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

Jason D Wittenbach,Michael S Brainard,Kristofer E Bouchard,Dezhe Z Jin,Frédéric E Theunissen

doi:10.1371/journal.pcbi.1004471

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.

Highlights

Many complex behaviors—human speech, playing a piano, or birdsong—consist of a set of discrete actions that can be flexibly organized into variable sequences [1,2,3]
Because of the delays in both motor and sensory processing in nervous systems, it has been argued that a sequence generation mechanism relying solely on sensory feedback would be too slow to account for the execution of fast sequences such as typing and speech [1]
The critical features of our framework for repeat generation are: (1) the population of neurons generating a repeated syllable receives a source of excitatory input in addition to the recurrent excitation from the sequencing network, and (2) the strength of this input adapts over time during repeat generation. We instantiate this framework as a ‘branchedchain’ network with adapting auditory feedback, and place this network in nucleus HVC

Summary

Introduction

Many complex behaviors—human speech, playing a piano, or birdsong—consist of a set of discrete actions that can be flexibly organized into variable sequences [1,2,3]. A central issue in understanding how nervous systems generate complex sequences is the role of sensory feedback versus internal motor programs [4] (Fig 1a). Because of the delays in both motor and sensory processing in nervous systems, it has been argued that a sequence generation mechanism relying solely on sensory feedback would be too slow to account for the execution of fast sequences such as typing and speech [1]. Sequences are generated by internal motor programs controlling sequence production without the use of sensory feedback [7,8,9]. Despite the ubiquity of sequencing in behavior, the neural mechanisms of how sensory feedback interacts with internal motor programs to influence discrete actions remain largely unexplored

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Results

Conclusion