Dynamic Causal White Matter Atlas of Auditory and Visual Speech Networks at Millisecond Resolution: Intracranial Evidence from 125 Patients

Abstract

Background and ObjectivesSince the era of Penfield, invasive neurophysiology has laid a lasting foundation for functional neuroscience by elucidating brain regions necessary for speech. However, whole-brain investigations have yet to distinguish the millisecond-scale dynamics and specific white matter pathways that support rapid naming in the auditory and visual domains. MethodsIn this observational study, we constructed a whole-brain Dynamic Causal Tractography atlas using intracranial neurophysiological data from 125 neurosurgical patients. The resulting video atlas captured local cortical high-gamma activity and cortico-cortical coactivation via white matter tracts during rapid and delayed auditory and picture naming. Direct electrical stimulation was employed to assess the causal significance of the observed neural dynamics. ResultsThe atlas revealed white matter coactivation intensity patterns at specific 5-millisecond time windows that best aligned with sensorimotor and language symptoms elicited by electrical stimulation (Spearmans {rho} = 0.58-0.91; p = 4.8 x 10cc to 1.6 x 10c{superscript 2}c). Rapid auditory naming was associated with deactivation of the right rostral middle frontal gyrus and increased coactivation along the left arcuate fasciculus, linked to stimulation-induced receptive and expressive aphasia. In contrast, delayed auditory naming correlated with a late surge in bifrontal coactivation. Rapid picture naming involved early coactivation between cortices connected via the bilateral inferior longitudinal fasciculi--associated with stimulation-induced visual distortions--coinciding with transient co-inactivation of Brocas area. DiscussionThese findings delineate dissociable white matter-mediated mechanisms supporting rapid naming in the auditory and visual domains. Reduced inhibitory monitoring by the right dorsolateral prefrontal cortex may facilitate efficient lexical retrieval via left perisylvian pathways during auditory naming. In contrast, excessive bifrontal interaction may underlie delayed auditory naming. Rapid visual object recognition appears to rely on early occipitotemporal coactivation with minimal involvement of Brocas area. The resulting atlas--accompanied by a publicly available dataset (61.2 GB) and analysis code--serves as a valuable resource for students and trainees studying the network dynamics underlying speech, as well as for presurgical language mapping in patients undergoing cortical or subcortical intervention.