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Contributions of an avian basal ganglia–forebrain circuit to real-time modulation of song

Abstract

Cortical–basal ganglia circuits have a critical role in motor control and motor learning1. In songbirds, the anterior forebrain pathway (AFP) is a basal ganglia–forebrain circuit required for song learning and adult vocal plasticity but not for production of learned song2,3,4,5. Here, we investigate functional contributions of this circuit to the control of song, a complex, learned motor skill. We test the hypothesis that neural activity in the AFP of adult birds can direct moment-by-moment changes in the primary motor areas responsible for generating song. We show that song-triggered microstimulation in the output nucleus of the AFP induces acute and specific changes in learned parameters of song6,7. Moreover, under both natural and experimental conditions, variability in the pattern of AFP activity is associated with variability in song structure. Finally, lesions of the output nucleus of the AFP prevent naturally occurring modulation of song variability. These findings demonstrate a previously unappreciated capacity of the AFP to direct real-time changes in song. More generally, they suggest that frontal cortical and basal ganglia areas may contribute to motor learning by biasing motor output towards desired targets or by introducing stochastic variability required for reinforcement learning.

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Figure 1: Song-triggered microstimulation in LMAN elicits acute changes in learned parameters of syllable structure.
Figure 2: Specificity of stimulation.
Figure 3: Context-dependent changes in variability.
Figure 4: Contributions of the AFP to real-time song modulation.

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Acknowledgements

We thank N. Hessler for a portion of the data in Fig. 3e. We thank A. Basbaum, S. Lisberger, J. Sakata and B. Wright for helpful comments on this manuscript and A. Arteseros and K. McManaway for technical assistance. This work was supported by an HHMI Predoctoral Fellowship (M.H.K.), the MacArthur Foundation, the Steven and Michele Kirsch Foundation, NARSAD and NIH (A.J.D.), and the HHMI Biomedical Research Support Program grant, the McKnight Foundation, the Klingenstein Fund, a Searle Scholars Award and NIH (M.S.B.).

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Correspondence to Mimi H. Kao.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure 1

This figure provides additional information for how the latency between the application of a stimulus and the onset of a change in syllable structure was measured. Latency measurements could be complicated because the effects of stimulation at a given site could be specific to a subset of syllables. (GIF 46 kb)

Supplementary Figure 2

This figure shows a correlation between the magnitude of changes in LMAN variability and the magnitude of changes in song variability. (GIF 36 kb)

Supplementary Table 1

Summary of the effects of stimulation in LMAN for each syllable tested in 5 birds. (DOC 72 kb)

Supplementary Table 2

Summary of the effects of LMAN stimulation for each bird by site. Stimulation evoked significant changes in syllable structure in 18/20 sites in LMAN of 5 birds. (DOC 34 kb)

Supplementary Table 3

Summary of the effects of differential activation of LMAN neurons at a particular site. (DOC 51 kb)

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Kao, M., Doupe, A. & Brainard, M. Contributions of an avian basal ganglia–forebrain circuit to real-time modulation of song. Nature 433, 638–643 (2005). https://doi.org/10.1038/nature03127

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