Intra– and inter–hemispheric network dynamics supporting object recognition and speech production

• Published in: NeuroImage (Orlando, Fla.) Vol. 270; p. 119954
• Main Authors: Kitazawa, Yu, Sonoda, Masaki, Sakakura, Kazuki, Mitsuhashi, Takumi, Firestone, Ethan, Ueda, Riyo, Kambara, Toshimune, Iwaki, Hirotaka, Luat, Aimee F., Marupudi, Neena I., Sood, Sandeep, Asano, Eishi
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 15-04-2023; Elsevier Limited; Elsevier
• Subjects: Brain; Brain Mapping - methods; Epilepsy; Event-related high-gamma synchronization; Firing pattern; Frontal gyrus; Functional language mapping; Hemispheric laterality; Hemodynamics; Humans; Hypotheses; Information processing; Language; Neural networks; Neuroimaging; Normative dynamic tractography atlas; Pattern recognition; pediatric epilepsy surgery; Sound; Speech; Speech - physiology; subdural electrocorticography (ECoG); Substantia alba; Visual Perception - physiology; pediatric epilepsy surgery; Event-related high-gamma synchronization; subdural electrocorticography (ECoG); Functional language mapping; Normative dynamic tractography atlas
• ISSN: 1053-8119; 1095-9572; 1095-9572
• DOI: 10.1016/j.neuroimage.2023.119954

•The movie animates naming-related neural network dynamics on a millisecond scale.•It visualizes neural interactions via intra- and inter-hemispheric white matter tracts.•Intra/interhemispheric connectivities are enhanced during perception and response.•Left intrahemispheric connectivity predominates during response preparation.•Distinct network dynamics support naming based on images, sounds, or sentences.
We built normative brain atlases that animate millisecond-scale intra- and inter-hemispheric white matter-level connectivity dynamics supporting object recognition and speech production. We quantified electrocorticographic modulations during three naming tasks using event-related high-gamma activity from 1,114 nonepileptogenic intracranial electrodes (i.e., non-lesional areas unaffected by epileptiform discharges). Using this electrocorticography data, we visualized functional connectivity modulations defined as significant naming-related high-gamma modulations occurring simultaneously at two sites connected by direct white matter streamlines on diffusion-weighted imaging tractography. Immediately after stimulus onset, intra- and inter-hemispheric functional connectivity enhancements were confined mainly across modality-specific perceptual regions. During response preparation, left intra-hemispheric connectivity enhancements propagated in a posterior-to-anterior direction, involving the left precentral and prefrontal areas. After overt response onset, inter- and intra-hemispheric connectivity enhancements mainly encompassed precentral, postcentral, and superior-temporal (STG) gyri. We found task-specific connectivity enhancements during response preparation as follows. Picture naming enhanced activity along the left arcuate fasciculus between the inferior-temporal and precentral/posterior inferior-frontal (pIFG) gyri. Nonspeech environmental sound naming augmented functional connectivity via the left inferior longitudinal and fronto-occipital fasciculi between the medial-occipital and STG/pIFG. Auditory descriptive naming task enhanced usage of the left frontal U-fibers, involving the middle-frontal gyrus. Taken together, the commonly observed network enhancements include inter-hemispheric connectivity optimizing perceptual processing exerted in each hemisphere, left intra-hemispheric connectivity supporting semantic and lexical processing, and inter-hemispheric connectivity for symmetric oral movements during overt speech. Our atlases improve the currently available models of object recognition and speech production by adding neural dynamics via direct intra- and inter-hemispheric white matter tracts.
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