Mapping cortical activations underlying covert and overt language production using high-density diffuse optical tomography

Gold standard neuroimaging modalities such as functional magnetic resonance imaging (fMRI), positron emission tomography (PET), and more recently electrocorticography (ECoG) have provided profound insights regarding the neural mechanisms underlying the processing of language, but they are limited in...

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Main Authors: Mariel L. Schroeder, Arefeh Sherafati, Rachel L. Ulbrich, Muriah D. Wheelock, Alexandra M. Svoboda, Emma D. Klein, Tessa G. George, Kalyan Tripathy, Joseph P. Culver, Adam T. Eggebrecht
Format: Article
Language:English
Published: Elsevier 2023-08-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811923003415
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author Mariel L. Schroeder
Arefeh Sherafati
Rachel L. Ulbrich
Muriah D. Wheelock
Alexandra M. Svoboda
Emma D. Klein
Tessa G. George
Kalyan Tripathy
Joseph P. Culver
Adam T. Eggebrecht
author_facet Mariel L. Schroeder
Arefeh Sherafati
Rachel L. Ulbrich
Muriah D. Wheelock
Alexandra M. Svoboda
Emma D. Klein
Tessa G. George
Kalyan Tripathy
Joseph P. Culver
Adam T. Eggebrecht
author_sort Mariel L. Schroeder
collection DOAJ
description Gold standard neuroimaging modalities such as functional magnetic resonance imaging (fMRI), positron emission tomography (PET), and more recently electrocorticography (ECoG) have provided profound insights regarding the neural mechanisms underlying the processing of language, but they are limited in applications involving naturalistic language production especially in developing brains, during face-to-face dialogues, or as a brain-computer interface. High-density diffuse optical tomography (HD-DOT) provides high-fidelity mapping of human brain function with comparable spatial resolution to that of fMRI but in a silent and open scanning environment similar to real-life social scenarios. Therefore, HD-DOT has potential to be used in naturalistic settings where other neuroimaging modalities are limited. While HD-DOT has been previously validated against fMRI for mapping the neural correlates underlying language comprehension and covert (i.e., “silent”) language production, HD-DOT has not yet been established for mapping the cortical responses to overt (i.e., “out loud”) language production. In this study, we assessed the brain regions supporting a simple hierarchy of language tasks: silent reading of single words, covert production of verbs, and overt production of verbs in normal hearing right-handed native English speakers (n = 33). First, we found that HD-DOT brain mapping is resilient to movement associated with overt speaking. Second, we observed that HD-DOT is sensitive to key activations and deactivations in brain function underlying the perception and naturalistic production of language. Specifically, statistically significant results were observed that show recruitment of regions in occipital, temporal, motor, and prefrontal cortices across all three tasks after performing stringent cluster-extent based thresholding. Our findings lay the foundation for future HD-DOT studies of imaging naturalistic language comprehension and production during real-life social interactions and for broader applications such as presurgical language assessment and brain-machine interfaces.
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spelling doaj.art-25d78d70abc34dffa561970005c762762023-06-21T06:51:09ZengElsevierNeuroImage1095-95722023-08-01276120190Mapping cortical activations underlying covert and overt language production using high-density diffuse optical tomographyMariel L. Schroeder0Arefeh Sherafati1Rachel L. Ulbrich2Muriah D. Wheelock3Alexandra M. Svoboda4Emma D. Klein5Tessa G. George6Kalyan Tripathy7Joseph P. Culver8Adam T. Eggebrecht9Mallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO, USA; Department of Speech, Language, and Hearing Sciences, Purdue University, West Lafayette, IN, USAMallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO, USA; Department of Neurology, University of California, San Francisco, San Francisco, CA, USAMallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO, USA; University of Missouri School of Medicine, Columbia, MO, USAMallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO, USAMallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO, USA; University of Cincinnati Medical Center, Cincinnati, Oh, USAMallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO, USA; Icahn School of Medicine at Mount Sinai, New York, NY, USAMallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO, USAMallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO, USA; Washington University School of Medicine, St Louis, MO, USAMallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO, USA; Division of Biology & Biomedical Sciences, Washington University School of Medicine, St Louis, MO, USA; Department of Physics, Washington University in St. Louis, St Louis, MO, USA; Department of Biomedical Engineering, Washington University in St. Louis, St Louis, MO, USAMallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO, USA; Division of Biology & Biomedical Sciences, Washington University School of Medicine, St Louis, MO, USA; Department of Biomedical Engineering, Washington University in St. Louis, St Louis, MO, USA; Corresponding author at: Mallinckrodt Institute of Radiology; Washington University School of Medicine; 660 S. Euclid Ave, St Louis, MO 63110; USA.Gold standard neuroimaging modalities such as functional magnetic resonance imaging (fMRI), positron emission tomography (PET), and more recently electrocorticography (ECoG) have provided profound insights regarding the neural mechanisms underlying the processing of language, but they are limited in applications involving naturalistic language production especially in developing brains, during face-to-face dialogues, or as a brain-computer interface. High-density diffuse optical tomography (HD-DOT) provides high-fidelity mapping of human brain function with comparable spatial resolution to that of fMRI but in a silent and open scanning environment similar to real-life social scenarios. Therefore, HD-DOT has potential to be used in naturalistic settings where other neuroimaging modalities are limited. While HD-DOT has been previously validated against fMRI for mapping the neural correlates underlying language comprehension and covert (i.e., “silent”) language production, HD-DOT has not yet been established for mapping the cortical responses to overt (i.e., “out loud”) language production. In this study, we assessed the brain regions supporting a simple hierarchy of language tasks: silent reading of single words, covert production of verbs, and overt production of verbs in normal hearing right-handed native English speakers (n = 33). First, we found that HD-DOT brain mapping is resilient to movement associated with overt speaking. Second, we observed that HD-DOT is sensitive to key activations and deactivations in brain function underlying the perception and naturalistic production of language. Specifically, statistically significant results were observed that show recruitment of regions in occipital, temporal, motor, and prefrontal cortices across all three tasks after performing stringent cluster-extent based thresholding. Our findings lay the foundation for future HD-DOT studies of imaging naturalistic language comprehension and production during real-life social interactions and for broader applications such as presurgical language assessment and brain-machine interfaces.http://www.sciencedirect.com/science/article/pii/S1053811923003415High-density diffuse optical tomographyNaturalistic languageOvertCovertSpeechArticulation
spellingShingle Mariel L. Schroeder
Arefeh Sherafati
Rachel L. Ulbrich
Muriah D. Wheelock
Alexandra M. Svoboda
Emma D. Klein
Tessa G. George
Kalyan Tripathy
Joseph P. Culver
Adam T. Eggebrecht
Mapping cortical activations underlying covert and overt language production using high-density diffuse optical tomography
NeuroImage
High-density diffuse optical tomography
Naturalistic language
Overt
Covert
Speech
Articulation
title Mapping cortical activations underlying covert and overt language production using high-density diffuse optical tomography
title_full Mapping cortical activations underlying covert and overt language production using high-density diffuse optical tomography
title_fullStr Mapping cortical activations underlying covert and overt language production using high-density diffuse optical tomography
title_full_unstemmed Mapping cortical activations underlying covert and overt language production using high-density diffuse optical tomography
title_short Mapping cortical activations underlying covert and overt language production using high-density diffuse optical tomography
title_sort mapping cortical activations underlying covert and overt language production using high density diffuse optical tomography
topic High-density diffuse optical tomography
Naturalistic language
Overt
Covert
Speech
Articulation
url http://www.sciencedirect.com/science/article/pii/S1053811923003415
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