Time-dependent neural processing of auditory feedback during voice pitch error detection

Abstract

The neural responses to sensory consequences of a self-produced motor act are suppressed compared with those in response to a similar but externally generated stimulus. Previous studies in the somatosensory and auditory systems have shown that the motor-induced suppression of the sensory mechanisms is sensitive to delays between the motor act and the onset of the stimulus. The present study investigated time-dependent neural processing of auditory feedback in response to self-produced vocalizations. ERPs were recorded in response to normal and pitch-shifted voice auditory feedback during active vocalization and passive listening to the playback of the same vocalizations. The pitch-shifted stimulus was delivered to the subjects' auditory feedback after a randomly chosen time delay between the vocal onset and the stimulus presentation. Results showed that the neural responses to delayed feedback perturbations were significantly larger than those in response to the pitch-shifted stimulus occurring at vocal onset. Active vocalization was shown to enhance neural responsiveness to feedback alterations only for nonzero delays compared with passive listening to the playback. These findings indicated that the neural mechanisms of auditory feedback processing are sensitive to timing between the vocal motor commands and the incoming auditory feedback. Time-dependent neural processing of auditory feedback may be an important feature of the audio-vocal integration system that helps to improve the feedback-based monitoring and control of voice structure through vocal error detection and correction.

Figure 1

Schematic of the experimental setup for introducing time delays between the vocal onset and the onset of auditory feedback pitch perturbation. The vocal onset, detected by a voice onset detector (VOD), triggered the pitch-shift stimulus (PSS) after a randomly chosen time delay (Δt). The PSS onset triggered a TTL pulse that was recorded on the computer and used for averaging the neural responses with respect to the onset of the stimulus.

Figure 2

Time course of the neural responses to (A) normal auditory feedback (NAF) occurring at vocal onset (delay = 0 msec) and to PSS for (A) 0-msec, (B) 200-msec, (C) 500-msec, and (D) 1000-msec delays between the vocal onset and the onset of the stimulus. The neural responses for each condition are separately plotted for all recording sites during active vocalization (solid) and passive listening (dashed) conditions. The dashed vertical lines mark the onset of normal (A) and pitch-shifted (B–E) feedback in each subplot.

Figure 2

Time course of the neural responses to (A) normal auditory feedback (NAF) occurring at vocal onset (delay = 0 msec) and to PSS for (A) 0-msec, (B) 200-msec, (C) 500-msec, and (D) 1000-msec delays between the vocal onset and the onset of the stimulus. The neural responses for each condition are separately plotted for all recording sites during active vocalization (solid) and passive listening (dashed) conditions. The dashed vertical lines mark the onset of normal (A) and pitch-shifted (B–E) feedback in each subplot.

Figure 3

Bar plots of the difference between P₁–N₁–P₂ neural peak amplitudes for active vocalization versus passive listening conditions in response to normal auditory feedback (NAF) and +200 cents pitch-shift stimulus (PSS) occurring at different delay times after vocal onset. The negative amplitudes on the y-axis indicate neural suppression during active vocalization compared with passive listening, and the positive amplitudes indicate vocalization-induced enhancement of neural responsiveness to +200 cents PSS. The asterisks (*) indicate a significant amplitude difference (p < .05) between vocalization and listening conditions.

Figure 4

Topographical scalp distributions of the averaged neural responses to normal (first column from left) and pitch-shifted (second to fifth column from left) auditory feedback across 17 subjects. The maps are calculated for 13 recording sites on the surface of the scalp (C_Z, C₃, C₄, T₃, T₄, F_Z, F₃, F₄, F₇, F₈, P_Z, P₃, and P₄) for (A) P₁ (latency = 67.08 msec), (B) N₁ (latency = 124.72 msec), and (C) P₂ (latency = 213.02 msec) peak amplitudes. The top and the bottom rows in each plot show the scalp distributions during passive listening and active vocalization conditions, respectively.