Abstracts

Rationale: We visualized the dynamics of neural communications in white matter pathways during a picture naming task. We determined the significance of such neural communications by assessing the relationship with response times and symptoms elicited by electrical stimulation mapping (ESM).

Methods: We studied 92 patients (mean age: 14; age range: 5-49 years) who underwent intracranial EEG recording as part of their epilepsy presurgical evaluation. We quantified task-related high-gamma modulations (70-110 Hz) at 7343 nonepileptic electrode sites and visualized the dynamics of functional connectivity modulations across 68 regions of interest (ROIs). Functional connectivity was considered enhanced or diminished between an ROI pair if they were connected by a direct streamline on tractography and exhibited significant, simultaneous, and sustained high-gamma augmentation or attenuation. Using effective connectivity analysis, we determined the directionality of neural information flows, declaring that information flowed from one region to another if the high-gamma activity in a region was predictive of subsequent activity changes in another. Mixed model analysis was utilized to assess the effect of network dynamics on response times. Additionally, we applied probability mapping of ESM-induced language symptoms to elucidate the causal roles of specific cortical regions.

Results: Among 2,278 ROI pairs, 989 were judged as having a direct white matter streamline. Functional connectivity initially increased within visual areas, showing posterior-to-anterior dominant neural information flows, with decreased connectivity in bilateral prefrontal areas. Subsequently, functional connectivity was enhanced and bidirectional neural information flows occurred through the arcuate fasciculus connecting from the left posterior inferior temporal, fusiform, and parahippocampal gyri to the left inferior precentral gyrus. Enhanced functional connectivity through these specific arcuate fasciculus segments was linked to faster response times, and the cortical areas connected by these arcuate segments were associated with a higher risk of naming errors upon stimulation. Conversely, the left arcuate fasciculus from the posterior superior/middle temporal gyri showed functional connectivity enhancement only at response onset or afterward.

Conclusions: Our dynamic tractography atlas reveals critical network dynamics supporting picture naming. Direct neural communications through a specific segment of the left arcuate fasciculus, originating from the posterior inferior temporal, fusiform, and parahippocampal regions and extending to the inferior precentral gyrus, are crucial for lexical retrieval during picture naming.

Funding: NIH R01 NS064033 (to E.A.).