Impairment of speech auditory feedback error detection and motor correction in post-stroke aphasia.

INTRODUCTION: The present study investigated how damage to left-hemisphere brain networks affects the ability for speech auditory feedback error detection and motor correction in post-stroke aphasia. METHODS: 34 individuals with left-hemisphere stroke and 25 neurologically intact age-matched control participants performed two randomized experimental tasks in which their online speech auditory feedback was altered using externally induced pitch-shift stimuli: 1) vocalization of a steady speech vowel sound /a/, and 2) listening to the playback of the same self-produced vowel vocalizations. Randomized control condition trials were interleaved in between vocalization and listening tasks where no pitch-shift stimuli were delivered. Following each trial, participants pressed a button to indicate whether they detected a pitch-shift error in their speech auditory feedback during vocalization and listening tasks. RESULTS: Our data analysis revealed that speech auditory feedback error detection accuracy rate was significantly lower in the stroke compared with control participants, irrespective of the experimental task (i.e. vocalization vs. listening) and trial condition (i.e. pitch-shifted vs. no-pitch-shift). We found that this effect was associated with the reduced magnitude of speech compensation in the early phase of responses at 150-200 ms following the onset of pitch-shift stimuli in stroke participants. In addition, motor speech compensation deficit in the stroke group was correlated with lower scores on speech repetition tasks as an index of language impairment resulting from aphasia. CONCLUSIONS: These findings provide evidence that left-hemisphere stroke is associated with impaired speech auditory feedback error processing, and such deficits account for specific aspects of language impairment in aphasia.

Neural Correlates of Vocal Auditory Feedback Processing: Unique Insights from Electrocorticography Recordings in a Human Cochlear Implant User.

There is considerable interest in understanding cortical processing and the function of top-down and bottom-up human neural circuits that control speech production. Research efforts to investigate these circuits are aided by analysis of spectro-temporal response characteristics of neural activity recorded by electrocorticography (ECoG). Further, cortical processing may be altered in the case of hearing-impaired cochlear implant (CI) users, as electric excitation of the auditory nerve creates a markedly different neural code for speech compared with that of the functionally intact hearing system. Studies of cortical activity in CI users typically record scalp potentials and are hampered by stimulus artifact contamination and by spatiotemporal filtering imposed by the skull. We present a unique case of a CI user who required direct recordings from the cortical surface using subdural electrodes implanted for epilepsy assessment. Using experimental conditions where the subject vocalized in the presence (CIs ON) or absence (CIs OFF) of auditory feedback, or listened to playback of self-vocalizations without production, we observed ECoG activity primarily in γ (32-70 Hz) and high γ (70-150 Hz) bands at focal regions on the lateral surface of the superior temporal gyrus (STG). High γ band responses differed in their amplitudes across conditions and cortical sites, possibly reflecting different rates of stimulus presentation and differing levels of neural adaptation. STG γ responses to playback and vocalization with auditory feedback were not different from responses to vocalization without feedback, indicating this activity reflects not only auditory, but also attentional, efference-copy, and sensorimotor processing during speech production.

Neural bases of sensorimotor adaptation in the vocal motor system.

The present study used event-related potential (ERP) recordings to investigate the neural mechanisms of sensorimotor adaptation in response to altered auditory feedback (AAF) during vocal production. 12 healthy speakers were tested under a vocal motor adaptation paradigm in which the fundamental frequency (F0) of their voice auditory feedback was pitch-shifted downward by one semi-tone (- 100 cents) during vowel vocalizations. Behavioral results revealed that subjects adapted to AAF by producing opposing (upward) responses to pitch-shift stimuli, and this adaptive behavior persisted after feedback alteration was removed (washout). We found that adaptation to AAF was accompanied by a significant increase in the amplitude of a parietal ERP activity elicited after the onset of vocalization. However, no such effect was observed for pre-motor ERPs elicited before vocalization onset. Moreover, we found that adaptive vocal responses were negatively correlated with ERPs over the parietal and positively correlated with those over the fronto-central areas after vocalization onset. These findings suggest that vocal motor adaptation is mediated by sensorimotor reprogramming of feedforward motor commands through incorporating auditory feedback, which is indexed by modulation of behavioral and ERP responses to AAF. We suggest that modulation of neural activities in the parietal cortex highlights its significance as a neural interface for sensorimotor integration and indicates its critical role in vocal motor adaptation. Our findings support the notion that the parietal mechanisms are involved in driving adaptive motor behavior to cope with unexpected changes in the sensory environment to accomplish communication goals during vocal production and motor control.

Neural Correlates of Vocal Production and Motor Control in Human Heschl's Gyrus.

The present study investigated how pitch frequency, a perceptually relevant aspect of periodicity in natural human vocalizations, is encoded in Heschl's gyrus (HG), and how this information may be used to influence vocal pitch motor control. We recorded local field potentials from multicontact depth electrodes implanted in HG of 14 neurosurgical epilepsy patients as they vocalized vowel sounds and received brief (200 ms) pitch perturbations at 100 Cents in their auditory feedback. Event-related band power responses to vocalizations showed sustained frequency following responses that tracked voice fundamental frequency (F0) and were significantly enhanced in posteromedial HG during speaking compared with when subjects listened to the playback of their own voice. In addition to frequency following responses, a transient response component within the high gamma frequency band (75-150 Hz) was identified. When this response followed the onset of vocalization, the magnitude of the response was the same for the speaking and playback conditions. In contrast, when this response followed a pitch shift, its magnitude was significantly enhanced during speaking compared with playback. We also observed that, in anterolateral HG, the power of high gamma responses to pitch shifts correlated with the magnitude of compensatory vocal responses. These findings demonstrate a functional parcellation of HG with neural activity that encodes pitch in natural human voice, distinguishes between self-generated and passively heard vocalizations, detects discrepancies between the intended and heard vocalization, and contains information about the resulting behavioral vocal compensations in response to auditory feedback pitch perturbations. SIGNIFICANCE STATEMENT: The present study is a significant contribution to our understanding of sensor-motor mechanisms of vocal production and motor control. The findings demonstrate distinct functional parcellation of core and noncore areas within human auditory cortex on Heschl's gyrus that process natural human vocalizations and pitch perturbations in the auditory feedback. In addition, our data provide evidence for distinct roles of high gamma neural oscillations and frequency following responses for processing periodicity in human vocalizations during vocal production and motor control.

A temporal predictive code for voice motor control: Evidence from ERP and behavioral responses to pitch-shifted auditory feedback.

The predictive coding model suggests that voice motor control is regulated by a process in which the mismatch (error) between feedforward predictions and sensory feedback is detected and used to correct vocal motor behavior. In this study, we investigated how predictions about timing of pitch perturbations in voice auditory feedback would modulate ERP and behavioral responses during vocal production. We designed six counterbalanced blocks in which a +100 cents pitch-shift stimulus perturbed voice auditory feedback during vowel sound vocalizations. In three blocks, there was a fixed delay (500, 750 or 1000 ms) between voice and pitch-shift stimulus onset (predictable), whereas in the other three blocks, stimulus onset delay was randomized between 500, 750 and 1000 ms (unpredictable). We found that subjects produced compensatory (opposing) vocal responses that started at 80 ms after the onset of the unpredictable stimuli. However, for predictable stimuli, subjects initiated vocal responses at 20 ms before and followed the direction of pitch shifts in voice feedback. Analysis of ERPs showed that the amplitudes of the N1 and P2 components were significantly reduced in response to predictable compared with unpredictable stimuli. These findings indicate that predictions about temporal features of sensory feedback can modulate vocal motor behavior. In the context of the predictive coding model, temporally-predictable stimuli are learned and reinforced by the internal feedforward system, and as indexed by the ERP suppression, the sensory feedback contribution is reduced for their processing. These findings provide new insights into the neural mechanisms of vocal production and motor control.

Sensory-motor networks involved in speech production and motor control: an fMRI study.

Speaking is one of the most complex motor behaviors developed to facilitate human communication. The underlying neural mechanisms of speech involve sensory-motor interactions that incorporate feedback information for online monitoring and control of produced speech sounds. In the present study, we adopted an auditory feedback pitch perturbation paradigm and combined it with functional magnetic resonance imaging (fMRI) recordings in order to identify brain areas involved in speech production and motor control. Subjects underwent fMRI scanning while they produced a steady vowel sound /a/ (speaking) or listened to the playback of their own vowel production (playback). During each condition, the auditory feedback from vowel production was either normal (no perturbation) or perturbed by an upward (+600 cents) pitch-shift stimulus randomly. Analysis of BOLD responses during speaking (with and without shift) vs. rest revealed activation of a complex network including bilateral superior temporal gyrus (STG), Heschl's gyrus, precentral gyrus, supplementary motor area (SMA), Rolandic operculum, postcentral gyrus and right inferior frontal gyrus (IFG). Performance correlation analysis showed that the subjects produced compensatory vocal responses that significantly correlated with BOLD response increases in bilateral STG and left precentral gyrus. However, during playback, the activation network was limited to cortical auditory areas including bilateral STG and Heschl's gyrus. Moreover, the contrast between speaking vs. playback highlighted a distinct functional network that included bilateral precentral gyrus, SMA, IFG, postcentral gyrus and insula. These findings suggest that speech motor control involves feedback error detection in sensory (e.g. auditory) cortices that subsequently activate motor-related areas for the adjustment of speech parameters during speaking.

Event related potentials study of aberrations in voice control mechanisms in adults with attention deficit hyperactivity disorder.

OBJECTIVE: The present study was designed to test for neural signs of impulsivity related to voice motor control in young adults with ADHD using EEG recordings in a voice pitch perturbation paradigm. METHODS: Two age-matched groups of young adults were presented with brief pitch shifts of auditory feedback during vocalization. Compensatory behavioral and corresponding bioelectrical brain responses were elicited by the pitch-shifted voice feedback. RESULTS: The analysis of bioelectrical responses showed that the ADHD group had shorter peak latency and onset time of motor-related bioelectrical brain responses as compared to the controls. CONCLUSIONS: These results were interpreted to suggest differences in executive functions between ADHD and control participants. SIGNIFICANCE: We hypothesize that more rapid motor-related bioelectrical responses found in the present study may be a manifestation of impulsiveness in adults with ADHD at the involuntary level of voice control.

Using speech and electrocorticography to map human auditory cortex.

Much less is known about the organization of the human auditory cortex compared to non-human primate auditory cortices. In an effort to further investigate the response properties of human auditory cortex, we present preliminary findings from human subjects implanted with depth electrodes in Heschl's gyrus (HG) as part of their neurosurgical treatment of epilepsy. Each subject had electrocorticography (ECoG) responses taken from medial and lateral HG in response to both speech and non-speech stimuli, including during speech production. Responses were somewhat variable across subjects, but posteromedial HG demonstrated frequency following responses to the stimuli in all subjects to some degree. Results and implications are discussed.

Neuronal mechanisms of voice control are affected by implicit expectancy of externally triggered perturbations in auditory feedback.

Accurate vocal production relies on several factors including sensory feedback and the ability to predict future challenges to the control processes. Repetitive patterns of perturbations in sensory feedback by themselves elicit implicit expectations in the vocal control system regarding the timing, quality and direction of perturbations. In the present study, the predictability of voice pitch-shifted auditory feedback was experimentally manipulated. A block of trials where all pitch-shift stimuli were upward, and therefore predictable was contrasted against an unpredictable block of trials in which the stimulus direction was randomized between upward and downward pitch-shifts. It was found that predictable perturbations in voice auditory feedback led to a reduction in the proportion of compensatory vocal responses, which might be indicative of a reduction in vocal control. The predictable perturbations also led to a reduction in the magnitude of the N1 component of cortical Event Related Potentials (ERP) that was associated with the reflexive compensations to the perturbations. We hypothesize that formation of expectancy in our study is accompanied by involuntary allocation of attentional resources occurring as a result of habituation or learning, that in turn trigger limited and controlled exploration-related motor variability in the vocal control system.

ERP correlates of pitch error detection in complex tone and voice auditory feedback with missing fundamental.

Previous studies have shown that the pitch of a sound is perceived in the absence of its fundamental frequency (F0), suggesting that a distinct mechanism may resolve pitch based on a pattern that exists between harmonic frequencies. The present study investigated whether such a mechanism is active during voice pitch control. ERPs were recorded in response to +200 cents pitch shifts in the auditory feedback of self-vocalizations and complex tones with and without the F0. The absence of the fundamental induced no difference in ERP latencies. However, a right-hemisphere difference was found in the N1 amplitudes with larger responses to complex tones that included the fundamental compared to when it was missing. The P1 and N1 latencies were shorter in the left hemisphere, and the N1 and P2 amplitudes were larger bilaterally for pitch shifts in voice and complex tones compared with pure tones. These findings suggest hemispheric differences in neural encoding of pitch in sounds with missing fundamental. Data from the present study suggest that the right cortical auditory areas, thought to be specialized for spectral processing, may utilize different mechanisms to resolve pitch in sounds with missing fundamental. The left hemisphere seems to perform faster processing to resolve pitch based on the rate of temporal variations in complex sounds compared with pure tones. These effects indicate that the differential neural processing of pitch in the left and right hemispheres may enable the audio-vocal system to detect temporal and spectral variations in the auditory feedback for vocal pitch control.

ERP correlates of auditory processing during automatic correction of unexpected perturbations in voice auditory feedback.

Auditory sensory processing is an important element of the neural mechanisms controlling human vocalization. We evaluated which components of Event Related Potentials (ERP) elicited by the unexpected shift of fundamental frequency in a subject's own voice might correlate with his/her ability to process auditory information. A significant negative correlation between the latency of the N1 component of the ERP and the Montreal Battery of Evaluation of Amusia scores for Melodic organization was found. A possible functional role of neuronal activity underling the N1 component in voice control mechanisms is discussed.

Error-dependent modulation of speech-induced auditory suppression for pitch-shifted voice feedback.

BACKGROUND: The motor-driven predictions about expected sensory feedback (efference copies) have been proposed to play an important role in recognition of sensory consequences of self-produced motor actions. In the auditory system, this effect was suggested to result in suppression of sensory neural responses to self-produced voices that are predicted by the efference copies during vocal production in comparison with passive listening to the playback of the identical self-vocalizations. In the present study, event-related potentials (ERPs) were recorded in response to upward pitch shift stimuli (PSS) with five different magnitudes (0, +50, +100, +200 and +400 cents) at voice onset during active vocal production and passive listening to the playback. RESULTS: Results indicated that the suppression of the N1 component during vocal production was largest for unaltered voice feedback (PSS: 0 cents), became smaller as the magnitude of PSS increased to 200 cents, and was almost completely eliminated in response to 400 cents stimuli. CONCLUSIONS: Findings of the present study suggest that the brain utilizes the motor predictions (efference copies) to determine the source of incoming stimuli and maximally suppresses the auditory responses to unaltered feedback of self-vocalizations. The reduction of suppression for 50, 100 and 200 cents and its elimination for 400 cents pitch-shifted voice auditory feedback support the idea that motor-driven suppression of voice feedback leads to distinctly different sensory neural processing of self vs. non-self vocalizations. This characteristic may enable the audio-vocal system to more effectively detect and correct for unexpected errors in the feedback of self-produced voice pitch compared with externally-generated sounds.

Laryngeal electromyographic responses to perturbations in voice pitch auditory feedback.

The present study was conducted to test the hypothesis that intrinsic laryngeal muscles are involved in producing voice fundamental frequency (F(0)) responses to perturbations in voice pitch auditory feedback. Electromyography (EMG) recordings of the cricothyroid and thyroarytenoid muscles were made with hooked-wire electrodes, while subjects sustained vowel phonations at three different voice F(0) levels (conversational, high pitch in head register, and falsetto register) and received randomized pitch shifts (±100 or ±300 cents) in their voice auditory feedback. The median latencies from stimulus onset to the peak in the EMG and voice F(0) responses were 167 and 224 ms, respectively. Among the three different F(0) levels, the falsetto register produced compensatory EMG responses that occurred prior to vocal responses and increased along with rising voice F(0) responses and decreased for falling F(0) responses. For the conversational and high voice levels, the EMG response timing was more variable than in the falsetto voice, and changes in EMG activity with relevance to the vocal responses did not follow the consistent trend observed in the falsetto condition. The data from the falsetto condition suggest that both the cricothyroid and thyroarytenoid muscles are involved in generating the compensatory vocal responses to pitch-shifted voice feedback.

Differential effects of perturbation direction and magnitude on the neural processing of voice pitch feedback.

OBJECTIVE: The present study examined the differential effects of voice auditory feedback perturbation direction and magnitude on voice fundamental frequency (F(0)) responses and event-related potentials (ERPs) from EEG electrodes on the scalp. METHODS: The voice F(0) responses and N1 and P2 components of ERPs were examined from 12 right-handed speakers when they sustained a vowel phonation and their mid-utterance voice pitch feedback was shifted ±100, ±200, and ±500 cents with 200 ms duration. RESULTS: Downward voice pitch feedback perturbations led to larger voice F(0) responses than upward perturbations. The amplitudes of N1 and P2 components were larger for downward compared with upward pitch-shifts for 200 and 500 cents stimulus magnitudes. Shorter N1 and P2 latencies were also associated with larger magnitudes of pitch feedback perturbations. CONCLUSIONS: Corresponding changes in vocal and neural responses to upward and downward voice pitch feedback perturbations suggest that the N1 and P2 components of ERPs reflect neural concomitants of the vocal responses. SIGNIFICANCE: The findings of interactive effects between the magnitude and direction of voice feedback pitch perturbation on N1 and P2 ERP components indicate that the neural mechanisms underlying error detection and correction in voice pitch auditory feedback are differentially sensitive to both the magnitude and direction of pitch perturbations.