Vulnerability of the ventral language network in children with focal epilepsy

Children with focal epilepsy are at increased risk of language impairment, yet the neural substrate of this dysfunction is not yet known. Using functional magnetic resonance imaging we investigated the impact of focal epilepsy on the developing language system using measures of network topology (spatial organization of activation) and synchrony (functional connectivity). We studied healthy children (n = 48, 4-12 years, 24 females) and children with focal epilepsy (n = 21, 5-12 years, nine females) with left hemisphere language dominance. Participants performed an age-adjusted auditory description decision task during functional magnetic resonance imaging, to identify perisylvian language regions. Mean signal change was extracted from eight left perisylvian regions of interest and compared between groups. Paired region of interest functional connectivity analysis was performed on time course data from the same regions, to investigate left network synchrony. Two principal component analyses were performed to extract (i) patterns of activation (using mean signal change data); and (ii) patterns of synchronized regions (using functional connectivity data). For both principal component analyses two components (networks) were extracted, which mapped onto the functional anatomy of dorsal and ventral language systems. Associations among network variables, age, epilepsy-related factors and verbal ability were assessed. Activated networks were affected by age and epilepsy [F(2,60) = 3.74, P = 0.03]: post hoc analyses showed, for healthy children, activation in both ventral and dorsal networks decreased with age (P = 0.02). Regardless of age and task performance, children with epilepsy showed reduced activation of the ventral network (P < 0.001). They also showed a trend for increased activation of the dorsal network (P = 0.08) associated with improved task performance (r = 0.62, P = 0.008). Crucially, decreased activation of the ventral network in patients predicted poorer language outcome ([Formula: see text] = 0.47, P = 0.002). This suggests childhood onset epilepsy preferentially alters maturation of the ventral language system, and this is related to poorer language ability.