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
Affiliations
Yu Kitazawa
Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA; Department of Neurology and Stroke Medicine, Yokohama City University, Yokohama, 2360004, Japan
Masaki Sonoda
Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA; Department of Neurosurgery, Yokohama City University, Yokohama, 2360004, Japan
Kazuki Sakakura
Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA; Department of Neurosurgery, University of Tsukuba, Tsukuba, 3058575, Japan
Takumi Mitsuhashi
Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA; Department of Neurosurgery, Juntendo University, Tokyo, 1138421, Japan
Ethan Firestone
Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA; Department of Physiology, Wayne State University, Detroit, 48201, USA
Riyo Ueda
Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA
Toshimune Kambara
Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA; Department of Psychology, Hiroshima University, Hiroshima, 7398524, Japan
Hirotaka Iwaki
Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA; Department of Psychiatry, Hachinohe City Hospital, Hachinohe, 0318555, Japan
Aimee F. Luat
Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA; Department of Neurology, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA; Department of Pediatrics, Central Michigan University, Mount Pleasant, 48858, USA
Neena I. Marupudi
Department of Neurosurgery, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA
Sandeep Sood
Department of Neurosurgery, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA
Eishi Asano
Department of Pediatrics, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA; Department of Neurology, Children's Hospital of Michigan, Wayne State University, Detroit, 48201, USA; Corresponding author at: Division of Pediatric Neurology, Children's Hospital of Michigan. 3901 Beaubien St., Detroit, MI, 48201, USA.
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.
