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The Generic Inhibitory Function of Corollary Discharge in Motor Intention: Evidence from the Modulation Effects of Speech Preparation on the Late Components of Auditory Neural Responses

The importance of action–perception loops necessitates efficient computations linking motor and sensory systems. Corollary discharge (CD), a concept in motor-to-sensory transformation, has been proposed to predict the sensory consequences of actions for efficient motor and cognitive control. The pre...

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Autores principales: Zheng, Xiaodan, Zhu, Hao, Li, Siqi, Tian, Xing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9744182/
https://www.ncbi.nlm.nih.gov/pubmed/36443007
http://dx.doi.org/10.1523/ENEURO.0309-22.2022
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author Zheng, Xiaodan
Zhu, Hao
Li, Siqi
Tian, Xing
author_facet Zheng, Xiaodan
Zhu, Hao
Li, Siqi
Tian, Xing
author_sort Zheng, Xiaodan
collection PubMed
description The importance of action–perception loops necessitates efficient computations linking motor and sensory systems. Corollary discharge (CD), a concept in motor-to-sensory transformation, has been proposed to predict the sensory consequences of actions for efficient motor and cognitive control. The predictive computation has been assumed to realize via inhibiting sensory reafference when actions are executed. Continuous control throughout the course of action demands inhibitory function ubiquitously on all potential reafference when sensory consequences are not available before execution. However, the temporal and functional characteristics of CD are unclear. When does CD begin to operate? To what extent does CD inhibit sensory processes? How is the inhibitory function implemented in neural computation? Using a delayed articulation paradigm with three types of auditory probes (speech, nonspeech, and nonhuman sounds) in an electroencephalography experiment with 20 human participants (7 males), we found that preparing to speak without knowing what to say (general preparation) suppressed neural responses to each type of auditory probe, suggesting a generic inhibitory function of CD in motor intention. Moreover, power and phase coherence in low-frequency bands (1–8 Hz) were both suppressed, indicating that inhibition was mediated by dampening response amplitude and adding temporal variance to sensory processes. Furthermore, inhibition was stronger for sounds that humans can produce than nonhuman sounds, hinting that the generic inhibitory function of CD is regulated by the established motor–sensory associations. These results suggest a functional and temporal granularity of corollary discharge that mediates multifaceted computations in motor and cognitive control.
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spelling pubmed-97441822022-12-13 The Generic Inhibitory Function of Corollary Discharge in Motor Intention: Evidence from the Modulation Effects of Speech Preparation on the Late Components of Auditory Neural Responses Zheng, Xiaodan Zhu, Hao Li, Siqi Tian, Xing eNeuro Research Article: New Research The importance of action–perception loops necessitates efficient computations linking motor and sensory systems. Corollary discharge (CD), a concept in motor-to-sensory transformation, has been proposed to predict the sensory consequences of actions for efficient motor and cognitive control. The predictive computation has been assumed to realize via inhibiting sensory reafference when actions are executed. Continuous control throughout the course of action demands inhibitory function ubiquitously on all potential reafference when sensory consequences are not available before execution. However, the temporal and functional characteristics of CD are unclear. When does CD begin to operate? To what extent does CD inhibit sensory processes? How is the inhibitory function implemented in neural computation? Using a delayed articulation paradigm with three types of auditory probes (speech, nonspeech, and nonhuman sounds) in an electroencephalography experiment with 20 human participants (7 males), we found that preparing to speak without knowing what to say (general preparation) suppressed neural responses to each type of auditory probe, suggesting a generic inhibitory function of CD in motor intention. Moreover, power and phase coherence in low-frequency bands (1–8 Hz) were both suppressed, indicating that inhibition was mediated by dampening response amplitude and adding temporal variance to sensory processes. Furthermore, inhibition was stronger for sounds that humans can produce than nonhuman sounds, hinting that the generic inhibitory function of CD is regulated by the established motor–sensory associations. These results suggest a functional and temporal granularity of corollary discharge that mediates multifaceted computations in motor and cognitive control. Society for Neuroscience 2022-12-07 /pmc/articles/PMC9744182/ /pubmed/36443007 http://dx.doi.org/10.1523/ENEURO.0309-22.2022 Text en Copyright © 2022 Zheng et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article: New Research
Zheng, Xiaodan
Zhu, Hao
Li, Siqi
Tian, Xing
The Generic Inhibitory Function of Corollary Discharge in Motor Intention: Evidence from the Modulation Effects of Speech Preparation on the Late Components of Auditory Neural Responses
title The Generic Inhibitory Function of Corollary Discharge in Motor Intention: Evidence from the Modulation Effects of Speech Preparation on the Late Components of Auditory Neural Responses
title_full The Generic Inhibitory Function of Corollary Discharge in Motor Intention: Evidence from the Modulation Effects of Speech Preparation on the Late Components of Auditory Neural Responses
title_fullStr The Generic Inhibitory Function of Corollary Discharge in Motor Intention: Evidence from the Modulation Effects of Speech Preparation on the Late Components of Auditory Neural Responses
title_full_unstemmed The Generic Inhibitory Function of Corollary Discharge in Motor Intention: Evidence from the Modulation Effects of Speech Preparation on the Late Components of Auditory Neural Responses
title_short The Generic Inhibitory Function of Corollary Discharge in Motor Intention: Evidence from the Modulation Effects of Speech Preparation on the Late Components of Auditory Neural Responses
title_sort generic inhibitory function of corollary discharge in motor intention: evidence from the modulation effects of speech preparation on the late components of auditory neural responses
topic Research Article: New Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9744182/
https://www.ncbi.nlm.nih.gov/pubmed/36443007
http://dx.doi.org/10.1523/ENEURO.0309-22.2022
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