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Distinct domains of impulsivity are impaired in juvenile myoclonic epilepsy but not in temporal lobe epilepsy
Epilepsy & Behavior 45 (2015) 44–48
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Distinct domains of impulsivity are impaired in juvenile myoclonic epilepsy but not in temporal lobe epilepsy Patricia Rzezak a,b,c,⁎, Sylvie P. Moschetta a, Ellen Lima a, Carolina X.L. Castro a, Silvia Vincentiis a,b,c, Ana Carolina Coan d, Carlos Guerreiro d, Geraldo Busatto Filho b,c, Kette D. Valente a,b,c a
Group for the Study of Cognitive and Psychiatric Disorders in Epilepsy, Clinics Hospital, University of Sao Paulo (USP), Brazil Laboratory of Neuroimaging in Psychiatry, Clinics Hospital, University of Sao Paulo (USP), Brazil Center for Interdisciplinary Research on Applied Neurosciences (NAPNA), University of Sao Paulo (USP), Brazil d Department of Neurology, University of Campinas (UNICAMP), Brazil b c
a r t i c l e
i n f o
Article history: Received 6 November 2014 Revised 6 January 2015 Accepted 21 February 2015 Available online xxxx Keywords: Juvenile myoclonic epilepsy Temporal lobe epilepsy Impulsivity Barratt Impulsiveness Scale
a b s t r a c t Objective: The Barratt Impulsiveness Scale (BIS-11) is the most widely used questionnaire to study impulsivity in persons with psychiatric disorders, but it has rarely been applied to persons with epilepsy. The present study aimed to evaluate the usefulness of BIS-11 as a tool to explore impulsivity in two distinct epilepsy syndromes. Method: The BIS-11 was applied to 20 patients with juvenile myoclonic epilepsy (JME) (32.5 ± 8.95 years old), 20 patients with temporal lobe epilepsy (TLE) (37.7 ± 13.25 years old), and 26 healthy controls (31.86 ± 11.25 years old). The scores in motor, attentional, and lack of planning impulsivity were compared between groups. Results: Patients with JME showed higher scores than patients with TLE and controls in all domains: motor (JME vs TLE: 28.60 vs 13.25 (mean score), p b 0.001 and JME vs controls: 28.60 vs 14.12, p b 0.001), attentional (JME vs TLE: 21.55 vs 13.45, p b 0.001 and JME vs controls: 21.55 vs 14.88, p b 0.001) and nonplanning (JME vs TLE: 28.05 vs 13.10, p b 0.001 and JME vs controls: 28.05 vs 16.15, p b 0.001). Conclusion: Higher BIS-11 scores in all domains of impulsivity [i.e., motor, attentional, and lack of planning] corroborated previous findings described in patients with JME. On the other hand, BIS-11 could not demonstrate problem solving and inhibitory control deficits related to impulsive behavior, which were described in patients with TLE. Other behavioral measures may be more sensitive to some aspects of impulsivity in TLE. Our results reinforce the concept that distinct epileptic syndromes require different neuropsychological approaches, especially considering a complex construct such as impulsivity. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Impulsivity is a multifaceted construct that can be defined as “a predisposition towards rapid, unplanned reactions to internal or external stimuli [with diminished] regard to the negative consequences of these reactions to the impulsive individuals or others” [1,2]. Impulsivity can be assessed by self-report questionnaires and behavioral measures that assess specific dimensions of impulsivity related to three general areas: planning, attention, and motor responding [3–5]. These dimensions are informative in fractionating impulsivity and appear to be important clinically since each impulsive dimension is differentially related to psychiatric illnesses [5]. Behavioral tasks have been designed to capture these elements of impulsivity, largely consisting of decision-making and response inhibition tasks, and impairments in ⁎ Corresponding author at: Laboratorio de Neurofisiologia, Instituto de Psiquiatria, Hospital das Clinicas da FMUSP, Rua Ovidio Pires de Campos S/N, Cerqueira Cesar, 05403-010, Sao Paulo, Brazil. Tel.: +55 11 2661 8132; fax: +55 11 26618193. E-mail address: [email protected] (P. Rzezak).
http://dx.doi.org/10.1016/j.yebeh.2015.02.028 1525-5050/© 2015 Elsevier Inc. All rights reserved.
multiple of those tests may be indicative of higher levels of overall impulsivity. Gomide Vasconcelos et al. [6] demonstrated that distinct assessment methods provide unique information about aspects involved in impulsive behavior due to both the multidimensional nature of impulsivity and method specificities. The Barratt Impulsiveness Scale (BIS-11) [4] is a questionnaire designed to assess the personality/behavioral construct of impulsivity. It is the most widely used instrument for the assessment of impulsivity and has been used to increase understanding about the relationship between impulsivity and other clinical phenomena such as symptoms of psychiatric disorders and personality traits related to impulsive risky behaviors. The BIS-11 is a brief self-reported questionnaire that can easily be used in clinical practice and research studies, and it is applied to evaluate some aspects of impulsivity such as disinhibition, attention deficits, and lack of planning [4,7]. Although extensively used in studies of psychiatric disorders, to our knowledge, the BIS-11 has rarely been applied to persons with epilepsy [8].
P. Rzezak et al. / Epilepsy & Behavior 45 (2015) 44–48
Juvenile myoclonic epilepsy (JME) is a genetically determined syndrome with a favorable outcome considering seizure control in approximately 80% of all patients. On the other hand, temporal lobe epilepsy caused by hippocampal sclerosis (TLE-HS) is a refractory form of epilepsy and a common cause of referral for epilepsy surgery centers. Persons with JME tend to display more impulsive behavior [9], and approximately 20% may present cluster B personality disorders with abnormal impulse control [10]. In TLE-HS, depression is the most common psychiatric disorder; however, some aspects of impulsivity have also been reported, such as decision-making and inhibitory control impairments [11,12]. In a previous study, de Oliveira et al. [8] reported that motor impulsivity associated with major depression was associated with suicidal attempts and ideation in patients with TLE, regardless of etiology. To the best of our knowledge, there are no studies evaluating impulsivity with the BIS-11 in patients with JME and in patients with TLE without depression. Distinct epileptic syndromes may demand different neuropsychological approaches, and the old concept of applying the same battery for all patients regardless of the nature of their deficits may lead to extensive and unnecessary evaluations. In this context, we applied the BIS-11 in these two distinct syndromes (JME and TLE-HS) in order to evaluate its usefulness as a tool in each syndrome. 2. Methods 2.1. Participants Patients with JME and with TLE-HS who participated in this study were followed in the Outpatient Epilepsy Clinic in Clinics Hospital — University of São Paulo (USP) and University of Campinas (UNICAMP), Brazil, from 2013 to 2014. Before taking part in this study, all patients and controls signed an informed consent form approved by the local ethics committee. Patients with major psychiatric disorders, prior history of neurosurgery (including epilepsy surgery), drug intoxication, previous or current history of substance abuse, and lack of adherence to treatment were not included in the current study. Besides, patients with an IQ less than 70, obtained through the Block Design and Vocabulary subtests of the Wechsler Adult Intelligence Scale 3rd Edition (WAIS-III), were not included in the study. Patients were interviewed by a psychiatrist using a structured clinical interview (SCID-I/P) [13] for axis I of DSM-IV-TR [14]. Patients with major mood disorders (major depression, bipolar disorder), generalized anxiety disorder, conversive/dissociative disorders, or psychosis were not included in the study. 2.1.1. Patients with juvenile myoclonic epilepsy We prospectively evaluated 20 consecutive adolescent and adult patients with an unequivocal diagnosis of JME, as defined by the International League Against Epilepsy [15] proposal for syndrome classification. Only patients with classic JME were included, since different electroclinical subtypes of JME, such as childhood absence epilepsy persisting and evolving into JME, JME with adolescentonset pyknoleptic absence, and JME with astatic seizures, were excluded. Thirteen patients (65%) were male with a mean age of 32.5 (SD: 8.95, range: 18–51) and a mean length of education of 11.5 years (SD: 3.50). Eleven patients (55%) were seizure-free, and nine (45%) patients had sporadic generalized tonic–clonic (GTC) seizures. Mean age at onset was 13.50 years (SD: 4.43). Mean duration of epilepsy was 18.3 years (SD: 8.88). The estimated IQ of the sample was 98.26 (SD: 9.78). One patient was not taking any drug, eighteen were on monotherapy (17 patients were under sodium valproate and one under topiramate), and one was on polytherapy (sodium valproate and lamotrigine).
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2.1.2. Patients with temporal lobe epilepsy caused by hippocampal sclerosis (TLE-HS) Twenty patients with TLE-HS were evaluated. All patients had refractory TLE-HS and were evaluated before surgical procedure. Patients had an unequivocal diagnosis of TLE-HS according to electroencephalogram (EEG), video-EEG, and magnetic resonance imaging (MRI). Patients with other lesions, such as patients with dual pathology, previous history of stroke, or any other neurological disorder, were excluded from the evaluation. Four patients (20%) were male with a mean age of 37.70 (SD: 13.25, range: 19–56) and a mean length of education of 10.20 years (SD: 3.14). One patient (5%) was seizure-free at the time of clinical evaluation. Six (30%) patients had sporadic GTC seizures. Mean age at onset was 15.11 years (SD: 11.41). Mean duration of epilepsy was 23.22 years (SD: 14.16). The estimated IQ of the sample was 93.35 (SD: 14.74). Two patients were not taking any drug, three were on monotherapy (1 under carbamazepine, 1 under topiramate, and 1 under phenytoin), and eleven were on polytherapy (nine under carbamazepine/ oxcarbazepine with phenobarbital [3 patients], clobazam [3 patients],sodium valproate and clobazam [1 patient], and lamotrigine [2 patients] and two under clobazam, topiramate, and phenobarbital). Clinical data 154 were not available for four patients. 2.1.3. Controls Twenty-six healthy volunteers with no history of neurological or psychiatric disorders were also evaluated. First, controls underwent a neurological interview followed by a physical and neurological examination to exclude probable CNS disorders not diagnosed or referred to by the subjects. Then, controls were interviewed with the Structured Clinical Interview for Diagnostic and Statistical Manual of Mental Disorders (DSM-IV-TR) Axis I Disorders (SCID-I/P) [13] for the assessment of the presence of any psychiatric disorders. Ten subjects (38.5%) were male with a mean age of 31.86 (SD: 11.25, range: 19–55). Mean length of education was 12.82 years (SD: 2.53). 2.2. Instrument The BIS-11 [1] was used to assess self-reported impulsivity. This questionnaire is composed of 30 items measured on a four-point ordinal scale (1 = Rarely/Never, 2 = Occasionally, 3 = Often, 4 = Almost Always/Always). This scale has been translated into Portuguese and adapted for the Brazilian context [16]. Impulsivity is categorized into three subscales: motor impulsivity, attentional impulsivity, and nonplanning impulsivity. In the BIS-11, a higher score is indicative of higher self-reported impulsivity. In the current study, the dependent measures were the sum scores on each of the three subscales and the overall score. 2.3. Statistical analysis Analysis of variance (ANOVA) and chi-square tests were used to compare demographical variables such as age, gender distribution, and years of formal education. Analysis of variance was then applied to compare scores on the three subscales and the total score of the BIS-11. Bonferroni post hoc tests were applied when appropriate, and η2 effect size was calculated for significant results. Pearson correlation was used to verify the possible association between clinical epilepsy variables (i.e., age at onset, epilepsy duration) and BIS-11 scores. To verify the impact of gender on impulsivity in patients with epilepsy, a regression analysis was performed using gender and the interaction of gender and group as independent variables and each of the three impulsivity domains as a dependent variable. All reported probability values are two-tailed with the significance set at p = 0.013 (with Bonferroni correction). A tendency towards significance was adopted when the p-value was until 5 percentiles above 0.013. Stata 12.0 was used for the statistical analyses.
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3. Results
Table 2 Group comparison in BIS-11 subdomains and overall score with gender as a covariate.
The three groups showed similar age (F = 1.80; p = 0.175) and years of formal education (F = 2.08; p = 0.135) but differed for gender distribution (χ2 = 8.48; p = 0.014). Patients with JME and TLE-HS had similar estimated IQ scores (t = 1.22; p = 0.230), age at epilepsy onset (t = 0.34; p = 0.736), and epilepsy duration (t = 1.44; p = 0.159). Sociodemographic and epilepsy clinical variables are presented in Table 1. Differences among groups were observed in all subscales of the BIS-11 — motor impulsivity (F = 56.66; p b 0.001; η2 = 0.61); attentional impulsivity (F = 23.25; p b 0.001; η2 = 0.42); nonplanning impulsivity (F = 39.55; p b 0.001; η2 = 0.51) — and in the overall score (F = 50.69; p b 0.001; η2 = 0.60). Patients with JME showed higher scores on all subscales of the BIS-11 — motor impulsivity (p b 0.001; p b 0.001), attentional impulsivity (p b 0.001; p b 0.001), and nonplanning impulsivity (p b 0.001; p b 0.001) — and in the overall score (p b 0.001; p b 0.001) when compared to patients with TLE-HS and healthy controls, respectively (Table 2). Age at onset and epilepsy duration were not correlated to any BIS-11 impulsivity domains either in patients with JME or in patients with TLE-HS after correction for multiple comparisons (Table 3). Therefore, duration of epilepsy was not related with the presence of impulsivity. An interaction between gender and group was observed in the following: (i) self-reported motor impulsivity, with better performance observed in control men (t = − 2.12; p = 0.038) and women (t = − 3.98; p b 0.001); (ii) nonplanning impulsivity, with control women showing better performance (t = −2.50; p = 0.015); (iii) attentional impulsivity, with better performance observed in control women (t = − 2.23; p = 0.029); and (iv) BIS-11 overall score, with control women presenting better performance (t = −3.34; p = 0.001).
4. Discussion This is the first study, to our knowledge, comparing self-reported impulsivity of patients with distinct and well-defined epilepsy syndromes. Despite the already established validity of the BIS-11 to explore distinct domains of impulsivity, it has rarely been used in patients with epilepsy [8]. In the present study, we demonstrated the usefulness of BIS-11 to describe impulsive behavior in patients with JME. On the other hand, the self-perception of impulsivity of patients with TLE-HS was similar to that of healthy volunteers. Self-reported inventories present pros and cons. According to some authors, measuring impulsivity by self-report questionnaires may present some limitations as this method is dependent on the selfperception of a complex behavior, representing an artificial method of Table 1 Demographical variables of the three evaluated groups. TLE-HS Sociodemographic variables Age 37.70 (13.25) Education 10.20 (3.14) Gender F 16 M 4 Clinical epilepsy variables Age at onset 14.53 (11.37) Epilepsy duration 23.16 (14.48)
JME
Controls
Statistical test
p
31.84 (8.69) 11.50 (3.50)
31.86 (11.25) 13.30 (2.11)
1.80 2.08 8.48
0.175 0.135 0.014⁎
7 13
16 10
13.6 (4.32) 17.6 (9.21)
– –
Motor Nonplanning Attentional BIS-11 total
TLE-HS
JME
Controls
F
p
13.25 (5.13) 13.10 (5.11) 13.45 (5.05) 39.90 (13.28)
28.60 (3.83)a,b 28.05 (5.54)a,b 21.55 (2.80)a,b 78.20 (9.29)a,b
14.12 (5.97) 16.15 (5.05) 14.88 (3.97) 45.58 (13.46)
56.66 39.55 23.25 50.69
b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎
Legend: TLE-HS: temporal lobe epilepsy related to hippocampal sclerosis; JME: juvenile myoclonic epilepsy; BIS-11: Barratt Impulsiveness Scale. Bold emphasis can be taken out as it emphasized statistical differences only. a Patients with JME with a higher score than controls (Bonferroni post hoc: p b 0.001). b Patients with JME with a higher score than patients with TLE-HS (Bonferroni post hoc: p b 0.01). ⁎ Refers to statistical significant differences.
assessment [17]. Besides, this method could be considered not indicative of specific causes of impulsivity like dysfunctional inhibition processes. On the other hand, Kräplin et al. [18] have demonstrated, in pathological gamblers, that self-reported impulsivity scales can tackle specific aspects of impulsivity, which are not addressed in behavioral tasks such as social desirability, self-reflection, and trait impulsivity [2,19,20]. Thus, an impulsivity questionnaire was able to capture broader situational and behavioral aspects that could not be explored with cognitive tests [21,22]. Some authors suggest that self-report questionnaires represent impulsivity as a stable trait, while behavioral tasks are subject to statedependent variations [23]. The BIS-11 was elaborated not only to address impulsivity but also to categorize distinct domains of impulsivity, such as attention (inability to focus attention or concentrate), lack of planning (lack of future orientation or forethought), and motor impulsivity (acting without thinking). In this context, it is possible to delineate profiles related to distinct groups of patients. For instance, patients with binge-eating disorder had higher scores on the motor impulsivity subscale compared to healthy controls but did not differ on the other two subscales [24], patients with obsessive–compulsive behavior showed higher scores than controls in attentional impulsivity [25], and higher scores of motor impulsivity were observed in adolescents with ADHD, while all domains were affected in adolescents with bipolar disorder [26]. In this study, patients with JME showed higher scores in all domains compared to healthy controls and patients with TLE-HS. Patients with TLE-HS did not differ from controls. This is not an unexpected finding since patients with JME have higher impulsive traits and even personality disorders related to impulse control [9,27]. De Araújo Filho et al. [10] and Gélisse et al. [28], using the categorical classification of the DSM, showed that approximately 20% of these patients presented cluster B personality disorders related to impulse control. Moschetta et al. [9], using a personality inventory, showed that persons with JME had higher impulsive traits compared to controls based on higher scores in the Novelty Seeking dimension of the Cloninger's Temperament and Character Inventory.
Table 3 Correlation between epilepsy clinical variables and impulsivity in patients with JME and TLE-HS. TLE-HS
0.34 1.44
0.736 0.159
Legend: TLE-HS: temporal lobe epilepsy related to hippocampal sclerosis; JME: juvenile myoclonic epilepsy; F: female; M: male. Bold emphasis can be taken out as it emphasized statistical differences only. ⁎ Refers to statistical significant differences.
JME
r
p
r
p
Age at onset Motor Nonplanning Attentional
0.06 0.01 −0.13
0.829 0.997 0.605
0.08 0.17 0.52
0.751 0.467 0.019
Epilepsy duration Motor Nonplanning Attentional
−0.03 −0.02 0.05
0.910 0.928 0.858
0.44 0.13 −0.21
0.054 0.591 0.371
Legend: TLE-HS: temporal lobe epilepsy related to hippocampal sclerosis; JME: juvenile myoclonic epilepsy.
P. Rzezak et al. / Epilepsy & Behavior 45 (2015) 44–48
Our data with BIS-11 corroborate previous findings and, at the same time, add valuable information showing that all domains of impulsivity are affected in JME, but higher scores can be observed in the motor and planning subdomains compared to attention. These data corroborate previous findings of executive function impairment in persons with JME. In a previous paper, our group published how attentional deficits are neglected in JME [29]. A very likely reason, based on these results, is that attentional deficits, although present, are not a major complaint in these patients compared to other executive impairments, such as planning and motor inhibition. To the best of our knowledge, this is the first study to address impulsivity with the BIS-11 in patients with JME. Our findings highlights the importance of assessing the trait-related impulsivity aspects in these patients. Impulsive behavior is not a major feature in TLE-HS, and according to the present study, patients do not recognize themselves as impulsive. One alternative interpretation for our findings relates to the fact that patients with TLE-HS may not perceive their impulsivity because of the cognitive deficits that have been widely reported [30–33] and relevant impairment on social functioning, also previously reported reported [34]. Such relative lack of awareness could lead to low scores in selfreported scales such as the BIS-11. This fact could be related to the cumulative neurobiological burden associated with chronic epilepsy and the risk of progressive cognitive impairment already demonstrated in patients with pharmacoresistant epilepsy [35] such as our group with TLE-HS. Our findings on the absence of an association between the performance on the BIS-11 and age at onset or epilepsy duration do not rule out the possibility of an indirect effect of these clinical variables on the cognitive functioning of these patients and thus on the awareness of this subgroup on their behavior. Some antiepileptic drugs may worsen or trigger depressive symptoms, which could compromise our results. However, most of our patients were using mood stabilizers — sodium valproate in JME and carbamazepine/ oxcarbazepine in TLE-HS. The only drug used by our patients with a direct impact on impulsivity is topiramate, frequently used for psychiatric disorders related to impulse control [36]. However, due to the cognitive effects of topiramate, this antiepileptic drug was used only in a few patients. One may pose the question on polytherapy for patients with TLE-HS vs monotherapy for patients with JME. It would be expected that patients with TLE-HS would present worse performance in some subdomains, such as attention. However, patients with JME using monotherapy, usually in low doses, had a poorer performance in all impulsivity subdomains. Our findings suggest that although antiepileptic drugs have always to be considered due to the undeniable cognitive and behavioral effect, impulsivity in JME seems to be related to neurobiological factors, previously demonstrated by neuroimaging studies [27,37]. In this context, BIS-11 may not be as valuable as other more objective measures for this group of patients. Patients with TLE-HS have demonstrated relevant impairments in objective tasks evaluating inhibitory control [12,38] and, as shown more recently, in decision-making tasks [11]. Both domains are related to impulse control considering impulsivity as a multifaceted construct that can be evaluated through a distinct and complementary approach. Therefore, in this group of patients with epilepsy, other instruments may be more useful than BIS-11 in order to determine impulsive behavior. It is well known that epilepsy is not a disease but a condition. Indeed, epilepsy is a complex condition with several syndromes that present different psychiatric disorders and cognitive impairments. The social impact differs and seems to be related with seizure frequency and the type of psychiatric disorders [34,39]. It is relevant to determine how impulsivity can be better addressed in each syndrome. Persons with epilepsy are exposed to impulsivity in different ways. For some, like persons with JME, impulsivity may be represented by unsafe sexual behavior, unnecessary exposure to risky factors (sleep deprivation), nonadherence to antiepileptic drug treatment, and use of alcohol and drugs. On the other hand, suicide is a frequent cause of death in epilepsy
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and especially in persons with TLE-HS. According to de Oliveira et al. [8], in a subset of persons with TLE and major depression, the finding of motor impulsivity, evaluated by BIS-11, was associated with suicide risk and attempts at suicide. However, more sensitive instruments, such as behavioral measures, may be more useful in earlier stages to detect subtle impulsive traits, which is highly desirable. Acknowledgments This work was supported by a grant from the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Foundation for the Support of Research in the State of São Paulo; Grant nos. 12/09025-3 and 13/11361-4) as well as by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Office for the Advancement of Higher Education), and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, National Council for Scientific and Technological Development Grant No. 307262/2011-1). Conflict of interest The authors state that there are no conflicts of interest. References [1] Barratt EN, Patton JH. Impulsivity: cognitive, behavioral and psychophysiological correlates. Hillsdale: Lawrence Erlbaum; 1983. [2] Moeller FG, Barratt ES, Dougherty DM, Schmitz JM, Swann AC. Psychiatric aspects of impulsivity. Am J Psychiatry 2001;158:1783–93. [3] De Wit H. Impulsivity as a determinant and consequence of drug use: a review of underlying processes. Addict Biol 2009;14:22–31. [4] Patton JH, Stanford MS, Barratt ES. Factor structure of the Barratt Impulsiveness Scale. J Clin Psychol 1995;51:768–74. [5] Swann AC, Anderson JC, Dougherty DM, Moeller FG. Measurement of inter-episode impulsivity in bipolar disorder. Psychiatry Res 2001;101:195–7. [6] Gomide Vasconcelos A, Sergeant J, Corrêa H, Mattos P, Malloy-Diniz L. When selfreport diverges from performance: the usage of BIS-11 along with neuropsychological tests. Psychiatry Res 2014;218:236–43. [7] Stanford M, Mathias C, Dougherty D, Lake S, Anderson N, Patton J. Fifty years of the Barratt Impulsiveness Scale: an update and review. Pers Individ Differ 2009;47: 385–95. [8] de Oliveira GN, Kummer A, Salgado JV, Filho GM, David AS, Teixeira AL. Suicidality in temporal lobe epilepsy: measuring the weight of impulsivity and depression. Epilepsy Behav 2011;22:745–9. [9] Moschetta S, Fiore L, Fuentes D, Gois J, Valente K. Personality traits in patients with juvenile myoclonic epilepsy. Epilepsy Behav 2011;21:473–7. [10] De Araújo Filho GM, Pascalicchio TF, Sousa PDS, Lin K, Ferreira Guilhoto LMF, Yacubian EMT. Psychiatric disorders in juvenile myoclonic epilepsy: a controlled study of 100 patients. Epilepsy Behav 2007;10:437–41. [11] Labudda K, Frigge K, Horstmann S, Aengenendt J, Woermann FG, Ebner A, et al. Decision making in patients with temporal lobe epilepsy. Neuropsychologia 2009; 47:50–8. [12] Rzezak P, Fuentes D, Guimarães C a, Thome-Souza S, Kuczynski E, Li LM, et al. Frontal lobe dysfunction in children with temporal lobe epilepsy. Pediatr Neurol 2007;37: 176–85. [13] First MB, Spitzer RL, Miriam G, Williams JBW. Structured Clinical Interview for DSMIV-TR Axis I Disorders, research version, non-patient edition. New York, New York, USA: Biometrics Research, New York State Psychiatric Institute; 2002. [14] American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th. ed. Washington, DC: American Psychiatric Association; 2000. [15] Commission on Classification and Terminology of the International League Against Epilepsy. Proposal for revised classification of epilepsies and epileptic syndromes. Commission on Classification and Terminology of the International League Against Epilepsy. Epilepsia 1989;30:389–99. [16] Malloy-Diniz L, Mattos P, Leite WB, Abreu N, Coutinho G, de Paula JJ, et al. Translation and cultural adaptation of Barratt Impulsiveness Scale (BIS-11) for administration in Brazilian adults. J Bras Psiquiatr 2010;59:99–105. [17] Reynolds B, Penfold RB, Patak M. Dimensions of impulsive behavior in adolescents: laboratory behavioral assessments. Exp Clin Psychopharmacol 2008;16:124–31. [18] Kräplin A, Bühringer G, Oosterlaan J, van den Brink W, Goschke T, Goudriaan AE. Dimensions and disorder specificity of impulsivity in pathological gambling. Addict Behav 2014;39:1646–51. [19] Broos N, Schmaal L, Wiskerke J, Kostelijk L, Lam T, Stoop N, et al. The relationship between impulsive choice and impulsive action: a cross-species translational study. PLoS One 2012;7:e36781. [20] Enticott P, Ogloff J. Elucidation of impulsivity. Aust Psychol 2006;41:3–14. [21] Dick DM, Smith G, Olausson P, Mitchell SH, Leeman RF, O'Malley SS, et al. Understanding the construct of impulsivity and its relationship to alcohol use disorders. Addict Biol 2010;15:217–26.
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Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Distinct domains of impulsivity are impaired in juvenile myoclonic epilepsy but not in temporal lobe epilepsy Patricia Rzezak a,b,c,⁎, Sylvie P. Moschetta a, Ellen Lima a, Carolina X.L. Castro a, Silvia Vincentiis a,b,c, Ana Carolina Coan d, Carlos Guerreiro d, Geraldo Busatto Filho b,c, Kette D. Valente a,b,c a
Group for the Study of Cognitive and Psychiatric Disorders in Epilepsy, Clinics Hospital, University of Sao Paulo (USP), Brazil Laboratory of Neuroimaging in Psychiatry, Clinics Hospital, University of Sao Paulo (USP), Brazil Center for Interdisciplinary Research on Applied Neurosciences (NAPNA), University of Sao Paulo (USP), Brazil d Department of Neurology, University of Campinas (UNICAMP), Brazil b c
a r t i c l e
i n f o
Article history: Received 6 November 2014 Revised 6 January 2015 Accepted 21 February 2015 Available online xxxx Keywords: Juvenile myoclonic epilepsy Temporal lobe epilepsy Impulsivity Barratt Impulsiveness Scale
a b s t r a c t Objective: The Barratt Impulsiveness Scale (BIS-11) is the most widely used questionnaire to study impulsivity in persons with psychiatric disorders, but it has rarely been applied to persons with epilepsy. The present study aimed to evaluate the usefulness of BIS-11 as a tool to explore impulsivity in two distinct epilepsy syndromes. Method: The BIS-11 was applied to 20 patients with juvenile myoclonic epilepsy (JME) (32.5 ± 8.95 years old), 20 patients with temporal lobe epilepsy (TLE) (37.7 ± 13.25 years old), and 26 healthy controls (31.86 ± 11.25 years old). The scores in motor, attentional, and lack of planning impulsivity were compared between groups. Results: Patients with JME showed higher scores than patients with TLE and controls in all domains: motor (JME vs TLE: 28.60 vs 13.25 (mean score), p b 0.001 and JME vs controls: 28.60 vs 14.12, p b 0.001), attentional (JME vs TLE: 21.55 vs 13.45, p b 0.001 and JME vs controls: 21.55 vs 14.88, p b 0.001) and nonplanning (JME vs TLE: 28.05 vs 13.10, p b 0.001 and JME vs controls: 28.05 vs 16.15, p b 0.001). Conclusion: Higher BIS-11 scores in all domains of impulsivity [i.e., motor, attentional, and lack of planning] corroborated previous findings described in patients with JME. On the other hand, BIS-11 could not demonstrate problem solving and inhibitory control deficits related to impulsive behavior, which were described in patients with TLE. Other behavioral measures may be more sensitive to some aspects of impulsivity in TLE. Our results reinforce the concept that distinct epileptic syndromes require different neuropsychological approaches, especially considering a complex construct such as impulsivity. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Impulsivity is a multifaceted construct that can be defined as “a predisposition towards rapid, unplanned reactions to internal or external stimuli [with diminished] regard to the negative consequences of these reactions to the impulsive individuals or others” [1,2]. Impulsivity can be assessed by self-report questionnaires and behavioral measures that assess specific dimensions of impulsivity related to three general areas: planning, attention, and motor responding [3–5]. These dimensions are informative in fractionating impulsivity and appear to be important clinically since each impulsive dimension is differentially related to psychiatric illnesses [5]. Behavioral tasks have been designed to capture these elements of impulsivity, largely consisting of decision-making and response inhibition tasks, and impairments in ⁎ Corresponding author at: Laboratorio de Neurofisiologia, Instituto de Psiquiatria, Hospital das Clinicas da FMUSP, Rua Ovidio Pires de Campos S/N, Cerqueira Cesar, 05403-010, Sao Paulo, Brazil. Tel.: +55 11 2661 8132; fax: +55 11 26618193. E-mail address: [email protected] (P. Rzezak).
http://dx.doi.org/10.1016/j.yebeh.2015.02.028 1525-5050/© 2015 Elsevier Inc. All rights reserved.
multiple of those tests may be indicative of higher levels of overall impulsivity. Gomide Vasconcelos et al. [6] demonstrated that distinct assessment methods provide unique information about aspects involved in impulsive behavior due to both the multidimensional nature of impulsivity and method specificities. The Barratt Impulsiveness Scale (BIS-11) [4] is a questionnaire designed to assess the personality/behavioral construct of impulsivity. It is the most widely used instrument for the assessment of impulsivity and has been used to increase understanding about the relationship between impulsivity and other clinical phenomena such as symptoms of psychiatric disorders and personality traits related to impulsive risky behaviors. The BIS-11 is a brief self-reported questionnaire that can easily be used in clinical practice and research studies, and it is applied to evaluate some aspects of impulsivity such as disinhibition, attention deficits, and lack of planning [4,7]. Although extensively used in studies of psychiatric disorders, to our knowledge, the BIS-11 has rarely been applied to persons with epilepsy [8].
P. Rzezak et al. / Epilepsy & Behavior 45 (2015) 44–48
Juvenile myoclonic epilepsy (JME) is a genetically determined syndrome with a favorable outcome considering seizure control in approximately 80% of all patients. On the other hand, temporal lobe epilepsy caused by hippocampal sclerosis (TLE-HS) is a refractory form of epilepsy and a common cause of referral for epilepsy surgery centers. Persons with JME tend to display more impulsive behavior [9], and approximately 20% may present cluster B personality disorders with abnormal impulse control [10]. In TLE-HS, depression is the most common psychiatric disorder; however, some aspects of impulsivity have also been reported, such as decision-making and inhibitory control impairments [11,12]. In a previous study, de Oliveira et al. [8] reported that motor impulsivity associated with major depression was associated with suicidal attempts and ideation in patients with TLE, regardless of etiology. To the best of our knowledge, there are no studies evaluating impulsivity with the BIS-11 in patients with JME and in patients with TLE without depression. Distinct epileptic syndromes may demand different neuropsychological approaches, and the old concept of applying the same battery for all patients regardless of the nature of their deficits may lead to extensive and unnecessary evaluations. In this context, we applied the BIS-11 in these two distinct syndromes (JME and TLE-HS) in order to evaluate its usefulness as a tool in each syndrome. 2. Methods 2.1. Participants Patients with JME and with TLE-HS who participated in this study were followed in the Outpatient Epilepsy Clinic in Clinics Hospital — University of São Paulo (USP) and University of Campinas (UNICAMP), Brazil, from 2013 to 2014. Before taking part in this study, all patients and controls signed an informed consent form approved by the local ethics committee. Patients with major psychiatric disorders, prior history of neurosurgery (including epilepsy surgery), drug intoxication, previous or current history of substance abuse, and lack of adherence to treatment were not included in the current study. Besides, patients with an IQ less than 70, obtained through the Block Design and Vocabulary subtests of the Wechsler Adult Intelligence Scale 3rd Edition (WAIS-III), were not included in the study. Patients were interviewed by a psychiatrist using a structured clinical interview (SCID-I/P) [13] for axis I of DSM-IV-TR [14]. Patients with major mood disorders (major depression, bipolar disorder), generalized anxiety disorder, conversive/dissociative disorders, or psychosis were not included in the study. 2.1.1. Patients with juvenile myoclonic epilepsy We prospectively evaluated 20 consecutive adolescent and adult patients with an unequivocal diagnosis of JME, as defined by the International League Against Epilepsy [15] proposal for syndrome classification. Only patients with classic JME were included, since different electroclinical subtypes of JME, such as childhood absence epilepsy persisting and evolving into JME, JME with adolescentonset pyknoleptic absence, and JME with astatic seizures, were excluded. Thirteen patients (65%) were male with a mean age of 32.5 (SD: 8.95, range: 18–51) and a mean length of education of 11.5 years (SD: 3.50). Eleven patients (55%) were seizure-free, and nine (45%) patients had sporadic generalized tonic–clonic (GTC) seizures. Mean age at onset was 13.50 years (SD: 4.43). Mean duration of epilepsy was 18.3 years (SD: 8.88). The estimated IQ of the sample was 98.26 (SD: 9.78). One patient was not taking any drug, eighteen were on monotherapy (17 patients were under sodium valproate and one under topiramate), and one was on polytherapy (sodium valproate and lamotrigine).
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2.1.2. Patients with temporal lobe epilepsy caused by hippocampal sclerosis (TLE-HS) Twenty patients with TLE-HS were evaluated. All patients had refractory TLE-HS and were evaluated before surgical procedure. Patients had an unequivocal diagnosis of TLE-HS according to electroencephalogram (EEG), video-EEG, and magnetic resonance imaging (MRI). Patients with other lesions, such as patients with dual pathology, previous history of stroke, or any other neurological disorder, were excluded from the evaluation. Four patients (20%) were male with a mean age of 37.70 (SD: 13.25, range: 19–56) and a mean length of education of 10.20 years (SD: 3.14). One patient (5%) was seizure-free at the time of clinical evaluation. Six (30%) patients had sporadic GTC seizures. Mean age at onset was 15.11 years (SD: 11.41). Mean duration of epilepsy was 23.22 years (SD: 14.16). The estimated IQ of the sample was 93.35 (SD: 14.74). Two patients were not taking any drug, three were on monotherapy (1 under carbamazepine, 1 under topiramate, and 1 under phenytoin), and eleven were on polytherapy (nine under carbamazepine/ oxcarbazepine with phenobarbital [3 patients], clobazam [3 patients],sodium valproate and clobazam [1 patient], and lamotrigine [2 patients] and two under clobazam, topiramate, and phenobarbital). Clinical data 154 were not available for four patients. 2.1.3. Controls Twenty-six healthy volunteers with no history of neurological or psychiatric disorders were also evaluated. First, controls underwent a neurological interview followed by a physical and neurological examination to exclude probable CNS disorders not diagnosed or referred to by the subjects. Then, controls were interviewed with the Structured Clinical Interview for Diagnostic and Statistical Manual of Mental Disorders (DSM-IV-TR) Axis I Disorders (SCID-I/P) [13] for the assessment of the presence of any psychiatric disorders. Ten subjects (38.5%) were male with a mean age of 31.86 (SD: 11.25, range: 19–55). Mean length of education was 12.82 years (SD: 2.53). 2.2. Instrument The BIS-11 [1] was used to assess self-reported impulsivity. This questionnaire is composed of 30 items measured on a four-point ordinal scale (1 = Rarely/Never, 2 = Occasionally, 3 = Often, 4 = Almost Always/Always). This scale has been translated into Portuguese and adapted for the Brazilian context [16]. Impulsivity is categorized into three subscales: motor impulsivity, attentional impulsivity, and nonplanning impulsivity. In the BIS-11, a higher score is indicative of higher self-reported impulsivity. In the current study, the dependent measures were the sum scores on each of the three subscales and the overall score. 2.3. Statistical analysis Analysis of variance (ANOVA) and chi-square tests were used to compare demographical variables such as age, gender distribution, and years of formal education. Analysis of variance was then applied to compare scores on the three subscales and the total score of the BIS-11. Bonferroni post hoc tests were applied when appropriate, and η2 effect size was calculated for significant results. Pearson correlation was used to verify the possible association between clinical epilepsy variables (i.e., age at onset, epilepsy duration) and BIS-11 scores. To verify the impact of gender on impulsivity in patients with epilepsy, a regression analysis was performed using gender and the interaction of gender and group as independent variables and each of the three impulsivity domains as a dependent variable. All reported probability values are two-tailed with the significance set at p = 0.013 (with Bonferroni correction). A tendency towards significance was adopted when the p-value was until 5 percentiles above 0.013. Stata 12.0 was used for the statistical analyses.
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3. Results
Table 2 Group comparison in BIS-11 subdomains and overall score with gender as a covariate.
The three groups showed similar age (F = 1.80; p = 0.175) and years of formal education (F = 2.08; p = 0.135) but differed for gender distribution (χ2 = 8.48; p = 0.014). Patients with JME and TLE-HS had similar estimated IQ scores (t = 1.22; p = 0.230), age at epilepsy onset (t = 0.34; p = 0.736), and epilepsy duration (t = 1.44; p = 0.159). Sociodemographic and epilepsy clinical variables are presented in Table 1. Differences among groups were observed in all subscales of the BIS-11 — motor impulsivity (F = 56.66; p b 0.001; η2 = 0.61); attentional impulsivity (F = 23.25; p b 0.001; η2 = 0.42); nonplanning impulsivity (F = 39.55; p b 0.001; η2 = 0.51) — and in the overall score (F = 50.69; p b 0.001; η2 = 0.60). Patients with JME showed higher scores on all subscales of the BIS-11 — motor impulsivity (p b 0.001; p b 0.001), attentional impulsivity (p b 0.001; p b 0.001), and nonplanning impulsivity (p b 0.001; p b 0.001) — and in the overall score (p b 0.001; p b 0.001) when compared to patients with TLE-HS and healthy controls, respectively (Table 2). Age at onset and epilepsy duration were not correlated to any BIS-11 impulsivity domains either in patients with JME or in patients with TLE-HS after correction for multiple comparisons (Table 3). Therefore, duration of epilepsy was not related with the presence of impulsivity. An interaction between gender and group was observed in the following: (i) self-reported motor impulsivity, with better performance observed in control men (t = − 2.12; p = 0.038) and women (t = − 3.98; p b 0.001); (ii) nonplanning impulsivity, with control women showing better performance (t = −2.50; p = 0.015); (iii) attentional impulsivity, with better performance observed in control women (t = − 2.23; p = 0.029); and (iv) BIS-11 overall score, with control women presenting better performance (t = −3.34; p = 0.001).
4. Discussion This is the first study, to our knowledge, comparing self-reported impulsivity of patients with distinct and well-defined epilepsy syndromes. Despite the already established validity of the BIS-11 to explore distinct domains of impulsivity, it has rarely been used in patients with epilepsy [8]. In the present study, we demonstrated the usefulness of BIS-11 to describe impulsive behavior in patients with JME. On the other hand, the self-perception of impulsivity of patients with TLE-HS was similar to that of healthy volunteers. Self-reported inventories present pros and cons. According to some authors, measuring impulsivity by self-report questionnaires may present some limitations as this method is dependent on the selfperception of a complex behavior, representing an artificial method of Table 1 Demographical variables of the three evaluated groups. TLE-HS Sociodemographic variables Age 37.70 (13.25) Education 10.20 (3.14) Gender F 16 M 4 Clinical epilepsy variables Age at onset 14.53 (11.37) Epilepsy duration 23.16 (14.48)
JME
Controls
Statistical test
p
31.84 (8.69) 11.50 (3.50)
31.86 (11.25) 13.30 (2.11)
1.80 2.08 8.48
0.175 0.135 0.014⁎
7 13
16 10
13.6 (4.32) 17.6 (9.21)
– –
Motor Nonplanning Attentional BIS-11 total
TLE-HS
JME
Controls
F
p
13.25 (5.13) 13.10 (5.11) 13.45 (5.05) 39.90 (13.28)
28.60 (3.83)a,b 28.05 (5.54)a,b 21.55 (2.80)a,b 78.20 (9.29)a,b
14.12 (5.97) 16.15 (5.05) 14.88 (3.97) 45.58 (13.46)
56.66 39.55 23.25 50.69
b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎
Legend: TLE-HS: temporal lobe epilepsy related to hippocampal sclerosis; JME: juvenile myoclonic epilepsy; BIS-11: Barratt Impulsiveness Scale. Bold emphasis can be taken out as it emphasized statistical differences only. a Patients with JME with a higher score than controls (Bonferroni post hoc: p b 0.001). b Patients with JME with a higher score than patients with TLE-HS (Bonferroni post hoc: p b 0.01). ⁎ Refers to statistical significant differences.
assessment [17]. Besides, this method could be considered not indicative of specific causes of impulsivity like dysfunctional inhibition processes. On the other hand, Kräplin et al. [18] have demonstrated, in pathological gamblers, that self-reported impulsivity scales can tackle specific aspects of impulsivity, which are not addressed in behavioral tasks such as social desirability, self-reflection, and trait impulsivity [2,19,20]. Thus, an impulsivity questionnaire was able to capture broader situational and behavioral aspects that could not be explored with cognitive tests [21,22]. Some authors suggest that self-report questionnaires represent impulsivity as a stable trait, while behavioral tasks are subject to statedependent variations [23]. The BIS-11 was elaborated not only to address impulsivity but also to categorize distinct domains of impulsivity, such as attention (inability to focus attention or concentrate), lack of planning (lack of future orientation or forethought), and motor impulsivity (acting without thinking). In this context, it is possible to delineate profiles related to distinct groups of patients. For instance, patients with binge-eating disorder had higher scores on the motor impulsivity subscale compared to healthy controls but did not differ on the other two subscales [24], patients with obsessive–compulsive behavior showed higher scores than controls in attentional impulsivity [25], and higher scores of motor impulsivity were observed in adolescents with ADHD, while all domains were affected in adolescents with bipolar disorder [26]. In this study, patients with JME showed higher scores in all domains compared to healthy controls and patients with TLE-HS. Patients with TLE-HS did not differ from controls. This is not an unexpected finding since patients with JME have higher impulsive traits and even personality disorders related to impulse control [9,27]. De Araújo Filho et al. [10] and Gélisse et al. [28], using the categorical classification of the DSM, showed that approximately 20% of these patients presented cluster B personality disorders related to impulse control. Moschetta et al. [9], using a personality inventory, showed that persons with JME had higher impulsive traits compared to controls based on higher scores in the Novelty Seeking dimension of the Cloninger's Temperament and Character Inventory.
Table 3 Correlation between epilepsy clinical variables and impulsivity in patients with JME and TLE-HS. TLE-HS
0.34 1.44
0.736 0.159
Legend: TLE-HS: temporal lobe epilepsy related to hippocampal sclerosis; JME: juvenile myoclonic epilepsy; F: female; M: male. Bold emphasis can be taken out as it emphasized statistical differences only. ⁎ Refers to statistical significant differences.
JME
r
p
r
p
Age at onset Motor Nonplanning Attentional
0.06 0.01 −0.13
0.829 0.997 0.605
0.08 0.17 0.52
0.751 0.467 0.019
Epilepsy duration Motor Nonplanning Attentional
−0.03 −0.02 0.05
0.910 0.928 0.858
0.44 0.13 −0.21
0.054 0.591 0.371
Legend: TLE-HS: temporal lobe epilepsy related to hippocampal sclerosis; JME: juvenile myoclonic epilepsy.
P. Rzezak et al. / Epilepsy & Behavior 45 (2015) 44–48
Our data with BIS-11 corroborate previous findings and, at the same time, add valuable information showing that all domains of impulsivity are affected in JME, but higher scores can be observed in the motor and planning subdomains compared to attention. These data corroborate previous findings of executive function impairment in persons with JME. In a previous paper, our group published how attentional deficits are neglected in JME [29]. A very likely reason, based on these results, is that attentional deficits, although present, are not a major complaint in these patients compared to other executive impairments, such as planning and motor inhibition. To the best of our knowledge, this is the first study to address impulsivity with the BIS-11 in patients with JME. Our findings highlights the importance of assessing the trait-related impulsivity aspects in these patients. Impulsive behavior is not a major feature in TLE-HS, and according to the present study, patients do not recognize themselves as impulsive. One alternative interpretation for our findings relates to the fact that patients with TLE-HS may not perceive their impulsivity because of the cognitive deficits that have been widely reported [30–33] and relevant impairment on social functioning, also previously reported reported [34]. Such relative lack of awareness could lead to low scores in selfreported scales such as the BIS-11. This fact could be related to the cumulative neurobiological burden associated with chronic epilepsy and the risk of progressive cognitive impairment already demonstrated in patients with pharmacoresistant epilepsy [35] such as our group with TLE-HS. Our findings on the absence of an association between the performance on the BIS-11 and age at onset or epilepsy duration do not rule out the possibility of an indirect effect of these clinical variables on the cognitive functioning of these patients and thus on the awareness of this subgroup on their behavior. Some antiepileptic drugs may worsen or trigger depressive symptoms, which could compromise our results. However, most of our patients were using mood stabilizers — sodium valproate in JME and carbamazepine/ oxcarbazepine in TLE-HS. The only drug used by our patients with a direct impact on impulsivity is topiramate, frequently used for psychiatric disorders related to impulse control [36]. However, due to the cognitive effects of topiramate, this antiepileptic drug was used only in a few patients. One may pose the question on polytherapy for patients with TLE-HS vs monotherapy for patients with JME. It would be expected that patients with TLE-HS would present worse performance in some subdomains, such as attention. However, patients with JME using monotherapy, usually in low doses, had a poorer performance in all impulsivity subdomains. Our findings suggest that although antiepileptic drugs have always to be considered due to the undeniable cognitive and behavioral effect, impulsivity in JME seems to be related to neurobiological factors, previously demonstrated by neuroimaging studies [27,37]. In this context, BIS-11 may not be as valuable as other more objective measures for this group of patients. Patients with TLE-HS have demonstrated relevant impairments in objective tasks evaluating inhibitory control [12,38] and, as shown more recently, in decision-making tasks [11]. Both domains are related to impulse control considering impulsivity as a multifaceted construct that can be evaluated through a distinct and complementary approach. Therefore, in this group of patients with epilepsy, other instruments may be more useful than BIS-11 in order to determine impulsive behavior. It is well known that epilepsy is not a disease but a condition. Indeed, epilepsy is a complex condition with several syndromes that present different psychiatric disorders and cognitive impairments. The social impact differs and seems to be related with seizure frequency and the type of psychiatric disorders [34,39]. It is relevant to determine how impulsivity can be better addressed in each syndrome. Persons with epilepsy are exposed to impulsivity in different ways. For some, like persons with JME, impulsivity may be represented by unsafe sexual behavior, unnecessary exposure to risky factors (sleep deprivation), nonadherence to antiepileptic drug treatment, and use of alcohol and drugs. On the other hand, suicide is a frequent cause of death in epilepsy
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and especially in persons with TLE-HS. According to de Oliveira et al. [8], in a subset of persons with TLE and major depression, the finding of motor impulsivity, evaluated by BIS-11, was associated with suicide risk and attempts at suicide. However, more sensitive instruments, such as behavioral measures, may be more useful in earlier stages to detect subtle impulsive traits, which is highly desirable. Acknowledgments This work was supported by a grant from the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Foundation for the Support of Research in the State of São Paulo; Grant nos. 12/09025-3 and 13/11361-4) as well as by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Office for the Advancement of Higher Education), and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, National Council for Scientific and Technological Development Grant No. 307262/2011-1). Conflict of interest The authors state that there are no conflicts of interest. References [1] Barratt EN, Patton JH. Impulsivity: cognitive, behavioral and psychophysiological correlates. Hillsdale: Lawrence Erlbaum; 1983. [2] Moeller FG, Barratt ES, Dougherty DM, Schmitz JM, Swann AC. Psychiatric aspects of impulsivity. Am J Psychiatry 2001;158:1783–93. [3] De Wit H. Impulsivity as a determinant and consequence of drug use: a review of underlying processes. Addict Biol 2009;14:22–31. [4] Patton JH, Stanford MS, Barratt ES. Factor structure of the Barratt Impulsiveness Scale. J Clin Psychol 1995;51:768–74. [5] Swann AC, Anderson JC, Dougherty DM, Moeller FG. Measurement of inter-episode impulsivity in bipolar disorder. Psychiatry Res 2001;101:195–7. [6] Gomide Vasconcelos A, Sergeant J, Corrêa H, Mattos P, Malloy-Diniz L. When selfreport diverges from performance: the usage of BIS-11 along with neuropsychological tests. Psychiatry Res 2014;218:236–43. [7] Stanford M, Mathias C, Dougherty D, Lake S, Anderson N, Patton J. Fifty years of the Barratt Impulsiveness Scale: an update and review. Pers Individ Differ 2009;47: 385–95. [8] de Oliveira GN, Kummer A, Salgado JV, Filho GM, David AS, Teixeira AL. Suicidality in temporal lobe epilepsy: measuring the weight of impulsivity and depression. Epilepsy Behav 2011;22:745–9. [9] Moschetta S, Fiore L, Fuentes D, Gois J, Valente K. Personality traits in patients with juvenile myoclonic epilepsy. Epilepsy Behav 2011;21:473–7. [10] De Araújo Filho GM, Pascalicchio TF, Sousa PDS, Lin K, Ferreira Guilhoto LMF, Yacubian EMT. Psychiatric disorders in juvenile myoclonic epilepsy: a controlled study of 100 patients. Epilepsy Behav 2007;10:437–41. [11] Labudda K, Frigge K, Horstmann S, Aengenendt J, Woermann FG, Ebner A, et al. Decision making in patients with temporal lobe epilepsy. Neuropsychologia 2009; 47:50–8. [12] Rzezak P, Fuentes D, Guimarães C a, Thome-Souza S, Kuczynski E, Li LM, et al. Frontal lobe dysfunction in children with temporal lobe epilepsy. Pediatr Neurol 2007;37: 176–85. [13] First MB, Spitzer RL, Miriam G, Williams JBW. Structured Clinical Interview for DSMIV-TR Axis I Disorders, research version, non-patient edition. New York, New York, USA: Biometrics Research, New York State Psychiatric Institute; 2002. [14] American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th. ed. Washington, DC: American Psychiatric Association; 2000. [15] Commission on Classification and Terminology of the International League Against Epilepsy. Proposal for revised classification of epilepsies and epileptic syndromes. Commission on Classification and Terminology of the International League Against Epilepsy. Epilepsia 1989;30:389–99. [16] Malloy-Diniz L, Mattos P, Leite WB, Abreu N, Coutinho G, de Paula JJ, et al. Translation and cultural adaptation of Barratt Impulsiveness Scale (BIS-11) for administration in Brazilian adults. J Bras Psiquiatr 2010;59:99–105. [17] Reynolds B, Penfold RB, Patak M. Dimensions of impulsive behavior in adolescents: laboratory behavioral assessments. Exp Clin Psychopharmacol 2008;16:124–31. [18] Kräplin A, Bühringer G, Oosterlaan J, van den Brink W, Goschke T, Goudriaan AE. Dimensions and disorder specificity of impulsivity in pathological gambling. Addict Behav 2014;39:1646–51. [19] Broos N, Schmaal L, Wiskerke J, Kostelijk L, Lam T, Stoop N, et al. The relationship between impulsive choice and impulsive action: a cross-species translational study. PLoS One 2012;7:e36781. [20] Enticott P, Ogloff J. Elucidation of impulsivity. Aust Psychol 2006;41:3–14. [21] Dick DM, Smith G, Olausson P, Mitchell SH, Leeman RF, O'Malley SS, et al. Understanding the construct of impulsivity and its relationship to alcohol use disorders. Addict Biol 2010;15:217–26.
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