Ictal semiology in anterior cingulate epilepsy: A systematic review

Abstract

Seizures originating from the anterior cingulate cortex (ACC) have distinct clinical features but can be difficult to identify in frontal lobe epilepsy (FLE). This systematic review examines the key semiology of ACC seizures and their anatomical correlations. A systematic search was conducted following PRISMA guidelines, including studies reporting ictal semiology, invasive EEG findings, and surgical outcomes in patients with ACC seizures, allowing for the establishment of anatomical and clinical correlations with a high level of confidence. Studies based only on stimulations were excluded. We selected 23 studies including 93 patients (57% males, 46% children). MRI positive (59%), invasive monitoring (74%), surgery (100%) with Engel class I outcome (80%) were the main characteristics. Cortical lesions were found by histology in 86% of the surgical specimen, including focal cortical dysplasia in 67%. The level of confidence in epileptogenic zone (EZ) localization was considered high and very high in 87% of patients. Auras reported by 58% of them mostly included affective (fear or negative emotional feelings) and/or autonomic symptoms (80%). The main ictal signs consisted of facial emotional expressions (46%), autonomic features (48%), vocalization and sudden complex/hypermotor behavior (60%). Spectacular manifestations with preserved awareness, verbalizations with emotional content, laughter, ictal pouting ("chapeau de gendarme") can also point to ACC involvement. In contrast, dystonic/tonic-clonic features, head and eye deviations were less frequently observed (<20%). Loss of consciousness was reported in 35% of patients. Immediate recovery at the seizure-end was usual. Short seizures (<1 min) occurring in clusters during sleep were also characteristics. Combination of these features enhanced the likelihood of ACC origin. Interictal personality disorders which improved after seizure control can be also observed. ACC seizures are predominantly characterized by emotional, autonomic, and striking behavior manifestations contrasting with preserved awareness. These semiology markers support an anatomical and clinical entity and help to localize the EZ in FLE.

Keywords: anatomo‐clinical correlations; anterior cingulate cortex; epilepsy surgery; focal epilepsy; ictal semiology; systematic review.

FIGURE 1

Flowchart of the systematic review.

FIGURE 2

Anatomical landmarks and functional subdivisions of the ACC. (A) The cingulate cortex has historically been divided into two regions based on cytoarchitectonic Brodmann's areas (BA). The anterior cingulate cortex (ACC) comprises BA24 (orange), BA25 (blue), BA32 (green), and BA33 (yellow), while the posterior cingulate cortex includes BA23 (red), BA29 and BA30 (brown), and BA31 (dark blue). The VAC (vertical of the anterior commissure) line demarcates the boundary between the anterior and posterior regions. (B) More recent classifications divide the cingulate cortex into four functional subdivisions based on connectivity patterns. The ventral ACC (green) exhibits strong connectivity with the limbic system and is involved in emotion and mood regulation. The dorsal ACC (dark green) connects with the dorsolateral prefrontal cortex and contributes to decision‐making via the frontoparietal network. The anterior midcingulate cortex (light blue) is linked to the dorsolateral prefrontal and premotor cortices and plays a role in cognitive control and effort‐based decision‐making. The posterior midcingulate cortex (dark blue) connects to motor and somatosensory cortices and is implicated in somatosensory integration and motor preparation. The posterior cingulate cortex (brown) serves as a core hub of the default mode network and is associated with self‐referential thought and consciousness. The retrosplenial cingulate cortex (yellow), which connects to the hippocampus and parietal regions, contributes to memory encoding and body position awareness.

FIGURE 3

Examples of facial expressions and motor behavior changes during ACC seizures. (A) Intense fear with sitting up and screaming, (B) Grimacing face with closed eyes, chapeau de gendarme, non‐integrated hypermotor behavior; (C) Facial expression of fear, ictal pouting with open eyes, and gesticulation; (D) Hypermotor behavior with projection of the lower limbs. All pictures correspond to the earliest phase of the seizure.

FIGURE 4

Symptom characteristics. Symptoms are listed row‐wise, with their rate of observation, confidence grade, and timing of observation visualized using color maps alongsd the actual values.

FIGURE 5

Typicality of symptoms. The occurrence percentage of each symptom is represented by numbers and bars. Green indicates typical symptoms, meaning they occur in more than one‐third of patients, as determined by one‐sided binomial tests assessing whether the observed rate significantly exceeds 0.33. Orange indicates not meeting this threshold.

FIGURE 6

Pairwise odds ratios for symptom occurrence. The color scale spans from orange (odds ratio: OR <1) to green (OR >1), with white indicating values near 1. Bold labels denote statistically significant comparisons after Holm correction. Each cell value represents the OR for the symptom on the x‐axis relative to the symptom on the y‐axis.