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Research ArticleResearch Article: New Research, Cognition and Behavior

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

Xiaodan Zheng, Hao Zhu, Siqi Li and Xing Tian
eNeuro 28 November 2022, 9 (6) ENEURO.0309-22.2022; https://doi.org/10.1523/ENEURO.0309-22.2022
Xiaodan Zheng
1Shanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, People’s Republic of China
2NYU-ECNU Institute of Brain and Cognitive Science, New York University Shanghai, Shanghai 200062, People’s Republic of China
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Hao Zhu
2NYU-ECNU Institute of Brain and Cognitive Science, New York University Shanghai, Shanghai 200062, People’s Republic of China
3Division of Arts and Sciences, New York University Shanghai, Shanghai 200122, People’s Republic of China
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Siqi Li
1Shanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, People’s Republic of China
2NYU-ECNU Institute of Brain and Cognitive Science, New York University Shanghai, Shanghai 200062, People’s Republic of China
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Xing Tian
1Shanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, People’s Republic of China
2NYU-ECNU Institute of Brain and Cognitive Science, New York University Shanghai, Shanghai 200062, People’s Republic of China
3Division of Arts and Sciences, New York University Shanghai, Shanghai 200122, People’s Republic of China
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  • Figure 1.
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    Figure 1.

    A schematic of the hypothesis about the generic inhibitory functions of CD. CD can be available as early as in the motor intention stage and throughout the entire course of action. CD inhibits sensory processing (demonstrated in blue). The inhibition function of CD could be nonspecific (generic) to all sounds at the beginning of the action course (motor intention) and becomes stronger and specific to the sensory consequences of actions. The generic inhibition function of CD may also depend on the established associations between actions and their sensory consequences—the strength of generic inhibition on the sensory process may depend on feature overlaps between feedback stimuli and the sensory representation that can be induced by actions performed by an agent. Specific in the auditory domain, the generic inhibition function of CD may suppress nonhuman sound less than for speech and nonspeech sounds that humans can produce, as indicated by the shorter blue bar in nonhuman sound.

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    Figure 2.

    Experimental paradigms, and behavioral and ERP results. A, Illustration of four types of trials. In GP trials, participants were asked to prepare to speak when two meaningless symbols were on screen. The symbols did not provide any information about what participants were going to say, and hence they generally prepare the action of speaking. An auditory probe (randomly selected from a syllable/ba/, a cough sound, and a 500 Hz pure tone) was presented at the end of the preparation stage to probe the modulatory effect of CD on auditory processes. When a green visual cue appeared, participants were asked to articulate accordingly. The visual cue “ba” is used as an example for illustration purposes; two other visual cues were included for producing cough and humming tone. GPNS trials were identical to GP trials except that no auditory probe was presented during the preparation stage. In NP trials, participants performed the articulation task without preceding preparation. GPNS and NP trials were used to control and quantify the general preparation. In the PL trials, participants were asked to passively listen to the auditory probes that were identical to those in GP trials. No preparation or articulation task was required in the PL trials. The PL trials were used to compare with auditory responses in GP trials to quantify the neural modulation effects of preparation (for details, see Materials and Methods) B, Mean RTs across three conditions with individual data. Participants articulated faster in GP and GPNS conditions than in NP condition, but no difference between GP and GPNS conditions, suggesting that the performance of general preparation was independent of the auditory probes. Error bars indicate ±SEM. ***p < 0.001. C, Grand average GFP waveforms and topographic responses for three types of auditory probes combined. Auditory N1 and P2 components were observed in each condition. Yellow and blue represent GP and PL conditions, respectively. Individual waveform responses are superimposed on the plot. D, Mean N1 and P2 amplitudes in two conditions with individual data. The magnitude of the P2 component was significantly smaller in GP than that in PL, suggesting that general preparation suppressed the auditory responses. Error bars indicate ±SEM. *p < 0.05.

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    Figure 3.

    Grand average ERP responses to auditory probes in the representative channel of Cz. The waveform responses are in the left column, and the N1/P2 component responses are in the right column in each panel. A–D, Responses to syllable (A), cough (B), tone (C), and the average across three types of sounds (D), respectively. Individual data are superimposed on each plot. Yellow and blue represent GP and PL conditions, respectively. Error bars indicate ±SEM. **p < 0.01, ***p < 0.001.

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    Figure 4.

    The results of spatiotemporal analysis on ERP responses. Each column indicates the results for syllable, cough, and tone, respectively. A, The results of the spatiotemporal analysis. The x-axis represents time relative to the auditory probe onset at 0 ms, and the y-axis represents each of the 32 electrodes. The grayscale in the background represents t values comparing the ERP responses between GP and PL conditions (GP minus PL). Yellow and green indicate significant clusters with positive and negative t values, respectively. B, Topographic representation of the significant spatiotemporal clusters in A and the raw ERP topographies that derived the significant cluster results. Each topography in the first row represents averaged t values across the time interval of each significant cluster in A, indicated by corresponding color dashed lines. The black squares on the topographies indicate the significant electrodes in the cluster. The second and third rows are the topographies of averaged ERP responses across the corresponding time interval of the cluster in the PL and GP, respectively. The black squares on the ERP topographies label the same electrodes in the corresponding significant cluster above. Considering the polarity of ERP responses, the clusters observed in typical latency of auditory responses (100–200 ms after stimuli onset) showed inhibition effects of general preparation on all types of auditory probes—the ERP amplitudes in GP were smaller than those in PL (less positive or less negative in electrodes of positive or negative ERP responses, respectively). C, The summarized results of three ERP clusters with individual data extracted using the group-level clusters as a spatial-temporal filter. To better compare the suppression effect of GP in each sound, the sum of ERP data in a similar cluster of frontal-temporal distribution was presented for each sound. Error bars indicate ±SEM. *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001.

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    Figure 5.

    Results of spatiotemporal cluster analysis in the delta frequency band (1–3 Hz) and the theta frequency band (4–8 Hz) for each type of auditory probe, separately for ITC and power. Each column indicates the results for syllable, cough, and tone, respectively. The grayscale images represent t values in each of the 32 electrodes across time, obtained by comparing the ITC or power between GP and PL conditions (GP minus PL). The yellow and green indicate clusters with positive and negative t values and hence enhancement and suppression effects, respectively. Topographies of averaged t values are plotted every 50 ms from −100 to 300 ms when the significant clusters were observed. Significant electrodes in each cluster are marked with black squares on each topography. A, Results in the delta frequency band. The ITC results are presented in the top row. For syllable, two significant clusters were found. Topographies of the first clusters in yellow, spanning from −100 to 200 ms, are shown at the top of the spatiotemporal plots. Significant electrodes in this cluster were mostly located in parietal regions, and some were extended to frontal regions. Topographies of the second cluster in green, spanning from 100 to 300 ms, are shown at the bottom of the spatiotemporal plots. Significant electrodes in this cluster were located in central regions. For cough and tone, one significant cluster in green was found, similar to the second cluster in the results of syllable. Power results are presented in the bottom row. For syllable, one significant cluster was found. For tone, two significant clusters were found. No significant cluster was found in the results of cough. B, Results in the theta frequency band. The top row shows ITC results in the theta band. For syllable and tone, one significant cluster in yellow was found. For cough, two significant clusters were found, which is similar to the results of syllable in the delta band. The bottom row shows the power results in the theta band. For syllable, one significant cluster in yellow was found. For cough, one significant cluster in green was found. For tone, no significant cluster was found.

  • Figure 6.
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    Figure 6.

    Results of spatiotemporal cluster analysis in one lower-frequency band (1–8 Hz) for each type of auditory probe, separately for ITC and power. Each column indicates the results for syllable, cough, and tone, respectively. The grayscale images represent t values in each of the 32 electrodes across time, obtained by comparing the ITC or power between GP and PL conditions (GP minus PL). The yellow and green indicate clusters with positive and negative t values and hence enhancement and suppression effects, respectively. Topographies of averaged t values are plotted every 50 ms from −100 to 300 ms when the significant clusters were observed. Significant electrodes in each cluster are marked with black squares on each topography. A, ITC results. For each auditory probe, two significant clusters were found. Topographies of the first clusters in yellow, spanning from −100 to 100 ms (for syllable, to 200 ms), are shown at the top of the spatiotemporal plots. Significant electrodes in this cluster were mostly located in parietal regions, and some extended to frontal regions. Topographies of the second cluster in green, spanning from 100 to 300 ms, are shown at the bottom of the spatiotemporal plots. Significant electrodes in this cluster were located in central regions. The summarized results of two ITC clusters of each sound with individual data superimposed are presented at the top and bottom near each cluster separately. B, Power results. For each auditory probe, one significant cluster was found. The clusters were observed from 100 to 300 ms after sound onset in central regions. The summarized results of the power cluster with individual data superimposed are presented at the bottom near each cluster. Error bars indicate ±SEM. **p < 0.01, ***p < 0.001, ****p < 0.0001.

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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
Xiaodan Zheng, Hao Zhu, Siqi Li, Xing Tian
eNeuro 28 November 2022, 9 (6) ENEURO.0309-22.2022; DOI: 10.1523/ENEURO.0309-22.2022

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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
Xiaodan Zheng, Hao Zhu, Siqi Li, Xing Tian
eNeuro 28 November 2022, 9 (6) ENEURO.0309-22.2022; DOI: 10.1523/ENEURO.0309-22.2022
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Keywords

  • action-induced sensory suppression
  • agency
  • internal forward model
  • motor control
  • sensorimotor integration

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