An Adapting Auditory-motor Feedback Loop Can Contribute to Generating Vocal Repetition

Abstract

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.

Auditory-induced neural dynamics in sensory-motor circuitry predict learned temporal and sequential statistics of birdsong

“…. → HVC) (45), and activation due to sensory feedback (29,35,46). Our observation that the dynamics of poststimulus activity were slowed by ∼10 ms relative to the expected timing of song [for both temporal tuning (Fig.…”

“…Acute electrophysiology procedures, as previously described (42), were performed in accordance with established animal care protocols approved by the University of California, San Francisco, Institutional Animal Care and Use Committee. Birds used in this study also contributed data to other studies (42,46,50). See SI Materials and Methods for further details.…”

The Effects of Pitch Shifts on Delay-Induced Changes in Vocal Sequencing in a Songbird

“…Although further refinements of our technique, such as testing of other delay magnitudes, might reveal such a difference, it is also possible that these two forms of variable sequencing (branch points and repeated syllables) differ in their reliance on the acoustic structure of auditory feedback (Wittenbach et al, 2015). Future studies could examine this possibility by investigating the effects of sensory perturbations on behavior and neural activity during vocal production.…”

Hidden neural states underlie canary song syntax

“…One neuron's activity was specific to a single context (Figure 4d ROI 10. c.f. as in 25 ) and the other three were active in multiple contexts (Figure 4d, ROIs 24,29,31). The phrase during which these cells were recorded precedes a complex transition and the type of the preceding phrase poorly predicts the transition outcome (right bar in Figure 4e, 0.08 out of 1 bit, bootstrapped mutual information estimate, methods).…”

“…15% had 1 st order correlations where activity during one phrase depends on the identity of an adjacent phrase, and 5.6% had ≥2 nd order relations (Figure 2d, Supplementary Figure 2 These sequence dependencies could potentially be explained by other factors inherent to the song that may be more predictive of phrase sequence than HVC activity. For example, transition probabilities following a given phrase could potentially depend on the phrase duration 1 , on the onset and offset timing of previous phrases, and on the global time since the start of the songimplicating processes such as neuromodulator tone, temperature buildup, or slow adaptation to auditory feedback [28][29][30][31][32][33] (c.f. Supplementary Figure 2 -7a,b, Supplementary Figure 2 -8).…”