Dynamic Causal Tractography Analysis of Auditory Descriptive Naming: An Intracranial Study of 106 Patients

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Abstract

Humans understand and respond to spoken questions through coordinated activity across distributed cortical networks. However, the causal roles of connectivity engagements alternating across multiple white matter bundles remain understudied at the whole-brain scale. Using intracranial high-gamma activity recorded from 7,792 non-epileptic electrode sites in 106 epilepsy patients who underwent direct cortical stimulation mapping, we constructed an atlas visualizing the millisecond-scale dynamics of functional connectivity during a naming task in response to auditory questions. This atlas, the Dynamic Causal Tractography Atlas, identified functional connectivity patterns at specific time windows most strongly associated with stimulation-induced language- and speech-related manifestations (p-value range: 2.5 × 10 -5 to 6.6 × 10 -14 ; rho range: +0.54 to +0.82). The atlas revealed that no single intra-hemispheric fasciculus was consistently engaged in all naming stages; instead, each fasciculus supported specific stages, with multiple distinct major fasciculi simultaneously contributing to each stage. Additionally, this atlas identified the specific linguistic stages and fasciculi where handedness effects became evident. Our findings clarify the dynamics and causal roles of alternating, coordinated neural activity through specific fasciculi during auditory descriptive naming, advancing current neurobiological models of speech network organization. Additionally, we have made our white matter streamline template and intracranial EEG data available as open-source material, enabling investigators to construct personalized dynamic tractography atlases.

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