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Across the animal kingdom, neural responses in the auditory cortex are suppressed during vocalization, and humans are no exception. A common hypothesis is that suppression increases sensitivity to auditory feedback, enabling the detection of vocalization errors. This hypothesis has been previously confirmed in non-human primates, however a direct link between auditory suppression and sensitivity in human speech monitoring remains elusive. To address this issue, we obtained intracranial electroencephalography (iEEG) recordings from 35 neurosurgical participants during speech production. We first characterized the detailed topography of auditory suppression, which varied across superior temporal gyrus (STG). Next, we performed a delayed auditory feedback (DAF) task to determine whether the suppressed sites were also sensitive to auditory feedback alterations. Indeed, overlapping sites showed enhanced responses to feedback, indicating sensitivity. Importantly, there was a strong correlation between the degree of auditory suppression and feedback sensitivity, suggesting suppression might be a key mechanism that underlies speech monitoring. Further, we found that when participants produced speech with simultaneous auditory feedback, posterior STG was selectively activated if participants were engaged in a DAF paradigm, suggesting that increased attentional load can modulate auditory feedback sensitivity.
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A cortical network processes auditory error signals during human speech production to maintain fluency
Hearing one’s own voice is critical for fluent speech production as it allows for the detection and correction of vocalization errors in real time. This behavior known as the auditory feedback control of speech is impaired in various neurological disorders ranging from stuttering to aphasia; however, the underlying neural mechanisms are still poorly understood. Computational models of speech motor control suggest that, during speech production, the brain uses an efference copy of the motor command to generate an internal estimate of the speech output. When actual feedback differs from this internal estimate, an error signal is generated to correct the internal estimate and update necessary motor commands to produce intended speech. We were able to localize the auditory error signal using electrocorticographic recordings from neurosurgical participants during a delayed auditory feedback (DAF) paradigm. In this task, participants hear their voice with a time delay as they produced words and sentences (similar to an echo on a conference call), which is well known to disrupt fluency by causing slow and stutter-like speech in humans. We observed a significant response enhancement in auditory cortex that scaled with the duration of feedback delay, indicating an auditory speech error signal. Immediately following auditory cortex, dorsal precentral gyrus (dPreCG), a region that has not been implicated in auditory feedback processing before, exhibited a markedly similar response enhancement, suggesting a tight coupling between the 2 regions. Critically, response enhancement in dPreCG occurred only during articulation of long utterances due to a continuous mismatch between produced speech and reafferent feedback. These results suggest that dPreCG plays an essential role in processing auditory error signals during speech production to maintain fluency.
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- Award ID(s):
- 1912286
- PAR ID:
- 10487892
- Editor(s):
- Bizley, Jennifer K.
- Publisher / Repository:
- Plos Biology
- Date Published:
- Journal Name:
- PLOS Biology
- Volume:
- 20
- Issue:
- 2
- ISSN:
- 1545-7885
- Page Range / eLocation ID:
- e3001493
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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When we vocalize, our brain distinguishes self-generated sounds from external ones. A corollary discharge signal supports this function in animals; however, in humans, its exact origin and temporal dynamics remain unknown. We report electrocorticographic recordings in neurosurgical patients and a connectivity analysis framework based on Granger causality that reveals major neural communications. We find a reproducible source for corollary discharge across multiple speech production paradigms localized to the ventral speech motor cortex before speech articulation. The uncovered discharge predicts the degree of auditory cortex suppression during speech, its well-documented consequence. These results reveal the human corollary discharge source and timing with far-reaching implication for speech motor-control as well as auditory hallucinations in human psychosis.more » « less
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When we vocalize, our brain distinguishes self-generated sounds from external ones. A corollary discharge signal supports this function in animals, however, in humans its exact origin and temporal dynamics remain unknown. We report Electrocorticographic (ECoG) recordings in neurosurgical patients and a novel connectivity approach based on Granger-causality that reveals major neural communications. We find a reproducible source for corollary discharge across multiple speech production paradigms localized to ventral speech motor cortex before speech articulation. The uncovered discharge predicts the degree of auditory cortex suppression during speech, its well-documented consequence. These results reveal the human corollary discharge source and timing with far-reaching implication for speech motor-control as well as auditory hallucinations in human psychosis.more » « less
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Abstract Objective: Acoustic distortions to the speech signal impair spoken language recognition, but healthy listeners exhibit adaptive plasticity consistent with rapid adjustments in how the distorted speech input maps to speech representations, perhaps through engagement of supervised error-driven learning. This puts adaptive plasticity in speech perception in an interesting position with regard to developmental dyslexia inasmuch as dyslexia impacts speech processing and may involve dysfunction in neurobiological systems hypothesized to be involved in adaptive plasticity. Method: Here, we examined typical young adult listeners ( N = 17), and those with dyslexia ( N = 16), as they reported the identity of native-language monosyllabic spoken words to which signal processing had been applied to create a systematic acoustic distortion. During training, all participants experienced incremental signal distortion increases to mildly distorted speech along with orthographic and auditory feedback indicating word identity following response across a brief, 250-trial training block. During pretest and posttest phases, no feedback was provided to participants. Results: Word recognition across severely distorted speech was poor at pretest and equivalent across groups. Training led to improved word recognition for the most severely distorted speech at posttest, with evidence that adaptive plasticity generalized to support recognition of new tokens not previously experienced under distortion. However, training-related recognition gains for listeners with dyslexia were significantly less robust than for control listeners. Conclusions: Less efficient adaptive plasticity to speech distortions may impact the ability of individuals with dyslexia to deal with variability arising from sources like acoustic noise and foreign-accented speech.more » « less
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Purpose: Delayed auditory feedback (DAF) interferes with speech output. DAF causes distorted and disfluent productions and errors in the serial order of produced sounds. Although DAF has been studied extensively, the specific patterns of elicited speech errors are somewhat obscured by relatively small speech samples, differences across studies, and uncontrolled variables. The goal of this study was to characterize the types of serial order errors that increase under DAF in a systematic syllable sequence production task, which used a closed set of sounds and controlled for speech rate. Method: Sixteen adult speakers repeatedly produced CVCVCV (C = consonant, V = vowel) sequences, paced to a “visual metronome,” while hearing self-generated feedback with delays of 0–250 ms. Listeners transcribed recordings, and speech errors were classified based on the literature surrounding naturally occurring slips of the tongue. A series of mixed-effects models were used to assess the effects of delay for different error types, for error arrival time, and for speaking rate. Results: DAF had a significant effect on the overall error rate for delays of 100 ms or greater. Statistical models revealed significant effects (relative to zero delay) for vowel and syllable repetitions, vowel exchanges, vowel omissions, onset disfluencies, and distortions. Serial order errors were especially dominated by vowel and syllable repetitions. Errors occurred earlier on average within a trial for longer feedback delays. Although longer delays caused slower speech, this effect was mediated by the run number (time in the experiment) and small compared with those in previous studies. Conclusions: DAF drives a specific pattern of serial order errors. The dominant pattern of vowel and syllable repetition errors suggests possible mechanisms whereby DAF drives changes to the activity in speech planning representations, yielding errors. These mechanisms are outlined with reference to the GODIVA (Gradient Order Directions Into Velocities of Articulators) model of speech planning and production. Supplemental Material: https://doi.org/10.23641/asha.19601785more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pbio.3001493
