Coupled versus decoupled visuomotor feedback: Differential frontoparietal activity during curved reach planning on simultaneous functional near‐infrared spectroscopy and electroencephalography

Abstract Introduction Interacting with the environment requires the planning and execution of reach‐to‐target movements along given reach trajectory paths. Human neural mechanisms for the motor planning of linear, or point‐to‐point, reaching movements are relatively well studied. However, the corres...

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Main Authors: Duc Trung Le, Hiroki Ogawa, Masato Tsuyuhara, Kazuki Watanabe, Tatsunori Watanabe, Ryosuke Ochi, Hisao Nishijo, Masahito Mihara, Naoto Fujita, Susumu Urakawa
Format: Article
Language:English
Published: Wiley 2022-07-01
Series:Brain and Behavior
Subjects:
Online Access:https://doi.org/10.1002/brb3.2681
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author Duc Trung Le
Hiroki Ogawa
Masato Tsuyuhara
Kazuki Watanabe
Tatsunori Watanabe
Ryosuke Ochi
Hisao Nishijo
Masahito Mihara
Naoto Fujita
Susumu Urakawa
author_facet Duc Trung Le
Hiroki Ogawa
Masato Tsuyuhara
Kazuki Watanabe
Tatsunori Watanabe
Ryosuke Ochi
Hisao Nishijo
Masahito Mihara
Naoto Fujita
Susumu Urakawa
author_sort Duc Trung Le
collection DOAJ
description Abstract Introduction Interacting with the environment requires the planning and execution of reach‐to‐target movements along given reach trajectory paths. Human neural mechanisms for the motor planning of linear, or point‐to‐point, reaching movements are relatively well studied. However, the corresponding representations for curved and more complex reaching movements require further investigation. Additionally, the visual and proprioceptive feedback of hand positioning can be spatially and sequentially coupled in alignment (e.g., directly reaching for an object), termed coupled visuomotor feedback, or spatially decoupled (e.g., dragging the computer mouse forward to move the cursor upward), termed decoupled visuomotor feedback. During reach planning, visuomotor processing routes may differ across feedback types. Methods We investigated the involvement of the frontoparietal regions, including the superior parietal lobule (SPL), dorsal premotor cortex (PMd), and dorsolateral prefrontal cortex (dlPFC), in curved reach planning under different feedback conditions. Participants engaged in two delayed‐response reaching tasks with identical starting and target position sets but different reach trajectory paths (linear or curved) under two feedback conditions (coupled or decoupled). Neural responses in frontoparietal regions were analyzed using a combination of functional near‐infrared spectroscopy and electroencephalography. Results The results revealed that, regarding the cue period, curved reach planning had a higher hemodynamic response in the left SPL and bilateral PMd and a smaller high‐beta power in the left parietal regions than linear reach planning. Regarding the delay period, higher hemodynamic responses during curved reach planning were observed in the right dlPFC for decoupled feedback than those for coupled feedback. Conclusion These findings suggest the crucial involvement of both SPL and PMd activities in trajectory‐path processing for curved reach planning. Moreover, the dlPFC may be especially involved in the planning of curved reaching movements under decoupled feedback conditions. Thus, this study provides insight into the neural mechanisms underlying reaching function via different feedback conditions.
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spelling doaj.art-b5ed27aeced84527a05de0b525171edf2022-12-22T03:04:10ZengWileyBrain and Behavior2162-32792022-07-01127n/an/a10.1002/brb3.2681Coupled versus decoupled visuomotor feedback: Differential frontoparietal activity during curved reach planning on simultaneous functional near‐infrared spectroscopy and electroencephalographyDuc Trung Le0Hiroki Ogawa1Masato Tsuyuhara2Kazuki Watanabe3Tatsunori Watanabe4Ryosuke Ochi5Hisao Nishijo6Masahito Mihara7Naoto Fujita8Susumu Urakawa9Department of Musculoskeletal Functional Research and Regeneration, Graduate School of Biomedical and Health Sciences Hiroshima University Hiroshima JapanDepartment of Musculoskeletal Functional Research and Regeneration, Graduate School of Biomedical and Health Sciences Hiroshima University Hiroshima JapanDepartment of Musculoskeletal Functional Research and Regeneration, Graduate School of Biomedical and Health Sciences Hiroshima University Hiroshima JapanDepartment of Musculoskeletal Functional Research and Regeneration, Graduate School of Biomedical and Health Sciences Hiroshima University Hiroshima JapanDepartment of Sensorimotor Neuroscience, Graduate School of Biomedical and Health Sciences Hiroshima University Hiroshima JapanDepartment of Musculoskeletal Functional Research and Regeneration, Graduate School of Biomedical and Health Sciences Hiroshima University Hiroshima JapanDepartment of System Emotional Science, Graduate School of Medicine and Pharmaceutical Science University of Toyama Toyama JapanDepartment of Neurology Kawasaki Medical School Okayama JapanDepartment of Musculoskeletal Functional Research and Regeneration, Graduate School of Biomedical and Health Sciences Hiroshima University Hiroshima JapanDepartment of Musculoskeletal Functional Research and Regeneration, Graduate School of Biomedical and Health Sciences Hiroshima University Hiroshima JapanAbstract Introduction Interacting with the environment requires the planning and execution of reach‐to‐target movements along given reach trajectory paths. Human neural mechanisms for the motor planning of linear, or point‐to‐point, reaching movements are relatively well studied. However, the corresponding representations for curved and more complex reaching movements require further investigation. Additionally, the visual and proprioceptive feedback of hand positioning can be spatially and sequentially coupled in alignment (e.g., directly reaching for an object), termed coupled visuomotor feedback, or spatially decoupled (e.g., dragging the computer mouse forward to move the cursor upward), termed decoupled visuomotor feedback. During reach planning, visuomotor processing routes may differ across feedback types. Methods We investigated the involvement of the frontoparietal regions, including the superior parietal lobule (SPL), dorsal premotor cortex (PMd), and dorsolateral prefrontal cortex (dlPFC), in curved reach planning under different feedback conditions. Participants engaged in two delayed‐response reaching tasks with identical starting and target position sets but different reach trajectory paths (linear or curved) under two feedback conditions (coupled or decoupled). Neural responses in frontoparietal regions were analyzed using a combination of functional near‐infrared spectroscopy and electroencephalography. Results The results revealed that, regarding the cue period, curved reach planning had a higher hemodynamic response in the left SPL and bilateral PMd and a smaller high‐beta power in the left parietal regions than linear reach planning. Regarding the delay period, higher hemodynamic responses during curved reach planning were observed in the right dlPFC for decoupled feedback than those for coupled feedback. Conclusion These findings suggest the crucial involvement of both SPL and PMd activities in trajectory‐path processing for curved reach planning. Moreover, the dlPFC may be especially involved in the planning of curved reaching movements under decoupled feedback conditions. Thus, this study provides insight into the neural mechanisms underlying reaching function via different feedback conditions.https://doi.org/10.1002/brb3.2681EEGfeedbackfNIRSfrontoparietal cortexreach planningvisuomotor transformation
spellingShingle Duc Trung Le
Hiroki Ogawa
Masato Tsuyuhara
Kazuki Watanabe
Tatsunori Watanabe
Ryosuke Ochi
Hisao Nishijo
Masahito Mihara
Naoto Fujita
Susumu Urakawa
Coupled versus decoupled visuomotor feedback: Differential frontoparietal activity during curved reach planning on simultaneous functional near‐infrared spectroscopy and electroencephalography
Brain and Behavior
EEG
feedback
fNIRS
frontoparietal cortex
reach planning
visuomotor transformation
title Coupled versus decoupled visuomotor feedback: Differential frontoparietal activity during curved reach planning on simultaneous functional near‐infrared spectroscopy and electroencephalography
title_full Coupled versus decoupled visuomotor feedback: Differential frontoparietal activity during curved reach planning on simultaneous functional near‐infrared spectroscopy and electroencephalography
title_fullStr Coupled versus decoupled visuomotor feedback: Differential frontoparietal activity during curved reach planning on simultaneous functional near‐infrared spectroscopy and electroencephalography
title_full_unstemmed Coupled versus decoupled visuomotor feedback: Differential frontoparietal activity during curved reach planning on simultaneous functional near‐infrared spectroscopy and electroencephalography
title_short Coupled versus decoupled visuomotor feedback: Differential frontoparietal activity during curved reach planning on simultaneous functional near‐infrared spectroscopy and electroencephalography
title_sort coupled versus decoupled visuomotor feedback differential frontoparietal activity during curved reach planning on simultaneous functional near infrared spectroscopy and electroencephalography
topic EEG
feedback
fNIRS
frontoparietal cortex
reach planning
visuomotor transformation
url https://doi.org/10.1002/brb3.2681
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