Cognitive impairments and neurofunctional alterations in children with electrical status epilepticus during sleep: insights from WISC-IV and resting-state fMRI

BACKGROUND: Electrical Status Epilepticus During Sleep (ESES) is a rare pediatric epilepsy syndrome characterized by sleep-induced epileptiform discharges, leading to cognitive and behavioral impairments. We aimed to investigate the underlying neural mechanisms that are critical for advancing early diagnosis and targeted interventions. METHODS: Twenty-five children with ESES and 30 age- and sex-matched healthy controls were enrolled. Cognitive function was assessed via the Wechsler Intelligence Scale for Children, Fourth Edition (WISC-IV), focusing on Full-Scale IQ (FSIQ), Verbal Comprehension Index (VCI), Perceptual Reasoning Index (PRI), Working Memory Index (WMI), and Processing Speed Index (PSI). Resting-state functional MRI (rs-fMRI) was conducted to evaluate neural activity via regional homogeneity (ReHo) analysis. Correlations between ReHo values and cognitive scores were analyzed in the ESES group. RESULTS: Compared with healthy controls, children with ESES presented significantly lower FSIQ and PRI scores (P = 0.017, P = 0.016), indicating cognitive impairments in global intellectual abilities and perceptual reasoning. rs-fMRI revealed decreased ReHo in the left Superior Frontal Gyrus (premotor area), bilateral postcentral gyri (primary somatosensory cortex), right cerebellum posterior, and rolandic operculum. In contrast, increased ReHo was observed in the left precuneus and left middle frontal gyrus. ReHo in the right postcentral gyrus showed a positive correlation with FSIQ and VCI scores (r = 0.56, P = 0.01; r = 0.67, P < 0.001). CONCLUSIONS: ESES is associated with significant cognitive deficits, particularly in perceptual reasoning and verbal comprehension, alongside altered neural activity patterns. ReHo analysis revealed changes in local neural activity within key brain regions linked to cognitive function. These findings highlight the potential of rs-fMRI metrics as biomarkers for assessing cognitive impairments and guiding therapeutic interventions in ESES.