Electrocorticography reveals spatiotemporal neuronal activation patterns of verbal fluency in patients with epilepsy

Verbal fluency is commonly used to evaluate cognitive dysfunction in a variety of neuropsychiatric diseases, yet the neurobiology underlying performance of this task is incompletely understood. Electrocorticography (ECoG) provides a unique opportunity to investigate temporal activation patterns during cognitive tasks with high spatial and temporal precision. We used ECoG to study high gamma activity (HGA) patterns in patients undergoing presurgical evaluation for intractable epilepsy as they completed an overt, free-recall verbal fluency task. We examined regions demonstrating changes in HGA during specific timeframes relative to speech onset. Early pre-speech high gamma activity was present in left frontal regions during letter fluency and in bifrontal regions during category fluency. During timeframes typically associated with word planning, a distributed network was engaged including left inferior frontal, orbitofrontal and posterior temporal regions. Peri-Rolandic activation was observed during speech onset, and there was post-speech activation in the bilateral posterior superior temporal regions. Based on these observations in the context of prior studies, we propose a model of neocortical activity patterns underlying verbal fluency.