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Research Articles, Systems/Circuits

Performance-Dependent Consolidation of Learned Vocal Changes in Adult Songbirds

Ryosuke O. Tachibana, Dahyun Lee, Kazuki Kai and Satoshi Kojima
Journal of Neuroscience 9 March 2022, 42 (10) 1974-1986; DOI: https://doi.org/10.1523/JNEUROSCI.1942-21.2021
Ryosuke O. Tachibana
1Department of Life Sciences and Center for Evolutionary Cognitive Sciences, Graduate School of Arts and Sciences, University of Tokyo, Tokyo, 153-8902, Japan
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Dahyun Lee
2Sensory and Motor Systems Research Group, Korea Brain Research Institute, Daegu, 41062, South Korea
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Kazuki Kai
2Sensory and Motor Systems Research Group, Korea Brain Research Institute, Daegu, 41062, South Korea
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Satoshi Kojima
2Sensory and Motor Systems Research Group, Korea Brain Research Institute, Daegu, 41062, South Korea
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Abstract

Motor skills learned through practice are consolidated at later time, which can include nighttime, but the time course of motor memory consolidation and its underlying mechanisms remain poorly understood. We investigated neural substrates underlying motor memory consolidation of learned changes in birdsong, a tractable model system for studying neural basis of motor skill learning. Previous studies in male zebra finches and Bengalese finches have demonstrated that adaptive changes in adult song structure learned through a reinforcement paradigm are initially driven by a cortical-basal ganglia circuit, and subsequently consolidated into downstream cortical motor circuitry. However, the time course of the consolidation process, including whether it occurs offline during nighttime or online during daytime, remains unclear and even controversial. Here, we provide in both species experimental evidence of virtually no consolidation of learned vocal changes during nighttime. We demonstrate instead that the consolidation occurs during daytime and the amount of consolidation is strongly correlated with the amount of learning, suggesting online, performance-dependent mechanisms of consolidation of learned vocal changes. Moreover, by using computer simulations based on our experimental results, we demonstrate that such online, performance-dependent consolidation can account for the contradicting conclusions concerning the time course of consolidation process reached by previous studies. These results thus reconcile a controversy in the study of vocal motor consolidation in songbirds, and illustrate the neural substrates through which newly learned motor skills initially implemented by cortical-basal ganglia circuits become encoded in the cortical motor circuitry.

SIGNIFICANCE STATEMENT Motor skills learned through repetitive practice become stable and are consolidated into cortical motor circuits. We investigate neural substrates of this “motor memory consolidation” in adult songbirds, which produce songs that are complex motor skills learned and maintained through repetitive vocal practice. We demonstrate that learned changes in song acoustic structure are consolidated into the cortical motor circuits predominantly during daytime, but not during nighttime, depending on ongoing song performance. These consolidation mechanisms reconcile seemingly contradicting results of previous studies regarding the time course of vocal learning consolidation, and provide fundamental insights into the process through which learned performance of complex motor skills is consolidated and encoded in in motor circuits.

  • basal ganglia
  • birdsong
  • memory consolidation
  • skill learning
  • songbird
  • vocal learning

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The Journal of Neuroscience: 42 (10)
Journal of Neuroscience
Vol. 42, Issue 10
9 Mar 2022
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Performance-Dependent Consolidation of Learned Vocal Changes in Adult Songbirds
Ryosuke O. Tachibana, Dahyun Lee, Kazuki Kai, Satoshi Kojima
Journal of Neuroscience 9 March 2022, 42 (10) 1974-1986; DOI: 10.1523/JNEUROSCI.1942-21.2021

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Performance-Dependent Consolidation of Learned Vocal Changes in Adult Songbirds
Ryosuke O. Tachibana, Dahyun Lee, Kazuki Kai, Satoshi Kojima
Journal of Neuroscience 9 March 2022, 42 (10) 1974-1986; DOI: 10.1523/JNEUROSCI.1942-21.2021
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Keywords

  • basal ganglia
  • birdsong
  • memory consolidation
  • skill learning
  • songbird
  • vocal learning

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