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Vocal learning is constrained by the statistics of sensorimotor experience.

Abstract

The brain uses sensory feedback to correct behavioral errors. Larger errors by definition require greater corrections, and many models of learning assume that larger sensory feedback errors drive larger motor changes. However, an alternative perspective is that larger errors drive learning less effectively because such errors fall outside the range of errors normally experienced and are therefore unlikely to reflect accurate feedback. This is especially crucial in vocal control because auditory feedback can be contaminated by environmental noise or sensory processing errors. A successful control strategy must therefore rely on feedback to correct errors while disregarding aberrant auditory signals that would lead to maladaptive vocal corrections. We hypothesized that these constraints result in compensation that is greatest for smaller imposed errors and least for larger errors. To test this hypothesis, we manipulated the pitch of auditory feedback in singing Bengalese finches. We found that learning driven by larger sensory errors was both slower than that resulting from smaller errors and showed less complete compensation for the imposed error. Additionally, we found that a simple principle could account for these data: the amount of compensation was proportional to the overlap between the baseline distribution of pitch production and the distribution experienced during the shift. Correspondingly, the fraction of compensation approached zero when pitch was shifted outside of the songs baseline pitch distribution. Our data demonstrate that sensory errors drive learning best when they fall within the range of production variability, suggesting that learning is constrained by the statistics of sensorimotor experience.

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