Auditory-motor learning during speech production in 9-11-year-old children

Background

Hearing ability is essential for normal speech development, however the precise mechanisms linking auditory input and the improvement of speaking ability remain poorly understood. Auditory feedback during speech production is believed to play a critical role by providing the nervous system with information about speech outcomes that is used to learn and subsequently fine-tune speech motor output. Surprisingly, few studies have directly investigated such auditory-motor learning in the speech production of typically developing children.

Methodology/Principal Findings

In the present study, we manipulated auditory feedback during speech production in a group of 9–11-year old children, as well as in adults. Following a period of speech practice under conditions of altered auditory feedback, compensatory changes in speech production and perception were examined. Consistent with prior studies, the adults exhibited compensatory changes in both their speech motor output and their perceptual representations of speech sound categories. The children exhibited compensatory changes in the motor domain, with a change in speech output that was similar in magnitude to that of the adults, however the children showed no reliable compensatory effect on their perceptual representations.

Conclusions

The results indicate that 9–11-year-old children, whose speech motor and perceptual abilities are still not fully developed, are nonetheless capable of auditory-feedback-based sensorimotor adaptation, supporting a role for such learning processes in speech motor development. Auditory feedback may play a more limited role, however, in the fine-tuning of children''s perceptual representations of speech sound categories.     

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.

Hearing one’s own voice is critical for fluent speech production, allowing detection and correction of vocalization errors in real-time. This study shows that the dorsal precentral gyrus is a critical component of a cortical network that monitors auditory feedback to produce fluent speech; this region is engaged specifically when speech production is effortful during articulation of long utterances.     

Attentional Demands Influence Vocal Compensations to Pitch Errors Heard in Auditory Feedback

Auditory feedback is required to maintain fluent speech. At present, it is unclear how attention modulates auditory feedback processing during ongoing speech. In this event-related potential (ERP) study, participants vocalized/a/, while they heard their vocal pitch suddenly shifted downward a ½ semitone in both single and dual-task conditions. During the single-task condition participants passively viewed a visual stream for cues to start and stop vocalizing. In the dual-task condition, participants vocalized while they identified target stimuli in a visual stream of letters. The presentation rate of the visual stimuli was manipulated in the dual-task condition in order to produce a low, intermediate, and high attentional load. Visual target identification accuracy was lowest in the high attentional load condition, indicating that attentional load was successfully manipulated. Results further showed that participants who were exposed to the single-task condition, prior to the dual-task condition, produced larger vocal compensations during the single-task condition. Thus, when participants’ attention was divided, less attention was available for the monitoring of their auditory feedback, resulting in smaller compensatory vocal responses. However, P1-N1-P2 ERP responses were not affected by divided attention, suggesting that the effect of attentional load was not on the auditory processing of pitch altered feedback, but instead it interfered with the integration of auditory and motor information, or motor control itself.     

Remapping auditory-motor representations in voice production

Evidence regarding visually guided limb movements suggests that the motor system learns and maintains neural maps between motor commands and sensory feedback. Such systems are hypothesized to be used in a feed-forward control strategy that permits precision and stability without the delays of direct feedback control. Human vocalizations involve precise control over vocal and respiratory muscles. However, little is known about the sensorimotor representations underlying speech production. Here, we manipulated the heard fundamental frequency of the voice during speech to demonstrate learning of auditory-motor maps. Mandarin speakers repeatedly produced words with specific pitch patterns (tone categories). On each successive utterance, the frequency of their auditory feedback was increased by 1/100 of a semitone until they heard their feedback one full semitone above their true pitch. Subjects automatically compensated for these changes by lowering their vocal pitch. When feedback was unexpectedly returned to normal, speakers significantly increased the pitch of their productions beyond their initial baseline frequency. This adaptation was found to generalize to the production of another tone category. However, results indicate that a more robust adaptation was produced for the tone that was spoken during feedback alteration. The immediate aftereffects suggest a global remapping of the auditory-motor relationship after an extremely brief training period. However, this learning does not represent a complete transformation of the mapping; rather, it is in part target dependent.     

An Adapting Auditory-motor Feedback Loop Can Contribute to Generating Vocal Repetition

Consecutive repetition of actions is common in behavioral sequences. Although integration of sensory feedback with internal motor programs is important for sequence generation, if and how feedback contributes to repetitive actions is poorly understood. Here we study how auditory feedback contributes to generating repetitive syllable sequences in songbirds. We propose that auditory signals provide positive feedback to ongoing motor commands, but this influence decays as feedback weakens from response adaptation during syllable repetitions. Computational models show that this mechanism explains repeat distributions observed in Bengalese finch song. We experimentally confirmed two predictions of this mechanism in Bengalese finches: removal of auditory feedback by deafening reduces syllable repetitions; and neural responses to auditory playback of repeated syllable sequences gradually adapt in sensory-motor nucleus HVC. Together, our results implicate a positive auditory-feedback loop with adaptation in generating repetitive vocalizations, and suggest sensory adaptation is important for feedback control of motor sequences.     

Impairment of auditory-motor timing and compensatory reorganization after ventral premotor cortex stimulation

Integrating auditory and motor information often requires precise timing as in speech and music. In humans, the position of the ventral premotor cortex (PMv) in the dorsal auditory stream renders this area a node for auditory-motor integration. Yet, it remains unknown whether the PMv is critical for auditory-motor timing and which activity increases help to preserve task performance following its disruption. 16 healthy volunteers participated in two sessions with fMRI measured at baseline and following rTMS (rTMS) of either the left PMv or a control region. Subjects synchronized left or right finger tapping to sub-second beat rates of auditory rhythms in the experimental task, and produced self-paced tapping during spectrally matched auditory stimuli in the control task. Left PMv rTMS impaired auditory-motor synchronization accuracy in the first sub-block following stimulation (p<0.01, Bonferroni corrected), but spared motor timing and attention to task. Task-related activity increased in the homologue right PMv, but did not predict the behavioral effect of rTMS. In contrast, anterior midline cerebellum revealed most pronounced activity increase in less impaired subjects. The present findings suggest a critical role of the left PMv in feed-forward computations enabling accurate auditory-motor timing, which can be compensated by activity modulations in the cerebellum, but not in the homologue region contralateral to stimulation.     

The sensory consequences of speaking: parametric neural cancellation during speech in auditory cortex

When we speak, we provide ourselves with auditory speech input. Efficient monitoring of speech is often hypothesized to depend on matching the predicted sensory consequences from internal motor commands (forward model) with actual sensory feedback. In this paper we tested the forward model hypothesis using functional Magnetic Resonance Imaging. We administered an overt picture naming task in which we parametrically reduced the quality of verbal feedback by noise masking. Presentation of the same auditory input in the absence of overt speech served as listening control condition. Our results suggest that a match between predicted and actual sensory feedback results in inhibition of cancellation of auditory activity because speaking with normal unmasked feedback reduced activity in the auditory cortex compared to listening control conditions. Moreover, during self-generated speech, activation in auditory cortex increased as the feedback quality of the self-generated speech decreased. We conclude that during speaking early auditory cortex is involved in matching external signals with an internally generated model or prediction of sensory consequences, the locus of which may reside in auditory or higher order brain areas. Matching at early auditory cortex may provide a very sensitive monitoring mechanism that highlights speech production errors at very early levels of processing and may efficiently determine the self-agency of speech input.     

Somatosensory precision in speech production

Speech production is dependent on both auditory and somatosensory feedback. Although audition may appear to be the dominant sensory modality in speech production, somatosensory information plays a role that extends from brainstem responses to cortical control. Accordingly, the motor commands that underlie speech movements may have somatosensory as well as auditory goals. Here we provide evidence that, independent of the acoustics, somatosensory information is central to achieving the precision requirements of speech movements. We were able to dissociate auditory and somatosensory feedback by using a robotic device that altered the jaw's motion path, and hence proprioception, without affecting speech acoustics. The loads were designed to target either the consonant- or vowel-related portion of an utterance because these are the major sound categories in speech. We found that, even in the absence of any effect on the acoustics, with learning subjects corrected to an equal extent for both kinds of loads. This finding suggests that there are comparable somatosensory precision requirements for both kinds of speech sounds. We provide experimental evidence that the neural control of stiffness or impedance--the resistance to displacement--provides for somatosensory precision in speech production.     

Feel what you say: an auditory effect on somatosensory perception

In the present study, we demonstrate an audiotactile effect in which amplitude modulation of auditory feedback during voiced speech induces a throbbing sensation over the lip and laryngeal regions. Control tasks coupled with the examination of speech acoustic parameters allow us to rule out the possibility that the effect may have been due to cognitive factors or motor compensatory effects. We interpret the effect as reflecting the tight interplay between auditory and tactile modalities during vocal production.     

Temporal recalibration in vocalization induced by adaptation of delayed auditory feedback

Background

We ordinarily perceive our voice sound as occurring simultaneously with vocal production, but the sense of simultaneity in vocalization can be easily interrupted by delayed auditory feedback (DAF). DAF causes normal people to have difficulty speaking fluently but helps people with stuttering to improve speech fluency. However, the underlying temporal mechanism for integrating the motor production of voice and the auditory perception of vocal sound remains unclear. In this study, we investigated the temporal tuning mechanism integrating vocal sensory and voice sounds under DAF with an adaptation technique.

Methods and Findings

Participants produced a single voice sound repeatedly with specific delay times of DAF (0, 66, 133 ms) during three minutes to induce ‘Lag Adaptation’. They then judged the simultaneity between motor sensation and vocal sound given feedback. We found that lag adaptation induced a shift in simultaneity responses toward the adapted auditory delays. This indicates that the temporal tuning mechanism in vocalization can be temporally recalibrated after prolonged exposure to delayed vocal sounds. Furthermore, we found that the temporal recalibration in vocalization can be affected by averaging delay times in the adaptation phase.

Conclusions

These findings suggest vocalization is finely tuned by the temporal recalibration mechanism, which acutely monitors the integration of temporal delays between motor sensation and vocal sound.     

Sensorimotor integration in speech processing: computational basis and neural organization

Sensorimotor integration is an active domain of speech research and is characterized by two main ideas, that the auditory system is critically involved in speech production and that the motor system is critically involved in speech perception. Despite the complementarity of these ideas, there is little crosstalk between these literatures. We propose an integrative model of the speech-related "dorsal stream" in which sensorimotor interaction primarily supports speech production, in the form of a state feedback control architecture. A critical component of this control system is forward sensory prediction, which affords a natural mechanism for limited motor influence on perception, as recent perceptual research has suggested. Evidence shows that this influence is modulatory but not necessary for speech perception. The neuroanatomy of the proposed circuit is discussed as well as some probable clinical correlates including conduction aphasia, stuttering, and aspects of schizophrenia.     

Speech Misperception: Speaking and Seeing Interfere Differently with Hearing

Speech perception is thought to be linked to speech motor production. This linkage is considered to mediate multimodal aspects of speech perception, such as audio-visual and audio-tactile integration. However, direct coupling between articulatory movement and auditory perception has been little studied. The present study reveals a clear dissociation between the effects of a listener’s own speech action and the effects of viewing another’s speech movements on the perception of auditory phonemes. We assessed the intelligibility of the syllables [pa], [ta], and [ka] when listeners silently and simultaneously articulated syllables that were congruent/incongruent with the syllables they heard. The intelligibility was compared with a condition where the listeners simultaneously watched another’s mouth producing congruent/incongruent syllables, but did not articulate. The intelligibility of [ta] and [ka] were degraded by articulating [ka] and [ta] respectively, which are associated with the same primary articulator (tongue) as the heard syllables. But they were not affected by articulating [pa], which is associated with a different primary articulator (lips) from the heard syllables. In contrast, the intelligibility of [ta] and [ka] was degraded by watching the production of [pa]. These results indicate that the articulatory-induced distortion of speech perception occurs in an articulator-specific manner while visually induced distortion does not. The articulator-specific nature of the auditory-motor interaction in speech perception suggests that speech motor processing directly contributes to our ability to hear speech.     

Resting-state brain activity in adult males who stutter

Although developmental stuttering has been extensively studied with structural and task-based functional magnetic resonance imaging (fMRI), few studies have focused on resting-state brain activity in this disorder. We investigated resting-state brain activity of stuttering subjects by analyzing the amplitude of low-frequency fluctuation (ALFF), region of interest (ROI)-based functional connectivity (FC) and independent component analysis (ICA)-based FC. Forty-four adult males with developmental stuttering and 46 age-matched fluent male controls were scanned using resting-state fMRI. ALFF, ROI-based FCs and ICA-based FCs were compared between male stuttering subjects and fluent controls in a voxel-wise manner. Compared with fluent controls, stuttering subjects showed increased ALFF in left brain areas related to speech motor and auditory functions and bilateral prefrontal cortices related to cognitive control. However, stuttering subjects showed decreased ALFF in the left posterior language reception area and bilateral non-speech motor areas. ROI-based FC analysis revealed decreased FC between the posterior language area involved in the perception and decoding of sensory information and anterior brain area involved in the initiation of speech motor function, as well as increased FC within anterior or posterior speech- and language-associated areas and between the prefrontal areas and default-mode network (DMN) in stuttering subjects. ICA showed that stuttering subjects had decreased FC in the DMN and increased FC in the sensorimotor network. Our findings support the concept that stuttering subjects have deficits in multiple functional systems (motor, language, auditory and DMN) and in the connections between them.     

LaDIVA: A neurocomputational model providing laryngeal motor control for speech acquisition and production

Many voice disorders are the result of intricate neural and/or biomechanical impairments that are poorly understood. The limited knowledge of their etiological and pathophysiological mechanisms hampers effective clinical management. Behavioral studies have been used concurrently with computational models to better understand typical and pathological laryngeal motor control. Thus far, however, a unified computational framework that quantitatively integrates physiologically relevant models of phonation with the neural control of speech has not been developed. Here, we introduce LaDIVA, a novel neurocomputational model with physiologically based laryngeal motor control. We combined the DIVA model (an established neural network model of speech motor control) with the extended body-cover model (a physics-based vocal fold model). The resulting integrated model, LaDIVA, was validated by comparing its model simulations with behavioral responses to perturbations of auditory vocal fundamental frequency (f_o) feedback in adults with typical speech. LaDIVA demonstrated capability to simulate different modes of laryngeal motor control, ranging from short-term (i.e., reflexive) and long-term (i.e., adaptive) auditory feedback paradigms, to generating prosodic contours in speech. Simulations showed that LaDIVA’s laryngeal motor control displays properties of motor equivalence, i.e., LaDIVA could robustly generate compensatory responses to reflexive vocal f_o perturbations with varying initial laryngeal muscle activation levels leading to the same output. The model can also generate prosodic contours for studying laryngeal motor control in running speech. LaDIVA can expand the understanding of the physiology of human phonation to enable, for the first time, the investigation of causal effects of neural motor control in the fine structure of the vocal signal.     

Differential activation of a frontoparietal network explains population-level differences in statistical learning from speech

People of all ages display the ability to detect and learn from patterns in seemingly random stimuli. Referred to as statistical learning (SL), this process is particularly critical when learning a spoken language, helping in the identification of discrete words within a spoken phrase. Here, by considering individual differences in speech auditory–motor synchronization, we demonstrate that recruitment of a specific neural network supports behavioral differences in SL from speech. While independent component analysis (ICA) of fMRI data revealed that a network of auditory and superior pre/motor regions is universally activated in the process of learning, a frontoparietal network is additionally and selectively engaged by only some individuals (high auditory–motor synchronizers). Importantly, activation of this frontoparietal network is related to a boost in learning performance, and interference with this network via articulatory suppression (AS; i.e., producing irrelevant speech during learning) normalizes performance across the entire sample. Our work provides novel insights on SL from speech and reconciles previous contrasting findings. These findings also highlight a more general need to factor in fundamental individual differences for a precise characterization of cognitive phenomena.

In the context of speech, statistical learning is thought to be an important mechanism for language acquisition. This study shows that language statistical learning is boosted by the recruitment of a fronto-parietal brain network related to auditory-motor synchronization and its interplay with a mandatory auditory-motor learning system.     

Auditory sensory support of complicated voluntary goal-aimed bimanual movements

The intrasensory and sensor-effector interactions between inter-spike intervals of acoustic stem-evoked potentials with parameters of hands coordination was found with the help of correlation analysis. Role of excitation of ascending fibres of rostral part of the pons and lateral loop in mechanisms of the auditory-motor coordination was determined. Sex-dependent differences in integration of elements of the sensor-motor system because of lateralization of incoming auditory information and complication of the motor task performed were revealed. In men, mechanisms of auditory-motor coordination have less determined character than in women. That probably determines higher level of bi-manual coordination in men. Optimal correct realization of motor program in men is performed prognostically, while in women--after a mistake has been done.     

Sensory-Motor Interactions for Vocal Pitch Monitoring in Non-Primary Human Auditory Cortex

The neural mechanisms underlying processing of auditory feedback during self-vocalization are poorly understood. One technique used to study the role of auditory feedback involves shifting the pitch of the feedback that a speaker receives, known as pitch-shifted feedback. We utilized a pitch shift self-vocalization and playback paradigm to investigate the underlying neural mechanisms of audio-vocal interaction. High-resolution electrocorticography (ECoG) signals were recorded directly from auditory cortex of 10 human subjects while they vocalized and received brief downward (−100 cents) pitch perturbations in their voice auditory feedback (speaking task). ECoG was also recorded when subjects passively listened to playback of their own pitch-shifted vocalizations. Feedback pitch perturbations elicited average evoked potential (AEP) and event-related band power (ERBP) responses, primarily in the high gamma (70–150 Hz) range, in focal areas of non-primary auditory cortex on superior temporal gyrus (STG). The AEPs and high gamma responses were both modulated by speaking compared with playback in a subset of STG contacts. From these contacts, a majority showed significant enhancement of high gamma power and AEP responses during speaking while the remaining contacts showed attenuated response amplitudes. The speaking-induced enhancement effect suggests that engaging the vocal motor system can modulate auditory cortical processing of self-produced sounds in such a way as to increase neural sensitivity for feedback pitch error detection. It is likely that mechanisms such as efference copies may be involved in this process, and modulation of AEP and high gamma responses imply that such modulatory effects may affect different cortical generators within distinctive functional networks that drive voice production and control.     

Vocal responses to perturbations in voice auditory feedback in individuals with Parkinson's disease

Background

One of the most common symptoms of speech deficits in individuals with Parkinson''s disease (PD) is significantly reduced vocal loudness and pitch range. The present study investigated whether abnormal vocalizations in individuals with PD are related to sensory processing of voice auditory feedback. Perturbations in loudness or pitch of voice auditory feedback are known to elicit short latency, compensatory responses in voice amplitude or fundamental frequency.

Methodology/Principal Findings

Twelve individuals with Parkinson''s disease and 13 age- and sex- matched healthy control subjects sustained a vowel sound (/α/) and received unexpected, brief (200 ms) perturbations in voice loudness (±3 or 6 dB) or pitch (±100 cents) auditory feedback. Results showed that, while all subjects produced compensatory responses in their voice amplitude or fundamental frequency, individuals with PD exhibited larger response magnitudes than the control subjects. Furthermore, for loudness-shifted feedback, upward stimuli resulted in shorter response latencies than downward stimuli in the control subjects but not in individuals with PD.

Conclusions/Significance

The larger response magnitudes in individuals with PD compared with the control subjects suggest that processing of voice auditory feedback is abnormal in PD. Although the precise mechanisms of the voice feedback processing are unknown, results of this study suggest that abnormal voice control in individuals with PD may be related to dysfunctional mechanisms of error detection or correction in sensory feedback processing.     

Dynamics of Vocalization-Induced Modulation of Auditory Cortical Activity at Mid-utterance

Background

Recent research has addressed the suppression of cortical sensory responses to altered auditory feedback that occurs at utterance onset regarding speech. However, there is reason to assume that the mechanisms underlying sensorimotor processing at mid-utterance are different than those involved in sensorimotor control at utterance onset. The present study attempted to examine the dynamics of event-related potentials (ERPs) to different acoustic versions of auditory feedback at mid-utterance.

Methodology/Principal findings

Subjects produced a vowel sound while hearing their pitch-shifted voice (100 cents), a sum of their vocalization and pure tones, or a sum of their vocalization and white noise at mid-utterance via headphones. Subjects also passively listened to playback of what they heard during active vocalization. Cortical ERPs were recorded in response to different acoustic versions of feedback changes during both active vocalization and passive listening. The results showed that, relative to passive listening, active vocalization yielded enhanced P2 responses to the 100 cents pitch shifts, whereas suppression effects of P2 responses were observed when voice auditory feedback was distorted by pure tones or white noise.

Conclusion/Significance

The present findings, for the first time, demonstrate a dynamic modulation of cortical activity as a function of the quality of acoustic feedback at mid-utterance, suggesting that auditory cortical responses can be enhanced or suppressed to distinguish self-produced speech from externally-produced sounds.     

Rapid change in articulatory lip movement induced by preceding auditory feedback during production of bilabial plosives

Background

There has been plentiful evidence of kinesthetically induced rapid compensation for unanticipated perturbation in speech articulatory movements. However, the role of auditory information in stabilizing articulation has been little studied except for the control of voice fundamental frequency, voice amplitude and vowel formant frequencies. Although the influence of auditory information on the articulatory control process is evident in unintended speech errors caused by delayed auditory feedback, the direct and immediate effect of auditory alteration on the movements of articulators has not been clarified.

Methodology/Principal Findings

This work examined whether temporal changes in the auditory feedback of bilabial plosives immediately affects the subsequent lip movement. We conducted experiments with an auditory feedback alteration system that enabled us to replace or block speech sounds in real time. Participants were asked to produce the syllable /pa/ repeatedly at a constant rate. During the repetition, normal auditory feedback was interrupted, and one of three pre-recorded syllables /pa/, /Φa/, or /pi/, spoken by the same participant, was presented once at a different timing from the anticipated production onset, while no feedback was presented for subsequent repetitions. Comparisons of the labial distance trajectories under altered and normal feedback conditions indicated that the movement quickened during the short period immediately after the alteration onset, when /pa/ was presented 50 ms before the expected timing. Such change was not significant under other feedback conditions we tested.

Conclusions/Significance

The earlier articulation rapidly induced by the progressive auditory input suggests that a compensatory mechanism helps to maintain a constant speech rate by detecting errors between the internally predicted and actually provided auditory information associated with self movement. The timing- and context-dependent effects of feedback alteration suggest that the sensory error detection works in a temporally asymmetric window where acoustic features of the syllable to be produced may be coded.