Characteristics and Neural Correlates of Emotional Behavior during Prefrontal Seizures.

OBJECTIVE: 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. ANN NEUROL 2022;92:1052-1065.

Postictal electroencephalographic (EEG) suppression: A stereo-EEG study of 100 focal to bilateral tonic-clonic seizures.

OBJECTIVES: We aimed to describe intracerebral aspects of postictal generalized electroencephalography suppression (PGES) following focal to bilateral tonic-clonic ("secondarily generalized tonic-clonic") seizures (GTCS) recorded using stereoelectroencephalographic (SEEG), and to correlate these with electroclinical features. METHODS: Three independent observers scored semiologic and SEEG features. Patient and epilepsy characteristics were collected. Descriptive statistics and multivariate analysis were performed. The operational definition of PGES on SEEG used strict criteria (absence of visible signal at 20 µV/mm amplitude, in all readable channels). Postictal regional suppression (RS) was identified if only a subset of implanted electrodes showed absence of signal. RESULTS: We evaluated 100 seizures in 52 patients. Interobserver agreement was good (κ 0.72 for clinical features and 0.73 for EEG features). PGES was present in 27 of 100 and RS without PGES present in 42 of 100 seizures. Region of RS included epileptogenic zone in 43 of 51 (86%). No effect of sampling (multilobar or bilateral exploration) was seen. Oral tonicity (mouth opening and/or tonic vocalization during the tonic phase of GTCS) was associated with the presence of PGES (P = 0.029; negative predictive value [NPV] 0.91). Bilateral upper limb extension during the tonic phase correlated with PGES (P = 0.041; NPV 0.85). Association of both oral tonicity and bilateral upper limb extension had a high NPV of 0.96. SIGNIFICANCE: SEEG recordings confirm true absence of signal during postictal EEG suppression. PGES is unlikely when both upper limb extension and oral tonicity are absent. We hypothesize that bilateral tonic seizure discharge at bulbar level brainstem regions is associated with the production of oral signs and may relate to mechanisms of PGES.

Early onset motor semiology in seizures triggered by cortical stimulation during SEEG.

OBJECTIVES: The objective of the study was to describe electroclinical patterns in habitual seizures with motor semiology at onset, triggered by diagnostic stimulation, in patients undergoing presurgical evaluation using stereoelectroencephalography (SEEG). METHODS: Seizure semiology, stimulation parameters, electroclinical data, and anatomical localization were evaluated in stimulated and spontaneous seizures. RESULTS: From 120 habitual seizures triggered by 50-Hz train bipolar stimulation during SEEG, 20 presented initial motor semiology (elementary motor signs, complex motor behavior, or both). Two patterns occurred: long latency onset (7/20), where semiology occurred after the stimulation train, following visible cortical epileptic discharge similarly to spontaneous seizures; and short latency onset (13/20), in which typical semiological expression occurred during the stimulation train, preceding typical cortical discharge. CONCLUSIONS: This novel observation shows that in some conditions, seizures with habitual motor semiology could be triggered early during stimulation, before typical cortical epileptic discharge became visible. The earliness of clinical onset with regard to visible cortical discharge, notably in comparison with clinically similar spontaneous seizures, suggests differences in electrophysiological mechanisms that require further investigation. These may involve preferential involvement of descending corticosubcortical connections within the same epileptogenic network for a given patient.