Spontaneous variability predicts adaptive motor response in vocal pitch control

Abstract

Our motor system uses sensory feedback to keep behavioral performance in desired status. From this view, motor fluctuation is not simply noise inevitably caused in the nervous system, but should provide a role in generating variations to explore better outcomes via their sensory feedback. Vocal control system offers a good model to investigate such adaptive sensory-motor interactions. The pitch, or fundamental frequency (FF), of voice is adaptively regulated by hearing its auditory feedback to compensate FF deviations. Animal studies, particularly for songbirds, have demonstrated that the variability in vocal features contributes to the adaptive control, although the same issue in human vocalizations has remained unclear. Here, we tested whether and how the motor variability contributes to adaptive control of vocal FF in humans. We measured the amount of compensatory vocal responses against FF shifts in the auditory feedback, and quantified the motor variability as amplitudes of spontaneous FF fluctuations during no shift vocalizations. The result showed a positive correlation between the ratio of compensation and the spontaneous vocal variability. Further analysis indicated that this correlation was due to slowly fluctuating components (<5 Hz) of the variability, but not fast fluctuations (6-30 Hz), which is likely to reflect controllability from the central nervous system. Moreover, the compensatory responses consisted of the same frequency range with the slow component in the spontaneous variability. These findings consistently demonstrated that the spontaneous motor variability predicts the adaptive control in vocal FF, supporting the motor exploration hypothesis. Significance statementWe regulate our own vocalization by hearing own voice. This fact is typically observed as canceling-out (compensatory) responses in vocalized pitch when artificial pitch shifts were induced in the auditory feedback of own voice. Interestingly, the amount of such compensation widely ranges among talkers from perfect cancellation to almost nothing. Here we demonstrated that participants who spontaneously exhibited larger fluctuations showed greater amounts of the compensation against feedbacked pitch shifts. Our in-depth analyses showed that slowly fluctuating components in spontaneous pitch variability are specifically correlated with the compensation ratios, and was shared in the compensatory response as a dominant component. These findings support the idea that such variability contributes to generating motor explorations to find better outcomes in motor controls.