Timing of speech in brain and glottis and the feedback delay problem in motor control

Abstract To learn complex motor skills, an organism must be able to assign sensory feedback events to the actions that caused them. This matching problem would be simple if motor neuron output led sensory feedback with a fixed, predictable lag. However, nonlinear dynamics in the brain and the body’s periphery can decouple the timing of critical events from that of the motor output which caused them. During human speech production, for example, phonation from the glottis (a sound source for speech) begins suddenly when subglottal pressure and laryngeal tension cross a sharp threshold (i.e. a bifurcation). Only if the brain can predict the timing of these discrete peripheral events resulting from motor output, then, would it be possible to match sensory feedback to movements based on temporal coherence. We show that event onsets in the human glottal waveform, as measured using electroglottography, are reflected in the human electroencephalogram during speech production, leading up to the time of the event itself. Conversely, glottal event times can be decoded from the electroencephalogram. After prolonged exposure to delayed auditory feedback, subjects recalibrate their behavioral threshold for detecting temporal auditory-motor mismatches, and decoded event times decouple from actual movements. This suggests decoding performance is driven by plastic predictions of peripheral timing, providing a missing component for hindsight credit assignment in motor control, in which specific feedback events are associated with the neural activity that gave rise to movements. We discuss parallel findings from the birdsong system suggesting that results may generalize across vocal learning species. Significance Statement To learn complex motor skills such as speech, the brain must pair actions with sensory feedback. However, feedback is delayed in time relative to actual movement, rendering this “hindsight credit assignment” problem a nontrivial task. We present evidence that events in the glottis, the articulatory organ that generates sound for human speech, are predictively encoded in the human brain during speech production. Given that corresponding events in auditory feedback are known to be prominently encoded in cortex, this highlights a common temporal marker by which articulatory gestures and sensory feedback could be aligned. Findings suggest activity in the human vocomotor system is shaped by biophysical dynamics in the vocal periphery, aligning with corresponding results in the birdsong system. Competing Interest Statement The authors have declared no competing interest. Footnotes Updated with revisions made during peer review.