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.Author Summary: Repetitions are common in animal vocalizations. Songs of many songbirds contain syllables that repeat a variable number of times, with non-Markovian distributions of repeat counts. The neural mechanism underlying such syllable repetitions is unknown. In this work, we show that auditory feedback plays an important role in sustaining syllable repetitions in the Bengalese finch. Deafening reduces syllable repetitions and skews the repeat number distribution towards short repeats. These effects are explained with our computational model, which suggests that syllable repeats are initially sustained by auditory feedback to the neural networks that drive the syllable production. The feedback strength weakens as the syllable repeats, increasing the likelihood that the syllable repetition stops. Neural recordings confirm such adaptation of auditory feedback to the auditory-motor circuit in the Bengalese finch. Our results suggests that sensory feedback can directly impact repetitions in motor sequences, and may provide insights into neural mechanisms of speech disorders such as stuttering.