Elsevier

Epilepsy & Behavior

Volume 98, Part A, September 2019, Pages 220-227
Epilepsy & Behavior

Neuroanatomical correlates of personality traits in temporal lobe epilepsy: Findings from the Epilepsy Connectome Project

https://doi.org/10.1016/j.yebeh.2019.07.025Get rights and content

Highlights

  • Individuals with Temporal Lobe Epilepsy (TLE) show higher levels of neuroticism in the NEO-Five Factor Inventory.

  • Higher neuroticism is associated with earlier age of epilepsy onset.

  • Distributed reductions in cortical gray matter volumes were associated with increased neuroticism in TLE.

  • Hippocampal and amygdala volume were negatively associated with neuroticism in TLE.

Abstract

Behavioral and personality disorders in temporal lobe epilepsy (TLE) have been a topic of interest and controversy for decades, with less attention paid to alterations in normal personality structure and traits. In this investigation, core personality traits (the Big 5) and their neurobiological correlates in TLE were explored using the Neuroticism Extraversion Openness-Five Factor Inventory (NEO-FFI) and structural magnetic resonance imaging (MRI) through the Epilepsy Connectome Project (ECP). NEO-FFI scores from 67 individuals with TLE (34.6 ± 9.5 years; 67% women) were compared to 31 healthy controls (32.8 ± 8.9 years; 41% women) to assess differences in the Big 5 traits (agreeableness, openness, conscientiousness, neuroticism, and extraversion). Individuals with TLE showed significantly higher neuroticism, with no significant differences on the other traits. Neural correlates of neuroticism were then determined in participants with TLE including cortical and subcortical volumes. Distributed reductions in cortical gray matter volumes were associated with increased neuroticism. Subcortically, hippocampal and amygdala volumes were negatively associated with neuroticism. These results offer insight into alterations in the Big 5 personality traits in TLE and their brain-related correlates.

Introduction

Temporal lobe epilepsy (TLE) is the most common drug-resistant epilepsy, accounting for 60% of the total 3.4 million people affected by epilepsy in the United States [1]. Structures within the temporal lobes, including the hippocampus and amygdala, have been implicated in anxiety, fear conditioning, and emotional memory [2]. Thus, it is reasonable to expect people with TLE to be at higher risk for affective and psychological comorbidities [3]. Clinically, these comorbidities often remain underdiagnosed and untreated [4] and their underlying etiology often uncertain or controversial [5].

There is a long history of interest in the relationship between epilepsy, personality, and psychopathology. Over the decades, views have ranged from early beliefs that personality “deteriorated” in epilepsy, to one that epilepsy was associated with inherent behavioral abnormalities likely associated with the same underlying “constitutional predispositions” that resulted in the seizures themselves, to one that personality and behavior were no different in epilepsy compared to in the general population [6]. Most influential and long-lasting, however, was the belief that abnormalities in personality and the risk of psychopathology were elevated specifically in those with TLE [7], [8], a view that had enormous influence on the field for decades.

This view of “TLE peculiarity” was reflected in reports that interictal aggression, depression, anxiety, sexual dysfunction, schizophreniform psychoses, and other diagnoses were elevated in TLE and likely attributable to epilepsy-induced dysfunction in mesial temporal and associated limbic structures [6], [9]. A related view was that not only psychopathology, but also a matrix of changes in nonpathological features of personality, affect, and behavior were associated with TLE due to a proposed underlying neurobiological mechanism (i.e., sensory-limbic hyperconnection) [10]. These personality traits could be assessed with specially designed inventories (e.g., Bear–Fedio Inventory) completed by the patient and/or proxies [11]. Using the Bear–Fedio Inventory and related behavioral measures, some studies provided findings supportive of the notion of personality change in TLE [11], [12], [13]. In contrast, numerous studies failed to show specific links to personality change in TLE compared to other epilepsies [14], [15], [16]. The attractiveness of this particular perspective was that TLE might provide a model to unite and understand a host of behavioral anomalies under a common neurobiological mechanism. The theory was of tremendous interest for decades, but ultimately systematic reviews were critical and not supportive of the notion of TLE specificity [17], [18], [19]. Lost in this debate was the pertinence of “normal personality structure”, how it might differ in epilepsy compared to healthy controls, and to what degree any observed differences might be related to features of the epilepsy (e.g., seizure frequency), its social complications (e.g., stigma), or changes in brain structure (e.g., quantitative volumetrics).

Independent of this debate, work progressed to demonstrate the so-called Big 5 personality traits [20] along with procedures for their assessment. The NEO-Personality Inventory (NEO-PI) [21] was developed to assess the core traits that included neuroticism, agreeableness, extraversion, openness, and conscientiousness. A shortened version, the NEO-Five Factor Inventory (NEO-FFI), was subsequently developed. This 60-item questionnaire uses a five-point Likert scale ranging from strongly agree to strongly disagree, and is designed to address the most important general personality traits and their defining factors [20].

The Big 5 personality traits can be defined as follows:

  • Neuroticism: Tendency to experience negative emotions such as anxiety, anger, stress, depression, and moodiness. Neuroticism is related to emotional instability.

  • Openness to experience: Characteristics of interest and willingness to try new ideas, intellectual curiosity, creative, and imaginative.

  • Extraversion: Reflects sociability, talkativeness, and tendency to seek the company of others.

  • Agreeableness: Includes characteristics such as trust, kindness, generousness, interest in helping others, compassion, and cooperation rather than antagonism.

  • Conscientiousness: Encompasses high levels of thoughtfulness, self-discipline, goal-directed behaviors, organization, and preference for planned, rather than spontaneous events.

To our knowledge, only three studies have examined the status of the Big 5 traits in people with epilepsy [17], [22], [23]. Locke and colleagues [22] evaluated differences in NEO-PI scores and the Minnesota Multiphasic Personality Inventory (MMPI) between individuals with TLE and extratemporal epilepsy, and between left and right TLE. No significant differences were observed for any of the pairwise comparisons. Cragar et al. [23] administered the same tests to participants with psychogenic nonepileptic seizures. They observed the following three clusters of personality: (1) very high neuroticism, low extraversion, low openness, high agreeableness, and average conscientiousness; (2) average across all domains; and (3) very high neuroticism, average extraversion, low openness, low agreeableness, and average conscientiousness. The third study by Swinkels and colleagues [17] compared participants with TLE to those with extratemporal epilepsy and found no differences. However, differences in the Big 5 traits between TLE and healthy controls, and their neuroanatomical correlates, have not been examined and are the subject of this investigation.

Lastly, while earlier views of the etiology of personality change in TLE focused predominantly on mesial structures including hippocampus and amygdala, recent studies have demonstrated evidence for structural abnormalities in TLE that extend outside the mesial temporal lobes, both ipsi- and contralaterally. Bilateral cortical thinning has been observed in people with mesial TLE in the frontal, temporal, parietal [24], and occipital regions [25], and in precentral gyrus [26]. A review of voxel-based morphometry (VBM) investigations showed 26 regions to be significantly reduced in volume in TLE, with asymmetrical distribution of temporal lobe abnormalities with preference towards the ipsilateral hemisphere, and bilateral distribution of extratemporal lobe atrophy [27]. Structural abnormalities have also been observed for subcortical extratemporal regions such as bilateral thalamus and the cerebellum [28], and in white matter tracts outside the temporal lobes [29], [30]. It is possible and even likely that structural abnormalities in both temporal and extratemporal regions contribute to the development of personality changes in TLE. To test this, we performed a whole-brain exploratory study of the neural correlates of personality traits.

Specifically, we examined the Big 5 traits in participants from the Epilepsy Connectome Project (ECP), a multisite study dedicated to developing the first large epilepsy connectome database including neuroimaging, cognitive, and behavioral data. We first determined differences in core personality traits between individuals with TLE and healthy controls. In participants with TLE, we then identified neuroanatomical correlates of the significantly different personality trait using quantitative magnetic resonance imaging (MRI).

Section snippets

Participants

The ECP is a multisite research project involving the Medical College of Wisconsin (MCW) and the University of Wisconsin-Madison (UW-Madison). Participants with TLE enrolled in the ECP are between the ages of 18 and 60 (inclusive), demonstrate estimated full-scale IQ (intelligence quotient) at or above 70, speak English fluently, and have no medical contraindications to MRI. Participants have a diagnosis of TLE supported by 2 or more of the following: 1) described or observed clinical semiology

NEO group comparisons

Multivariate analysis of covariance revealed a significant difference between groups for all traits (F = 3.01; p = 0.01; df = 5). Post hoc ANCOVAs to determine differences across each Big 5 trait revealed significantly higher neuroticism (p = 0.002) in TLE. Individuals with TLE also showed lower but not significantly abnormal agreeableness (p = 0.14), conscientiousness (p = 0.08), extraversion (p = 0.22), and openness (p = 0.10) (Fig. 1, Table 2). Supplementary Table 1 presents details of the

Discussion

The core findings from this investigation include the following: 1) there are differences in aspects of normal (Big 5) personality structure identified in people with TLE compared to controls; 2) a link is identified between selected clinical characteristics of the patients' epilepsy and personality; and 3) alterations in aspects of brain structure are associated with core personality traits in TLE. These points will be discussed below.

Acknowledgments

We would like to thank all the participants and their families. Additionally, the authors would like to thank Taylor McMillan for recruitment and participant acquisition, MRI technologists, and other support staff. Funding for healthy control subjects' data acquisition was provided in part by the Department of Radiology, University of Wisconsin-Madison. This study was supported by grant number U01NS093650 from the National Institutes of Health. Research reported in this publication was

References (67)

  • B.P. Hermann et al.

    Mood state in unilateral temporal lobe epilepsy

    Biol Psychiatry

    (1991)
  • J. Stretton et al.

    Frontal lobe function in temporal lobe epilepsy

    Epilepsy Res

    (2012)
  • S.J. Coen et al.

    Neuroticism influences brain activity during the experience of visceral pain

    Gastroenterology

    (2011)
  • M.P. Paulus et al.

    An insular view of anxiety

    Biol Psychiatry

    (2006)
  • G. Gainotti

    Emotional behavior and hemispheric side of the lesion

    Cortex.

    (1972)
  • R. Zack et al.

    National and state estimates of the numbers of adults and children with active epilepsy — United States, 2015

    (2017)
  • V. Rajmohan et al.

    The limbic system

    Indian J Psychiatry

    (2007)
  • L. Kandratavicius et al.

    Pathophysiology of mood disorders in temporal lobe epilepsy

    Rev Bras Psiquiatr

    (2012)
  • L.S. Boylan et al.

    Depression but not seizure frequency predicts quality of life in treatment-resistant epilepsy

    Neurology

    (2004)
  • F.G. Gilliam et al.

    Depression in epilepsy: ignoring clinical expression of neuronal network dysfunction?

    Epilepsia

    (2004)
  • J. Guerrant et al.

    Personality in epilepsy

    (1962)
  • E.L. Gibbs et al.

    Psychomotor epilepsy

    Arch Neurol Psychiatry

    (1948)
  • F.A. Gibbs et al.

    Psychiatric implications of discharging temporal lobe lesions

    Trans Am Neurol Assoc

    (1948)
  • B. Tizard

    The personality of epileptics: a discussion of the evidence

    Psychol Bull

    (1962)
  • D.M. B et al.

    Quantitative analysis of interictal behavior in temporal lobe epilepsy

    Arch Neurol

    (1977)
  • S.G. Waxman et al.

    The interictal behavior syndrome of temporal lobe epilepsy

    Arch Gen Psychiatry

    (1975)
  • N. Geschwind

    Behavioral change in temporal lobe epilepsy

    Arch Neurol

    (1977)
  • E. Rodin et al.

    The Bear-Fedio personality inventory and temporal lobe epilepsy

    Neurology

    (1984)
  • G. Tremont et al.

    Comparison of personality characteristics on the Bear-Fedio inventory between patients with epilepsy and those with non-epileptic seizures

    J Neuropsychiatry Clin Neurosci

    (2012)
  • D. Mungas

    Interictal behavior abnormality in temporal lobe epilepsy. A specific syndrome or nonspecific psychopathology?

    Arch Gen Psychiatry

    (1982)
  • W.A.M. Swinkels et al.

    Interictal depression, anxiety, personality traits, and psychological dissociation in patients with temporal lobe epilepsy (TLE) and extra-TLE

    Epilepsia

    (2006)
  • C. Turnbull et al.

    Epilepsy and personality

  • S.C. Bowden et al.

    Neuropsychological aspects of temporal-lobe epilepsy: seeking evidence-based practice

  • Cited by (13)

    • Personality changes in patients suffering from drug-resistant epilepsy after surgical treatment: a 1-year follow-up study

      2021, Epilepsy Research
      Citation Excerpt :

      Our sample showed that neuroticism was associated with higher HADS scores. The higher the neuroticism is, the more depressive and anxious the patient is; which is in line with many previous studies with both epileptic patients and healthy participants (Rivera Bonet et al., 2019; Lee et al., 2018; Kim et al., 2016; Endermann and Zimmermann, 2009; Wilson et al., 2009). Extraversion and openness to experience personality dimensions were negatively associated with depression scores in our research, which is in line with previous studies with healthy participants (Kim et al., 2016), and with neurologic diseases subjects (Magyar et al., 2017).

    • Personality changes in patients with refractory epilepsy after surgical treatment: A systematic review

      2021, Seizure
      Citation Excerpt :

      According to the current state of the art, personality differences between patients with epilepsy (PWE) and control subjects are usually found to be small and mostly explained by increased anxiety and depression [6–8]. Some authors also indicate higher levels of neuroticism [8,9] and aggression [10] in PWE compared to the general population. Not only the state of disease in general but also the localization of the epileptogenic foci can play a role in the specificity of neuropsychiatric disruptions [11,12].

    • Neuroticism in temporal lobe epilepsy is associated with altered limbic-frontal lobe resting-state functional connectivity

      2020, Epilepsy and Behavior
      Citation Excerpt :

      Furthermore, the studies suggest that functional phenotypes can be used to predict treatment outcomes. Previous research in our group [6] also showed that increasing neuroticism scores were associated with significantly decreased volumes of the left superior/middle frontal cortex, anterior insula, precentral gyrus, lateral parietal–occipital cortex, superior temporal gyrus, precuneus, and fusiform gyrus in individuals with TLE. Here, we demonstrate for the first time that increased neuroticism scores in TLE are associated with patterns of abnormal resting-state connectivity between mesial temporal and frontal regions, some abnormal connections unique to neuroticism and others shared with elevated symptoms of depression and anxiety.

    View all citing articles on Scopus
    1

    These 2 authors are co-Principal authors on this work.

    View full text