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.

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 [], have lower rates of employment [] and cite lack of social engagement and difficulty in developing satisfying interpersonal relationships as common problems []. 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.

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 [] 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 [].

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.

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’ []. 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.

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 []. 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 []. 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 [], 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.

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 []. Moreover, epilepsy patients apparently have an increased risk of having impaired social cognitive skills and suffering from communication problems and interpersonal difficulties []. 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.

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 []. 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 [].

These socio-cognitive functions cannot be linked to one specific brain region, but instead rely on distributed networks []. 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 [], 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.

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 []. 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.

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 [].

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 []. Thus, transient and chronic cognitive impairment in patients with epilepsies itself is a risk factor for poor social integration.

3. Multimodal recognition of emotion

20 Jack R.E.

Schyns P.G. The human face as a dynamic tool for social communication. 21 Bora E.

Meletti S. Social cognition in temporal lobe epilepsy: a systematic review and meta-analysis. 22 Monti G.

Meletti S. Emotion recognition in temporal lobe epilepsy: a systematic review. 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 []. 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 [] 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 [].

23 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. 24 Meletti S.

Benuzzi F.

Cantalupo G.

Rubboli G.

Tassinari C.A.

Nichelli P. Facial emotion recognition impairment in chronic temporal lobe epilepsy. 21 Bora E.

Meletti S. Social cognition in temporal lobe epilepsy: a systematic review and meta-analysis. 22 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 []. While poor FER performance has been observed repeatedly, the influence of clinical variables is still unclear. In their meta-analysis, Bora and Meletti [] 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 [].

25 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. 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 []. 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.

26 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. 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. [] 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.

27 Schacher M.

Haemmerle B.

Woermann F.G.

Okujava M.

Huber D.

Grunwald T.

et al. Amygdala fMRI lateralizes temporal lobe epilepsy. 28 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. 29 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. 29 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. 28 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. 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 []. Alterations of activity in response to fearful faces have been found for the ipsilateral amygdala [] and also for more widespread occipital, temporal and frontal regions []. Furthermore, activity of the amygdala has been linked to ratings of fear expressed by faces [] and empathetic concern in a self-report questionnaire []. Additional studies are needed to infer the behavioural relevance of these fMRI differences during the processing of emotional faces.

30 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. 31 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. 23 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. 23 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. 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 []. Rates of coinciding deficits in visual and auditory emotional recognition vary between studies and range from 25% [] to 36% [], 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. [] 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.

32 Gosselin N. Impaired recognition of scary music following unilateral temporal lobe excision. 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 []. 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.