Cargando…

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

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...

Descripción completa

Detalles Bibliográficos
Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10112006/
https://www.ncbi.nlm.nih.gov/pubmed/36828156
http://dx.doi.org/10.1016/j.neuroimage.2023.119954
_version_ 1785027557080432640
author 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
author_facet 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
author_sort Kitazawa, Yu
collection PubMed
description 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.
format Online
Article
Text
id pubmed-10112006
institution National Center for Biotechnology Information
language English
publishDate 2023
record_format MEDLINE/PubMed
spelling pubmed-101120062023-04-18 Intra– and inter–hemispheric network dynamics supporting object recognition and speech production 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 Neuroimage Article 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. 2023-04-15 2023-02-23 /pmc/articles/PMC10112006/ /pubmed/36828156 http://dx.doi.org/10.1016/j.neuroimage.2023.119954 Text en https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) )
spellingShingle Article
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
Intra– and inter–hemispheric network dynamics supporting object recognition and speech production
title Intra– and inter–hemispheric network dynamics supporting object recognition and speech production
title_full Intra– and inter–hemispheric network dynamics supporting object recognition and speech production
title_fullStr Intra– and inter–hemispheric network dynamics supporting object recognition and speech production
title_full_unstemmed Intra– and inter–hemispheric network dynamics supporting object recognition and speech production
title_short Intra– and inter–hemispheric network dynamics supporting object recognition and speech production
title_sort intra– and inter–hemispheric network dynamics supporting object recognition and speech production
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10112006/
https://www.ncbi.nlm.nih.gov/pubmed/36828156
http://dx.doi.org/10.1016/j.neuroimage.2023.119954
work_keys_str_mv AT kitazawayu intraandinterhemisphericnetworkdynamicssupportingobjectrecognitionandspeechproduction
AT sonodamasaki intraandinterhemisphericnetworkdynamicssupportingobjectrecognitionandspeechproduction
AT sakakurakazuki intraandinterhemisphericnetworkdynamicssupportingobjectrecognitionandspeechproduction
AT mitsuhashitakumi intraandinterhemisphericnetworkdynamicssupportingobjectrecognitionandspeechproduction
AT firestoneethan intraandinterhemisphericnetworkdynamicssupportingobjectrecognitionandspeechproduction
AT uedariyo intraandinterhemisphericnetworkdynamicssupportingobjectrecognitionandspeechproduction
AT kambaratoshimune intraandinterhemisphericnetworkdynamicssupportingobjectrecognitionandspeechproduction
AT iwakihirotaka intraandinterhemisphericnetworkdynamicssupportingobjectrecognitionandspeechproduction
AT luataimeef intraandinterhemisphericnetworkdynamicssupportingobjectrecognitionandspeechproduction
AT marupudineenai intraandinterhemisphericnetworkdynamicssupportingobjectrecognitionandspeechproduction
AT soodsandeep intraandinterhemisphericnetworkdynamicssupportingobjectrecognitionandspeechproduction
AT asanoeishi intraandinterhemisphericnetworkdynamicssupportingobjectrecognitionandspeechproduction