In the present study we performed a complete neurological and psychiatric evaluation of a cohort of patients with epilepsy who were admitted to the VEEG monitoring unit and compared the psychiatric profile and the impulsivity levels in two sub groups of patients with clearly defined temporal lobe (ELT) and extratemporal lobe (ETE) resistant epilepsy. Both groups of patients with TLE and ETE group presented significantly higher impulsivity values compared to the control group. As well higher values of impulsivity were found in ETE group when were compared with TLE group, no significant differences were found when the control group was incorporated to the analysis. However, patients with ETE presented a tendency but not significant to have a higher impulsivity in the motor factor (p = 0.05) compared to TLE.
In this study we used the most cited instrument to measure impulsivity, which has been developed by Ernest S. Barratt (1925–2005). Barratt have been worked on this scale during more than 40 and defined impulsivity as the predisposition to rapid and unexpected reactions to internal or external stimuli without regard to the negative consequences of these reactions [25]. Similar to our results, other authors [26] studied temporal lobe epilepsy (TLE) and frontal lobe epilepsy (FLE) patients, using Iowa Gamble Game test, and found that both patients with ELT and FLE were more impulsive than controls, with no significant differences between them [26]. Other studies were reported among patients with juvenile myoclonic epilepsy [12, 27, 28]. These studies showed that these patients have higher impulsivity scores [12, 27, 28]. Indeed, an overlap in prefrontal, striatal, and limbic networks involved in both JME and impulse control has been proposed to explain these findings [27]. Recently, other study showed higher impulsivity levels among patients with generalized epilepsy and in patients with frontal lobe epilepsy, similar to our results. However, they found the contrary among TLE patients[29]. Nevertheless, in our study we included patients with drug-resistant epilepsy, who are specially associated with comorbid psychiatric disorders and impulsivity.
Our results also coincide with previous researchers that reported an exacerbation of impulsivity in patients who suffered traumatic brain lesions [30–33]. Frontal lobe regions compromise, particularly orbital and left ventrolateral lesions have been classically related to higher impulsivity and engaging in risk-taking behaviors [31]. Such risk behaviors have also been described in patients with frontal lobe epilepsies, and could be due to the alteration in the normal functioning of frontal structures due to the epileptogenic network [34]. It has been postulated that prefrontal cortex areas can act as a brake on impulsive tendencies, exerting inhibitory control over subcortical structures and favoring optimal decision-making, while striatal structures without such adequate braking would stimulate the occurrence of impulsive behaviors [35]. This hypothesis is known as the "brake-and-throttle", consider also the temporal function and suggest that the frontal lobe could be regulated in turn by temporal structures, which would add a hierarchically superior instance in the control of impulsive behavior [36]. Indeed, it can explain why we also found higher impulsivity in both groups of patients with temporal and extratemporal epilepsy (most of them were frontal lobe epilepsies). In both frontal and temporal lobe epilepsies, the frontal-hippocampal networks are involved in the epileptogenic zone and/or in the propagation zone of the epileptic discharges [37]. It has been postulated that temporal structures could exert a regulatory function on frontal structures and in turn on subcortical structures to control impulsive behavior. These structures (frontal lobe and temporal lobe) are highly connected through the uncinate fasciculus, which unites the orbitofrontal lobe with the anterior temporal lobe [38, 39].
As expected, we found that the most frequent psychiatric comorbidity was depression in both groups of patients. It was followed by anxiety disorders and psychosis. This is in line with the international literature [17, 40, 41]. Similarly, to our findings other researchers endorsed significantly more depressive symptoms in both ELT and ELF groups, than in the control group without epilepsy [42]. The high prevalence of depression in both TLE and ETE has been related to the high epileptic activity in the temporal lobe, which may have distal effects on the frontal lobe and vice versa [43].
Regarding TLE group analysis, we observed that greater impulsivity was associated with psychiatric disorders and with comorbid depression. The importance of depression in TLE patients has emerged in the last years and the ILAE (International League Against Epilepsy) recognize depression as a main comorbid disorder in patients with epilepsy [44]. A bidirectional relationship between depression and TLE has been postulated [8], mainly based on epidemiological [7] experimental studies [8] and histopathological studies [9]. It is estimated that 30–50% of epilepsy patients suffer from comorbid depression at some point during life. It has been described that epilepsy may favor the development of depression by activating pathophysiological mechanisms associated with stress [45, 46], but depression can also may favor the development of epilepsy (a positive history of depression was associated with an increased risk of developing epilepsy)[7]. Particularly in TLE, hippocampal involvement has been linked to an increased risk of depression [8]. Epilepsy would act synergistically increasing the susceptibility of the hippocampus to stressors that favor a state of increased vulnerability and risk of depression [47]. It has been postulated that epileptic discharges could affect neurobiological pathogenic mechanisms of depressive disorders, and in turn depressive disorders, which have been associated with lower GABAergic activity and higher glutamatergic activity in the brain, could potentiate cortical hyperexcitability and/or facilitate the development of treatment-resistant epilepsy [48]. In 2012, Butler et al. [49] described different neuroanatomical substrates for depression with and without temporal lobe epilepsy and suggested an important role for the orbitofrontal cortex (OFC) (a limbic region that exerts a fundamental role in emotional processing and is strongly interconnected with medial temporal structures). In the group of patients without TLE, higher levels of depressive symptoms were associated with thinning of the left lateral orbito frontal cortex, somewhat opposite to what was found in patients with TLE [49]. Limbic areas usually affected in TLE such as the amygdala, and the hippocampus, are involved in social behaviors, including impulse control, anxiety, and emotional memory [3]. In addition, the temporal pole (TP) which has been considered a paralimbic region may be affected in TLE. Furthermore, the association between depression and impulsivity has been previously described by several authors, who have established a direct relationship between both manifestations in patients with psychiatric disorders [3, 50–53]. This relationship could help to interpret the existing link between temporal lobe, depression, and impulsivity [4].
In relation to EZ laterality, in this study a left laterality of the epileptogenic zone in the ELT group, was associated with higher impulsivity scores on the motor factor. These results contrast with one of the few studies about impulsivity and epilepsy and laterality, the study of McIntyre et al. in 1973 [54], in which it was found that adult patients with right-sided lesions were more impulsive. Although, these authors measured impulsivity with a different instrument (the familiar figure test). On the contrary, other previous studies using VBM in psychiatric patients with impulsivity found that a lower left lateral orbito frontal cortex volume was associated with greater attention impulsivity. Also, a lower volume in the left superior temporal gyrus was associated with greater impulsivity [55]. Also in this line, orbital and left ventrolateral lesions have been associated with increased risk behaviors in the general population and in patients with psychiatric disorders [31, 56–62]. However, there is only very few information in the literature about epilepsy clinical variables and impulsivity.