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Performance variability enables adaptive plasticity of ‘crystallized’ adult birdsong

Abstract

Significant trial-by-trial variation persists even in the most practiced skills. One prevalent view is that such variation is simply ‘noise’ that the nervous system is unable to control or that remains below threshold for behavioural relevance1,2,3. An alternative hypothesis is that such variation enables trial-and-error learning, in which the motor system generates variation and differentially retains behaviours that give rise to better outcomes. Here we test the latter possibility for adult bengalese finch song. Adult birdsong is a complex, learned motor skill that is produced in a highly stereotyped fashion from one rendition to the next4,5. Nevertheless, there is subtle trial-by-trial variation even in stable, ‘crystallized’ adult song6,7,8. We used a computerized system to monitor small natural variations in the pitch of targeted song elements and deliver real-time auditory disruption to a subset of those variations. Birds rapidly shifted the pitch of their vocalizations in an adaptive fashion to avoid disruption. These vocal changes were precisely restricted to the targeted features of song. Hence, birds were able to learn effectively by associating small variations in their vocal behaviour with differential outcomes. Such a process could help to maintain stable, learned song despite changes to the vocal control system arising from ageing or injury. More generally, our results suggest that residual variability in well learned skills is not entirely noise but rather reflects meaningful motor exploration that can support continuous learning and optimization of performance.

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Figure 1: Differential reinforcement can adaptively alter features of adult song.
Figure 2: Adaptive shifts in fundamental frequency occur rapidly and recover.
Figure 3: Changes are restricted to targeted features of song.
Figure 4: Delayed feedback prevents adaptive pitch shifts.
Figure 5: Incremental adjustment of threshold drives large pitch changes.

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Acknowledgements

We thank A. Doupe, L. Frank, T. Warren, M. Wohlgemuth, S. Sober, J. Sakata, C. Hampton and J. Wong for comments. This work was supported by an NIDCD NRSA postdoctoral fellowship and the Sloan-Swartz Foundation (E.C.T.) and by an NIDCD R01 award, an NIMH Conte Center for Neuroscience Research award and a McKnight Foundation Scholars Award (M.S.B).

Author Contributions E.C.T. performed the experiments and analysis; E.C.T. and M.S.B. designed the experiments and wrote the manuscript.

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Correspondence to Evren C. Tumer.

Supplementary information

Supplementary Information

This file contains Supplementary Notes with Supplementary Figures S1-S3 showing: details of differential reinforcement; relationship between baseline variation and capacity for adaptive change and how non-contingent feedback did not alter song. (PDF 254 kb)

Supplementary Audio 1

This file contains Supplementary Audio 1 demonstrating the stereotypy of normal adult Bengalese finch song. Three separate songs are played corresponding to the spectrograms of Figure 1a. (WAV 310 kb)

Supplementary Video 1

This file contains Supplementary Video 1 demonstrating the salience of changes driven by progressively increasing the reinforcement threshold. Points and sounds reflect pitch of 20 randomly selected syllables from each of 2 days of baseline data and 13 days of differential reinforcement. Blue line indicates reinforcement threshold. Data from experiment of Figure 5a. (MOV 454 kb)

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Tumer, E., Brainard, M. Performance variability enables adaptive plasticity of ‘crystallized’ adult birdsong. Nature 450, 1240–1244 (2007). https://doi.org/10.1038/nature06390

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