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

Yu Kitazawa, Masaki Sonoda, Kazuki Sakakura, Takumi Mitsuhashi, Ethan Firestone, Riyo Ueda, Toshimune Kambara, Hirotaka Iwaki, Aimee F. Luat, Neena I. Marupudi, Sandeep Sood, Eishi Asano

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

Abstract

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.

Original languageEnglish
Article number119954
JournalNeuroImage
Volume270
DOIs
StatePublished - Apr 15 2023

Keywords

  • Event-related high-gamma synchronization
  • Functional language mapping
  • Normative dynamic tractography atlas
  • pediatric epilepsy surgery
  • subdural electrocorticography (ECoG)

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