Abstract
Emotion Recognition and Social Cognition in Temporal Lobe Epilepsy and the Effect of Epilepsy Surgery.
Amlerova J, Cavanna AE, Bradac O, Javurkova A, Raudenska J, Marusic P. Epilepsy Behav 2014;36:86–89.
The abilities to identify facial expression from another person's face and to attribute mental states to others refer to preserved function of the temporal lobes. In the present study, we set out to evaluate emotion recognition and social cognition in presurgical and postsurgical patients with unilateral refractory temporal lobe epilepsy (TLE). The aim of our study was to investigate the effects of TLE surgery and to identify the main risk factors for impairment in these functions. We recruited 30 patients with TLE for longitudinal data analysis (14 with right-sided and 16 with left-sided TLE) and 74 patients for cross-sectional data analysis (37 with right-sided and 37 with left-sided TLE) plus 20 healthy controls. Besides standard neuropsychological assessment, we administered an analog of the Ekman and Friesen test and the Faux Pas Test to assess emotion recognition and social cognition, respectively. Both emotion recognition and social cognition were impaired in the group of patients with TLE, irrespective of the focus side, compared with healthy controls. The performance in both tests was strongly dependent on the intelligence level. Beyond intelligence level, earlier age at epilepsy onset, longer disease duration, and history of early childhood brain injury predicted social cognition problems in patients with TLE. Epilepsy surgery within the temporal lobe seems to have neutral effect on patients’ performances in both domains. However, there are a few individual patients who appear to be at risk of postoperative decline, even when seizure freedom is achieved following epilepsy surgery.
Commentary
Social cognition has a variety of definitions but can be described operationally as the encoding, storage, retrieval, and processing of information related to the interactions of individuals within a species. Social cognition is of obvious importance to most aspects of a person's daily life and has subsequently been the focus of considerable neuroscience research in the past 2 decades (1). The development of standardized testing of specific aspects of social cognition (e.g., facial expression recognition) in combination with neuroimaging techniques, such as functional MRI, has provided increased understanding of important neuroanatomic substrates (2, 3). As summarized in an excellent review of the neurobiology of social cognition, “Cortical regions in the temporal lobe participate in perceiving socially relevant stimuli, whereas the amygdala, right somatosensory cortices, orbitofrontal cortices, and cingulate cortices all participate in linking perception of such stimuli to motivation, emotion, and cognition” (4). Although not typically emphasized in conventional neuropsychological testing of persons with epilepsy, deficits in principal areas of social cognition may be extremely important for the ability to develop and sustain personal relationships and also to perform effectively in certain employment settings (5).
In a recent study of patients with temporal lobe epilepsy and healthy controls, Amlerova et al. used an analog of the Ekman and Friesen Test and the Faux Pas Test to assess facial emotion recognition and social cognition. They found that patients with temporal lobe epilepsy had significantly worse scores than controls for both emotional facial classification and also interpretation of faux pas in paragraphs describing social interactions. It is noteworthy that patients with either left or right temporal lobe epilepsy performed worse than healthy controls. The scores of the left and right groups were nearly identical, suggesting that the social cognitive abilities tested were not lateralized to a specific hemisphere in this representative sample of temporal lobe epilepsy patients. Bilateral temporal lobe dysfunction in unilateral epilepsy remains an alternative explanation. As suggested in prior studies (6, 7), the specific aspects of social cognition dysfunction could be different for left and right temporal lobe epilepsy; for example, it is possible that similar scores on facial emotion classification could occur in right temporal lobe patients with deficits in interpretation of emotional states, and left temporal lobe patients with deficits in retrieval or expression of socially relevant language.
Amlerova et al. also found no significant difference in scores of either the facial emotion or the faux pas tests between the presurgical and postsurgical assessments. This is a very important observation because prior studies of only postoperative social cognition have suggested that deficits may be due to the temporal lobe resection (8). The Amlerova et al. study supports the findings of the only other investigation of social cognition that included assessments for both before and after temporal lobe epilepsy surgery, which also found no worsening of measures of social cognition following surgery (9). However, the prior study observed improvement in interpretation of fearful faces following left temporal resection. Since assessment of facial fear has been associated with right amygdala dysfunction, the authors concluded that the improvement was either from removal of the hyperexcitable left amygdala that may misinterpret fearful facial expression with a blend of other emotions, or improvement of right amygdala function after ablation of the “noxious” effects the left temporal lobe (9). Perhaps this question, and others related to the localization of social cognition within the temporal lobes, could be answered through stimulation studies during presurgical intracranial EEG evaluations?
Another interesting observation in the study by Amlerova et al. was that overall intelligence was the strongest predictor of the scores on the assessments of social cognition. Additional significant factors included earlier age at epilepsy onset, longer disease duration, and history of early childhood brain injury. A subset of subjects, about one-fourth, experienced a decline of more than three points on either the emotional recognition or Faux Pas Test, but the change was not associated with any clinical or demographic variable. Future studies should evaluate the impact of social cognition on overall performance of daily activities, employment, and quality of life in epilepsy (i.e., ecological validity), but determining the specific role of social cognition may be difficult due to confounding by the strong correlation with overall IQ.
Despite the limitations of small sample size and a highly selected surgical series, Amlerova and colleagues make a compelling appeal for the inclusion of testing for social cognition and emotional recognition in routine neuropsychological assessments of persons with epilepsy. They emphasize that aspects of social cognition may be critically important for optimal management of common disabilities associated with epilepsy. Based on other recent publications (10), their findings may also extend to additional common seizure disorders such as idiopathic generalized epilepsy. Unfortunately, the larger considerations regarding the best methods to ameliorate adverse consequences of dysfunction of social cognition remain undetermined. Despite the formidable challenges that problems with social cognition pose, the recent findings by Amlerova et al. emphasize the potential importance of early control of refractory seizures and early identification of at-risk persons (such as those with childhood brain injury) with implementation of appropriate rehabilitation. Social cognition appears to deserve additional attention from the clinical and research epilepsy communities as we work toward improved understanding and outcomes.