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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...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Society for Neuroscience
2022
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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. |
format | Online Article Text |
id | pubmed-9744182 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Society for Neuroscience |
record_format | MEDLINE/PubMed |
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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