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Why epilepsy challenges social life

  • Bettina K. Steiger
    Affiliations
    Swiss Epilepsy Centre, Bleulerstrasse 60, CH-8008 Zurich, Switzerland

    Psychological Institute, University of Zurich, Zurich, Switzerland
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  • Hennric Jokeit
    Correspondence
    Corresponding author at: Swiss Epilepsy Centre, Bleulerstrasse 60, CH-8008 Zurich, Switzerland.
    Affiliations
    Swiss Epilepsy Centre, Bleulerstrasse 60, CH-8008 Zurich, Switzerland

    Neuroscience Center Zurich, Zurich, Switzerland

    Psychological Institute, University of Zurich, Zurich, Switzerland
    Search for articles by this author
Open ArchivePublished:October 09, 2016DOI:https://doi.org/10.1016/j.seizure.2016.09.008

      Highlights

      • People with epilepsy are at risk for reduced social competences and quality of life.
      • Neuropsychological deficits in social cognition may impede social interactions.
      • New diagnostic and therapeutic approaches are needed for better assessment and care.

      Abstract

      Social bonds are at the center of our daily living and are an essential determinant of our quality of life. In people with epilepsy, numerous factors can impede cognitive and affective functions necessary for smooth social interactions. Psychological and psychiatric complications are common in epilepsy and may hinder the processing of social information. In addition, neuropsychological deficits such as slowed processing speed, memory loss or attentional difficulties may interfere with enjoyable reciprocity of social interactions. We consider societal, psychological, and neuropsychological aspects of social life with particular emphasis on socio-cognitive functions in temporal lobe epilepsy. Deficits in emotion recognition and theory of mind, two main aspects of social cognition, are frequently observed in individuals with mesial temporal lobe epilepsy. Results from behavioural studies targeting these functions will be presented with a focus on their relevance for patients’ daily life. Furthermore, we will broach the issue of pitfalls in current diagnostic tools and potential directions for future research. By giving a broad overview of individual and interpersonal determinants of social functioning in epilepsy, we hope to provide a basis for future research to establish social cognition as a key component in the comprehensive assessment and care of those with epilepsy.

      Keywords

      1. Quality of life is social

      If you have close friends and confidants, friendly neighbours and supportive co-workers, you are less likely to experience sadness, loneliness, low self-esteem and problems with drugs, eating or sleeping [
      • Helliwell J.F.
      • Putnam R.D.
      The social context of well-being.
      ]. In fact, this ‘social capital’ has been found to impact positively on health, morbidity and mortality. Quality social networks (i.e. not Facebook) and support have also been found to be of great importance, acting as a buffer against the impacts of stress exposure in mental and physical health conditions [
      • Thoits P.A.
      Mechanisms linking social ties and support to physical and mental health.
      ].
      Many epidemiological studies have revealed that each of the major determinants of quality of life: employment, social interactions, family relationships, and experiential activities, are at considerable risk in patients with epilepsies [
      • Sherman E.M.S.
      Maximizing quality of life in people living with epilepsy.
      ]. Moreover, epilepsy patients apparently have an increased risk of having impaired social cognitive skills and suffering from communication problems and interpersonal difficulties [
      • Broicher S.D.
      • Jokeit H.
      On clinical diagnostics of social cognition in patients with epilepsies.
      ]. Here, we provide an overview of disease-related factors that can influence social functions in epilepsy. We will discuss societal, psychological, and neuropsychological aspects of social life with particular emphasis on socio-cognitive functions in temporal lobe epilepsy.
      Social difficulties in epilepsy are not restricted to adulthood. Already in childhood, children with epilepsy have been found to exhibit lower social competence than children without epilepsy [
      • Russ S.A.
      • Larson K.
      • Halfon N.
      A national profile of childhood epilepsy and seizure disorder.
      ]. Upon reaching adulthood, those who formerly suffered with epilepsy as children, are often found to have very high rates of social problems, even if they are intellectually within the normal range [
      • Camfield C.S.
      • Camfield P.R.
      Long-term social outcomes for children with epilepsy: social outcomes for children with epilepsy.
      ]. Such deficits in social functioning can contribute to difficulties in developing relationships and remaining in employment and thus, participating in life as a member of a family, community and culture [
      • Roder V.
      • Mueller D.R.
      • Schmidt S.J.
      Effectiveness of integrated psychological therapy (IPT) for schizophrenia patients: a research update.
      ], which in turn affects quality of life. Therefore, social functioning should be of paramount consideration when aiming to improve quality of life in epilepsy throughout the lifespan.
      Studies of social functioning in epilepsy have been subject to many major shifts in perspective. More than half a century ago, epilepsy was seriously stigmatised as a disorder that stamps the personality into an ‘epileptic personality’ surrounded by a ‘social abscess’ [
      • Guerrant J.
      • Anderson W.W.
      • Fischer A.
      • Weinstein M.R.
      • Jaros R.M.
      • Deskins A.
      Psychological observations.
      ]. Norman Geschwind was one of the first modern neurologists to develop elaborated neuroscientific concepts to explain the increased prevalence of certain behavioural abnormalities as signs of brain dysfunction.
      However, beginning in the 1970s, the social and psychological turn in psychiatry and related disciplines may have resulted in a tendency to neglect the neurological basis and overrate the social and psychological underpinnings of certain symptoms affecting social competencies. The following decades were characterised by tremendous efforts to de-stigmatise patients with epilepsy and empower them.
      To date, it is unclear to what extent difficulties in social competences arise from psychosocial conditions or underlying deficits caused by epilepsy-related brain lesions. From a psychological perspective, the effects of stigma, role and experience restrictions, the effects of parental overprotectiveness and fear of seizures [
      • Jacoby A.
      • Snape D.
      • Baker G.A.
      Epilepsy and social identity: the stigma of a chronic neurological disorder.
      ] can all impact on social engagement as well as the ability to learn and practice social knowledge and rules. The significantly enhanced prevalence of psychiatric disorders such as depression, anxiety, and psychosis in patients with epilepsy additionally contributes to risk of impaired social relations [
      • Dunn D.W.
      • Austin J.K.
      • Harezlak J.
      ADHD and epilepsy in childhood.
      ].
      Even though psychological factors such as social stigma likely contribute to difficulties in establishing and maintaining interpersonal relationships, people with epilepsy can suffer from impairments in social functioning that cannot be explained by psychological causes alone. Therefore, it is crucial to examine social functioning from multiple perspectives. Although social deficits are not always readily apparent in the majority of patients, signs of poor social amalgamation can permeate all spheres of social life in patients with epilepsy. People with epilepsy are generally found to have fewer social supports compared to those without this condition, are less likely to marry, have fewer children [
      • Jalava M.
      • Sillanpää M.
      Reproductive activity and offspring health of young adults with childhood-onset epilepsy: a controlled study.
      ], have lower rates of employment [
      • Strine T.W.
      • Kobau R.
      • Chapman D.P.
      • Thurman D.J.
      • Price P.
      • Balluz L.S.
      Psychological distress, comorbidities, and health behaviors among U.S. adults with seizures: results from the 2002 National Health Interview Survey.
      ] and cite lack of social engagement and difficulty in developing satisfying interpersonal relationships as common problems [
      • Broicher S.D.
      • Jokeit H.
      On clinical diagnostics of social cognition in patients with epilepsies.
      ,
      • Schmitz B.
      Emotion und soziale Kognition aus epileptologischer Sicht.
      ,
      • Thorbecke R.
      Zur Bedeutung von Defiziten in Emotion und sozialer Kognition für die soziale Integration von Menschen mit Epilepsie.
      ]. Though interpersonal problems surely do not apply to every person with epilepsy, their far-reaching influence on quality of life deserves clinicians’ and researchers’ close attention.

      2. Epilepsy and the social brain

      Taking a traditional neuropsychological perspective, it is plausible that cognitive impairment can give rise to social difficulties. Reductions in information processing speed and capacity may prevent a smooth social encounter irrespective of whether the slowing or limitation in capacity is due to post-ictal impairment, side effects of antiepileptic drugs or an underlying brain lesion. Moreover, attentional and executive deficits including heightened distractability and lowered inhibition may disrupt the fluidity of verbal and non-verbal communication. Having memories in common acts as social glue for couples, family, and close friends and can impel the wish to share future activities together. However, patients with temporal lobe epilepsies in particular frequently suffer from impaired autobiographical memory [
      • McAndrews M.P.
      Remote memory and temporal lobe epilepsy.
      ]. Thus, transient and chronic cognitive impairment in patients with epilepsies itself is a risk factor for poor social integration.
      A contemporary perspective comes from neuroscience and the relatively new area of social cognition, also termed social neurosciences. Social cognition is defined as information processing that contributes to the correct perception and interpretation of affective and mental states, dispositions and intentions of another individual [
      • Brothers L.
      The neural basis of primate social communication.
      ].
      Social cognition encompasses a wide range of functions involved in the processing of social cues. It can be divided into perception and recognition of emotions on the perceptual level, and into more advanced processes of theory of mind (ToM): the inference of mental states, intentions and beliefs of others as well as the prediction of their behaviour based on these mental states [
      • Mitchell R.L.C.
      • Phillips L.H.
      The overlapping relationship between emotion perception and theory of mind.
      ]. Social interactions depend on the efficient processing of social information at the perceptual and at the advanced level in order to ensure smooth communication and a shared understanding of social situations.
      These socio-cognitive functions cannot be linked to one specific brain region, but instead rely on distributed networks [
      • Amft M.
      • Bzdok D.
      • Laird A.R.
      • Fox P.T.
      • Schilbach L.
      • Eickhoff S.B.
      Definition and characterization of an extended social-affective default network.
      ]. Therefore, impairment of socio-cognitive functions can arise from lesions throughout these networks. While deficient processing of socially relevant information can be found in many types of epilepsy [
      • Stewart E.
      • Catroppa C.
      • Lah S.
      Theory of mind in patients with epilepsy: a systematic review and meta-analysis.
      ], temporal lobe epilepsy (TLE) is the most common and most uniform type of epilepsy and will therefore serve as the focus of our overview on social cognition and its putative relevance for patients’ daily lives.

      3. Multimodal recognition of emotion

      Deficits in social cognition in people with TLE can be identified at the basic level of emotion recognition. The face acts as a major source of information in social interactions and provides a wealth of cues for inferences about age, gender, identity, emotions and intentions [
      • Jack R.E.
      • Schyns P.G.
      The human face as a dynamic tool for social communication.
      ]. For this reason, most studies on emotion recognition have applied tasks that target facial emotion recognition (FER). In a recent meta-analysis, Bora and Meletti [
      • Bora E.
      • Meletti S.
      Social cognition in temporal lobe epilepsy: a systematic review and meta-analysis.
      ] analysed FER in adult TLE patients either before or after surgical intervention. In both pre- and postsurgical patients, the recognition of facial expressions was diminished for all six basic emotions (anger, disgust, fear, happiness, sadness, and surprise). The largest effects were found for the recognition of fear, whereas effects for happy and surprised faces were small. At least in cross-sectional studies, FER performance did not differ before and after resection of the mesial temporal lobe. With regard to laterality, poorer FER abilities were found in right-sided TLE for the recognition of fear, disgust, and sadness, whereas no difference was found in anger, surprise and happiness compared to left TLE. Impairments found at the group level were at best medium, with TLE patients obtaining FER scores at most 20% lower than healthy controls [
      • Monti G.
      • Meletti S.
      Emotion recognition in temporal lobe epilepsy: a systematic review.
      ].
      When analysing deficits on an individual level, great inter-individual variability exists among patients, and substantial deficits have been detected in 30 to 50 percent of patients [
      • Bonora A.
      • Benuzzi F.
      • Monti G.
      • Mirandola L.
      • Pugnaghi M.
      • Nichelli P.
      • et al.
      Recognition of emotions from faces and voices in medial temporal lobe epilepsy.
      ,
      • Meletti S.
      • Benuzzi F.
      • Cantalupo G.
      • Rubboli G.
      • Tassinari C.A.
      • Nichelli P.
      Facial emotion recognition impairment in chronic temporal lobe epilepsy.
      ]. While poor FER performance has been observed repeatedly, the influence of clinical variables is still unclear. In their meta-analysis, Bora and Meletti [
      • Bora E.
      • Meletti S.
      Social cognition in temporal lobe epilepsy: a systematic review and meta-analysis.
      ] found no significant association between FER abilities and age at seizure onset or the presence of hippocampal sclerosis. Contrary to this meta-analytic finding, it has been suggested that patients with epilepsy onset at a young age (<5 years) and patients with a long duration of the disease appear to be more heavily impaired in FER [
      • Monti G.
      • Meletti S.
      Emotion recognition in temporal lobe epilepsy: a systematic review.
      ].
      This assumption derived from studies of adult TLE patients was supported by a study examining children between 8 and 16 years of age with either right- or left-sided TLE or fronto-central epilepsy [
      • Golouboff N.
      • Fiori N.
      • Delalande O.
      • Fohlen M.
      • Dellatolas G.
      • Jambaqué I.
      Impaired facial expression recognition in children with temporal lobe epilepsy: impact of early seizure onset on fear recognition.
      ]. Impairments in FER were already present in approximately 25% of the children in all three epilepsy groups. On closer look, groups differed in their recognition performance for specific emotions: TLE children showed difficulties specifically for fear, and impaired recognition of happiness was present in children with fronto-central epilepsy. In children with right-sided TLE, impaired fear recognition was associated with the extent of psychopathological symptoms. Interestingly, half of the children with a history of febrile seizures during infancy displayed substantial FER deficits for fear, whereas only one child without febrile seizures showed borderline fear recognition. These findings indicate that the integrity of mesiotemporal structures is crucial for the development of perceptual socio-cognitive functions. However, the number of studies on the specific influence of disease onset remains small, and longitudinal studies are needed to clearly delineate the developmental course and impairment of FER.
      Furthermore, current research is somewhat limited by the low diversity of stimuli employed in experiments measuring FER. Most studies rely on the presentation and subsequent recognition of static black-and-white photographs of faces, yet these paradigms are only a crude approximation of the processes necessary in daily life interactions. In a more realistic study design, Tanaka et al. [
      • Tanaka A.
      • Akamatsu N.
      • Yamano M.
      • Nakagawa M.
      • Kawamura M.
      • Tsuji S.
      A more realistic approach, using dynamic stimuli, to test facial emotion recognition impairment in temporal lobe epilepsy.
      ] tested FER abilities using short movie clips displaying basic emotions. Consistent with studies using photographs, they found slightly lower recognition rates for TLE patients than healthy participants that were most pronounced for the facial expressions of fear, sadness and disgust. Still, there remains a great need for new, innovative study designs to capture FER in a more naturalistic way. More complex facial expressions such as shame or guilt also have yet to be examined.
      Facial expressions are not only frequently presented in behavioural studies; they are also often used in functional MRI (fMRI) studies exploring the neural response to emotional faces. This paradigm plays a special role in TLE pre-surgical evaluation of amygdala functionality [
      • Schacher M.
      • Haemmerle B.
      • Woermann F.G.
      • Okujava M.
      • Huber D.
      • Grunwald T.
      • et al.
      Amygdala fMRI lateralizes temporal lobe epilepsy.
      ]. Alterations of activity in response to fearful faces have been found for the ipsilateral amygdala [
      • Toller G.
      • Adhimoolam B.
      • Grunwald T.
      • Huppertz H.-J.
      • Kurthen M.
      • Rankin K.P.
      • et al.
      Right mesial temporal lobe epilepsy impairs empathy-related brain responses to dynamic fearful faces.
      ] and also for more widespread occipital, temporal and frontal regions [
      • Labudda K.
      • Mertens M.
      • Steinkroeger C.
      • Bien C.G.
      • Woermann F.G.
      Lesion side matters—an fMRI study on the association between neural correlates of watching dynamic fearful faces and their evaluation in patients with temporal lobe epilepsy.
      ]. Furthermore, activity of the amygdala has been linked to ratings of fear expressed by faces [
      • Labudda K.
      • Mertens M.
      • Steinkroeger C.
      • Bien C.G.
      • Woermann F.G.
      Lesion side matters—an fMRI study on the association between neural correlates of watching dynamic fearful faces and their evaluation in patients with temporal lobe epilepsy.
      ] and empathetic concern in a self-report questionnaire [
      • Toller G.
      • Adhimoolam B.
      • Grunwald T.
      • Huppertz H.-J.
      • Kurthen M.
      • Rankin K.P.
      • et al.
      Right mesial temporal lobe epilepsy impairs empathy-related brain responses to dynamic fearful faces.
      ]. Additional studies are needed to infer the behavioural relevance of these fMRI differences during the processing of emotional faces.
      Emotions can not only be deduced from faces, but also from voices based on prosody or from vocal bursts such as screams, moans or laughter. Although fewer studies have focussed on auditory emotion recognition, deficits have also frequently been reported in TLE [
      • Broicher S.D.
      • Kuchukhidze G.
      • Grunwald T.
      • Krämer G.
      • Kurthen M.
      • Jokeit H.
      ‘Tell me how do I feel’—emotion recognition and theory of mind in symptomatic mesial temporal lobe epilepsy.
      ]. Rates of coinciding deficits in visual and auditory emotional recognition vary between studies and range from 25% [
      • Fowler H.L.
      • Baker G.A.
      • Tipples J.
      • Hare D.J.
      • Keller S.
      • Chadwick D.W.
      • et al.
      Recognition of emotion with temporal lobe epilepsy and asymmetrical amygdala damage.
      ] to 36% [
      • Bonora A.
      • Benuzzi F.
      • Monti G.
      • Mirandola L.
      • Pugnaghi M.
      • Nichelli P.
      • et al.
      Recognition of emotions from faces and voices in medial temporal lobe epilepsy.
      ], indicating that multimodal deficits occur in some patients, but modalities can be impaired independently as well. Why some patients display emotion recognition deficits in multiple modalities is still unclear. Bonora et al. [
      • Bonora A.
      • Benuzzi F.
      • Monti G.
      • Mirandola L.
      • Pugnaghi M.
      • Nichelli P.
      • et al.
      Recognition of emotions from faces and voices in medial temporal lobe epilepsy.
      ] argue that patients with disease onset in childhood, and thus with a long duration of ongoing epileptogenic activity over the lifespan, are at particular risk for multimodal emotion recognition deficits.
      Apart from the classical approach of facially or vocally expressed emotions, emotion recognition can also be tested using more unconventional paradigms. In studies presenting pieces of music with differing emotional tones, worse recognition of the expressed emotion has been found for patients after anterior temporal lobe resection [
      • Gosselin N.
      Impaired recognition of scary music following unilateral temporal lobe excision.
      ]. When asked about the arousal caused by the musical excerpts, right TLE patients perceived scary music as less stimulating, and, compared to healthy controls, sad excerpts were rated as less relaxing. Left TLE patients indicated that peaceful music appeared less relaxing to them than it did to healthy individuals. Valence of the musical pieces was not rated differently by TLE patients and healthy controls. It would have interesting to discover whether TLE patients draw less pleasure from the musical excerpts due to their impaired recognition of the implied emotional tone and altered experience of arousal. Such a loss of satisfaction from pleasurable activities like listening to music could reduce patients’ quality of life.
      Traditional studies on emotion recognition, during which patients have to rate, match or label emotional expressions, have been criticised for neglecting the patient’s emotional experience while perceiving emotive stimuli. In order to measure this emotional experience, patients could be asked about their perceived arousal and valence of emotive stimuli [
      • Hennion S.
      • Sequeira H.
      • D’Hondt F.
      • Duhamel A.
      • Lopes R.
      • Tyvaert L.
      • et al.
      Arousal in response to neutral pictures is modified in temporal lobe epilepsy.
      ]. When confronted with fearful faces, Labudda et al. [
      • Labudda K.
      • Mertens M.
      • Steinkroeger C.
      • Bien C.G.
      • Woermann F.G.
      Lesion side matters—an fMRI study on the association between neural correlates of watching dynamic fearful faces and their evaluation in patients with temporal lobe epilepsy.
      ] found lower ratings of perceived fear in TLE patients. However, their perceived arousal in response to these fearful faces did not differ from that of healthy controls. Mirroring this finding, Hennion et al. [
      • Hennion S.
      • Sequeira H.
      • D’Hondt F.
      • Duhamel A.
      • Lopes R.
      • Tyvaert L.
      • et al.
      Arousal in response to neutral pictures is modified in temporal lobe epilepsy.
      ] reported equal levels of arousal related to unpleasant images in TLE and healthy participants, whereas arousal was higher for TLE patients when perceiving neutral pictures. Higher arousal was furthermore correlated with elevated levels of apathy, which could be interpreted as perception bias in emotional processing in TLE patients. However, alterations of arousal were not linked to further psychosocial variables. So far, no definite conclusion about the emotional experience of patients can be drawn, but incorporating such measures might be helpful in understanding their subjective perception of social stimuli.

      4. Theory of mind

      It is not sufficient to merely recognize the emotions of another individual on a perceptive level to successfully engage in beneficial social interactions. More complex socio-cognitive functions are necessary to infer the mental states of others and to predict their future behaviour based on their intentions, beliefs and emotions. Neuropsychological tests of these ToM functions usually present patients with situations that closely resemble social interactions typical of daily life, thus ToM deficits are likely to strain social bonds.
      Impaired ToM functions have frequently been found in TLE patients, and effect sizes have been found to exceed the impairments observed in FER [
      • Bora E.
      • Meletti S.
      Social cognition in temporal lobe epilepsy: a systematic review and meta-analysis.
      ]. Hennion et al. [
      • Hennion S.
      • Szurhaj W.
      • Duhamel A.
      • Lopes R.
      • Tyvaert L.
      • Derambure P.
      • et al.
      Characterization and prediction of the recognition of emotional faces and emotional bursts in temporal lobe epilepsy.
      ] showed that TLE patients struggled to deduce beliefs and emotions in stories in which protagonists unintentionally commit social blunders (faux-pas) or to understand sarcastic comments. These ToM deficits were correlated with lack of social support and affective disturbances. Interference of intentions and emotions in a story-based task was found to be impaired in TLE patients but not in patients with idiopathic generalized epilepsy [
      • Realmuto S.
      • Zummo L.
      • Cerami C.
      • Agrò L.
      • Dodich A.
      • Canessa N.
      • et al.
      Social cognition dysfunctions in patients with epilepsy: evidence from patients with temporal lobe and idiopathic generalized epilepsies.
      ]; however, the latter group also showed mild deficits in emotion recognition.
      Giovagnoli et al. [
      • Giovagnoli A.R.
      • Parente A.
      • Villani F.
      • Franceschetti S.
      • Spreafico R.
      Theory of mind and epilepsy: what clinical implications?.
      ] found poorer ToM abilities in TLE patients, but also in patients with frontal lobe epilepsy as compared to healthy controls. The two groups did not differ from each other in their abilities to detect and understand faux-pas. Patients who performed better on this task were reported to use more efficient coping strategies in response to stressful events and perceived their quality of life higher than patients with weaker ToM abilities. However, an association between ToM abilities and quality of life has not consistently been found [
      • Broicher S.D.
      • Kuchukhidze G.
      • Grunwald T.
      • Krämer G.
      • Kurthen M.
      • Jokeit H.
      ‘Tell me how do I feel’—emotion recognition and theory of mind in symptomatic mesial temporal lobe epilepsy.
      ]. The importance of ToM for one’s daily life was further demonstrated in Wang et al.’s study [
      • Wang W.-H.
      • Yu H.-Y.
      • Hua M.-S.
      Theory of mind and its brain distribution in patients with temporal lobe epilepsy.
      ] that examined ToM in a large sample of therapy-refractory TLE patients. TLE patients performed worse in understanding false belief, implied meaning, faux-pas and cartoon ToM stories. ToM deficits in the faux-pas test also predicted poor social functioning such as social engagement, leisure activities and instrumental living skills in patients. Together with the severity of psychiatric symptoms, ToM further predicted low interpersonal relationships, difficulties in communication, and employment status [
      • Wang W.-H.
      • Yu H.-Y.
      • Hua M.-S.
      Theory of mind and its brain distribution in patients with temporal lobe epilepsy.
      ].
      Although these findings are based on subjective self-report questionnaires, they demonstrate a link between the ability to infer the mental states of others and social functioning in TLE patients. Problematically, many TLE patients are not adequately aware of their own neuropsychological impairments in this area [
      • Giovagnoli A.R.
      Awareness, overestimation, and underestimation of cognitive functions in epilepsy.
      ], thus clearly limiting the validity of self-report measures in this population. Given the difficulties inferring the mental states of others, it is questionable if such patients have sufficient insight into their own mental states. This concern is underpinned by heterogeneous findings from self-report questionnaires on empathy in TLE patients. In studies where patients were asked to rate cognitive and affective aspects of empathy, findings range from lower empathetic concern for others in TLE [
      • Toller G.
      • Adhimoolam B.
      • Grunwald T.
      • Huppertz H.-J.
      • Kurthen M.
      • Rankin K.P.
      • et al.
      Right mesial temporal lobe epilepsy impairs empathy-related brain responses to dynamic fearful faces.
      ], to lower cognitive, but not affective, empathy [
      • Hennion S.
      • Szurhaj W.
      • Duhamel A.
      • Lopes R.
      • Tyvaert L.
      • Derambure P.
      • et al.
      Characterization and prediction of the recognition of emotional faces and emotional bursts in temporal lobe epilepsy.
      ], to no difference at all between TLE patients and controls [
      • Broicher S.D.
      • Kuchukhidze G.
      • Grunwald T.
      • Krämer G.
      • Kurthen M.
      • Jokeit H.
      ‘Tell me how do I feel’—emotion recognition and theory of mind in symptomatic mesial temporal lobe epilepsy.
      ]. Correspondence between self-report questionnaires and behavioural variables is often low [
      • Broicher S.D.
      • Kuchukhidze G.
      • Grunwald T.
      • Krämer G.
      • Kurthen M.
      • Jokeit H.
      ‘Tell me how do I feel’—emotion recognition and theory of mind in symptomatic mesial temporal lobe epilepsy.
      ].
      This points out that more appropriate measures of empathy and social functioning, such as third-party reports from family members, close friends or co-workers, should be implemented to better determine the actual influence of ToM deficits in a patient’s daily life. Of course, it is possible that behavioural deficits detected in neuropsychological examinations appear worse than patients’ socio-cognitive functions in their familiar surrounding actually are. On the other hand, the impact of these deficits might be underestimated due to inadequate test procedures and lack of objective evaluation of everyday socio-cognitive abilities.

      5. Perspectives

      As discussed, the reasons for difficulties with social competence and functioning are multifaceted in epilepsy (see Fig. 1), and at present there are no known therapeutic programs for this population that focus on deficits in social interactions [
      • Szemere E.
      • Jokeit H.
      Quality of life is social—towards an improvement of social abilities in patients with epilepsy.
      ]. To overcome the diagnostic discrepancy between neuropsychological findings and psychosocial measures of daily life, it is first necessary to gain a thorough understanding of social cognition as a multifaceted neuropsychological domain. While many studies have tried to characterize either basic or higher socio-cognitive functions in TLE, few attempts have been made to unravel the relationship between these levels of social cognition.
      Fig. 1
      Fig. 1Individual and interpersonal determinants of social functioning in epilepsy.
      Emotion recognition and ToM abilities are strongly entwined from a theoretical point of view, and an efficient interplay of perception and interpretation is needed for adaptive social behaviour [
      • Mitchell R.L.C.
      • Phillips L.H.
      The overlapping relationship between emotion perception and theory of mind.
      ]. Unfortunately, even studies with a comprehensive assessment of socio-cognitive functions fail to report correlations between various aspects.
      Broicher et al. [
      • Broicher S.D.
      • Kuchukhidze G.
      • Grunwald T.
      • Krämer G.
      • Kurthen M.
      • Jokeit H.
      ‘Tell me how do I feel’—emotion recognition and theory of mind in symptomatic mesial temporal lobe epilepsy.
      ] showed an association between emotion recognition and performance in the Iowa Gambling Task. Moreover, patients scoring high in emotion recognition showed more appropriate inferences of intentions and emotions when watching a movie clip of animated geometrical shapes whose movements implied social behaviour. However, emotion recognition and other ToM abilities such as the cognitive and affective understanding of faux-pas as well as ascribing mental states to people based on their eyes were independent of each other. In line with these findings, Amlerova et al. [
      • Amlerova J.
      • Cavanna A.E.
      • Bradac O.
      • Javurkova A.
      • Raudenska J.
      • Marusic P.
      Emotion recognition and social cognition in temporal lobe epilepsy and the effect of epilepsy surgery.
      ] failed to find an association between changes in emotion recognition and changes in ToM abilities after epilepsy surgery. For the time being, the relationship between different processes of social cognition remains elusive, and it is still unclear how other neuropsychological processes such as processing speed or working memory influence socio-cognitive processes and social functioning in real life.
      In conclusion, socio-cognitive deficits have been well established in a subgroup of TLE patients, but our understanding of the relationships among domains of socio-cognitive functions and its representations in the central and autonomous nervous system is astonishingly small. We have to keep in mind that the process of successful and enjoyable social interactions is characterized by reciprocity, smooth social encounters, mutual adjustment, temporal and emotional synchronisation, and entrainment. The presentation of photographs and sheets of paper with faux-pas stories, therefore, only represent our initial efforts to establish social cognition within neuropsychology. We call attention to the necessity of bridging the gap between behavioural findings obtained in highly standardized study settings and the processing of the enormous wealth of social cues in real life. Currently, it is not known how the observed socio-cognitive deficits seen in TLE patients translate to the enjoyable but demanding processing of social information in areas of life as diverse as employment, romantic and family relationships, or friendships. We hope that future research will bring forth new and differentiated diagnostic and therapeutic approaches that will allow social cognition to become a key component in the comprehensive assessment and care of people with epilepsy.

      Funding

      The position of B.K. Steiger is funded by the Swiss Epilepsy Foundation .

      Conflict of interest statement

      None.

      Acknowledgements

      We thank Victoria Reed and Esther Spirig for valuable comments regarding the improvement of the manuscript.

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