brazilian Research and Development
Council (CNPq 476250/2013-7 and 466995/2014).
Conflict of interest
The authors declare no conflicts of interest.
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