Abstract
Rainer LJ, Kuchukhidze G, Trinka E, Braun M, Kronbichler M, Langthaler P, Zimmermann G, Kronbichler L, Said-Yürekli S, Kirschner M, Zamarian L, Schmid E, Jokeit H, Höfler J. Epilepsia. 2023;64(12):3319-3330. doi:10.1111/epi.17783. Epub 2023 Oct 18. PMID: 37795683 Objective: Perception and recognition of emotions are fundamental prerequisites of human life. Patients with juvenile myoclonic epilepsy (JME) may have emotional and behavioral impairments that might influence socially desirable interactions. We aimed to investigate perception and recognition of emotions in patients with JME by means of neuropsychological tests and functional magnetic resonance imaging (fMRI). Methods: Sixty-five patients with JME (median age = 27 years, interquartile range [IQR] = 23-34) were prospectively recruited at the Department of Neurology, Christian Doppler University Hospital, Paracelsus Medical University, Salzburg, Austria. Patients were compared to 68 healthy controls (median age = 24 years, IQR = 21-31), matched for sex, age, and education. All study participants underwent the Networks of Emotion Processing test battery (NEmo), an fMRI paradigm of “dynamic fearful faces,” a structured interview for psychiatric and personality disorders, and comprehensive neuropsychological testing. Results: JME patients versus healthy controls demonstrated significant deficits in emotion recognition in facial and verbal tasks of all emotions, especially fear. fMRI revealed decreased amygdala activation in JME patients as compared to healthy controls. Patients were at a higher risk of experiencing psychiatric disorders as compared to healthy controls. Cognitive evaluation revealed impaired attentional and executive functioning, namely psychomotor speed, tonic alertness, divided attention, mental flexibility, and inhibition of automated reactions. Duration of epilepsy correlated negatively with parallel prosodic and facial emotion recognition in NEmo. Deficits in emotion recognition were not associated with psychiatric comorbidities, impaired attention and executive functions, types of seizures, and treatment. Significance: This prospective study demonstrated that as compared to healthy subjects, patients with JME had significant deficits in recognition and perception of emotions as shown by neuropsychological tests and fMRI. The results of this study may have importance for psychological/psychotherapeutic interventions in the management of patients with JME.
Commentary
Social cognition encompasses a set of mental functions that collectively facilitate the representation of relationships and the navigation of our social environment. 1 Evidence from functional imaging studies supports the existence of a neural network specialized for social cognition, spanning specific limbic and neocortical subregions. 2 Social cognitive function is measured using validated psychometric instruments. Basic psychometric instruments present static pictures of human faces and ask to infer the person's mental state, eg, Reading the Eyes in the Mind Task. 3 More complex paradigms present videos of people in social interactions and ask to judge intent, eg The Assessment of Social Inference Task. 4 Studies aiming to quantify social cognitive abilities in patients with epilepsy have identified deficits in patients with focal epilepsy, particularly temporal lobe epilepsy. 5 Conversely, much less is known about social cognition in patients with idiopathic generalized epilepsy.
In the present study, Rainer et al investigated elements of social cognition—specifically emotional perception and recognition—in 65 patients with juvenile myoclonic epilepsy (JME) and compared their performance to matched controls. The authors found that patients with JME have deficits in identifying all primary emotional states compared to controls. Furthermore, the authors found that patients with JME have weaker activation of the right and left amygdala during emotion perception as measured by fMRI. Lastly, the study identified higher levels of psychiatric disturbances and deficits in attention, executive function, and impulsivity in patients with JME. The clear identification of social cognitive deficits in patients with JME in this study provides a more comprehensive understanding of this population's relatively poor social functioning. For instance, it helps to explain why employment and marriage rates among individuals with JME are lower compared to healthy controls, irrespective of the degree of seizure control.6,7
Some caution must be exercised when interpreting these findings. First, the underlying cause of social cognitive deficits in JME is unclear. Evidence from imaging studies supports the idea that patients with JME have differences in neural anatomy and neural network connectivity, which could result in an erroneous representation of the social world, 8 including the finding of decreased amygdala activation in this study. An alternative explanation suggests a developmental mechanism. 7 Children with JME may be less exposed to social environments during critical periods of social cognitive development and, in turn, develop poor social skills. Second, social cognition is a complex cognitive domain that is challenging to model. Many standardized psychometric instruments are outdated, static, non-naturalistic, culturally insensitive, and may not measure social cognitive abilities critical to everyday life. Novel, more temporary, diverse, and naturalistic paradigms need to be developed to better measure the extent of social cognitive deficits. Third, adequate performance on social cognitive psychometric tasks requires sustained attention. However, studies in patients with JME often identify deficits in attention, executive function, and impulse control, 9 including in the present study. As such, deficits in these more fundamental cognitive domains in patients with JME may falsely augment the degree of social cognitive dysfunction, especially on the more complex social cognitive tasks which require strong working memory and sustained attention. Lastly, what do we do about these findings? Therapy designed to mitigate social cognitive dysfunction in patients with epilepsy has not been developed. Ensuring deep immersion in social activities during adolescence may be especially important in kids with JME to ensure development of strong social cognition. Advising adult patients with JME to seek help when preparing for job interviews or referring them for relationship therapy could help patients understand and manage these deficits.
