Characteristics and Neural Correlates of Emotional Behavior during Prefrontal Seizures

Abstract

This study was undertaken to characterize clinical expression and intracerebral electroencephalographic (EEG) correlates of emotional expression during prefrontal epileptic seizures. Methods: We performed a descriptive analysis of seizure semiology in patients explored with stereo-EEG (SEEG) for pharmacoresistant prefrontal epilepsy, using a semiquantitative score for seizure-related emotional behavior. Two independent observers scored occurrence and intensity of objective emotional features (face/body movements/vocalization/overall appearance), testing interobserver reliability. Intracerebral electrophysiological changes were documented. Cluster analysis and principal component analysis (PCA) compared behavioral signs with neural SEEG correlates. For each patient, the clinical and anatomoelectrophysiological scores were established, based on a prototypical emotional seizure. Results: Forty-two patients (469 seizures) were included. Interobserver correlation for emotional signs was satisfactory (kappa = 0.6-0.8). Prevalence of any subjective and/or objective ictal emotional phenomena was 79% (33/42); objective emotional signs occurred in 27 of 42 subjects (64%). Negatively valenced emotional semiology (ictal feeling of fear, defensive and/or aggressive behaviors) was much more prevalent than positively valenced, prosocial behaviors. Cluster analysis and PCA identified 4 groups with different occurrence of emotional signs and cerebral correlates. Two main clusters of negatively valenced behavior were identified: "active threat response," associated with seizure organizations involving posterior orbitofrontal cortex, anterior cingulate, and dorsolateral and/or ventrolateral prefrontal cortex; and "passive fear," associated with amygdala, other mesial temporal structures, and posterior orbitofrontal cortex. Interpretation: Emotional behaviors, especially fear/threat response, are common in prefrontal seizures, reflecting the role of the prefrontal cortex in emotional control. Different cortical seizure localizations were associated with "passive fear" and "active threat response" seizure behaviors at the group level.

Emotional experience elicited by direct electrical stimulation: Case series and literature review

“…While our research mainly focused on subjective emotional experiences. The difference between Singh et al 15 and our study probably due to subjective experience of fear and the objective behavioral function were controlled by different brain networks.…”

“…A recent study about emotional behavior during prefrontal seizures of Singh et al 15 found that positive behavioral during seizures had predominant involvement of the frontopolar and anterior orbitofrontal regions. However, our research mainly focused on subjective emotional experiences in relative normal brain regions, so our conclusions were slightly different from the study of Singh et al 15 …”

“…Singh et al 15 summarized objective movements or expressions and found that passive fear was correlated with mesial temporal structures (especially amygdala) and posterior orbitofrontal cortex and/or anterior cingulate, reflecting the role of the prefrontal cortex in emotional control. While our research mainly focused on subjective emotional experiences.…”

“…Clinical data for 400 medically refractory epilepsy cases who underwent stereo‐electroencephalography (SEEG) implantation for localization of the epileptogenic zone (EZ) at the Beijing Institute of Functional Neurosurgery (Beijing, China) between October 2015 and June 2021 were collected retrospectively. The aim of this study was to investigate the localization of subjective emotional responses in relatively normal brain regions, while it remains uncertain to what degree seizure‐related expressions could reflect mechanisms of physiological emotional expression 15 . And, it remains a question that whether the auras or the symptoms in early seizure propagation can reflect the physiological function of the stimulated focal cortex in the epileptogic network.…”

“…The aim of this study was to investigate the localization of subjective emotional responses in relatively normal brain regions, while it remains uncertain to what degree seizure-related expressions could reflect mechanisms of physiological emotional expression. 15 And, it remains a question that whether the auras or the symptoms in early seizure propagation can reflect the physiological function of the stimulated focal cortex in the epileptogic network. For this reason, we try to investigate the subjective emotional responses in relative normal cortex in this study.…”