Functional identification of sensory mechanisms required for developmental song learning

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Abstract

A young male zebra finch (Taeniopygia guttata) learns to sing by copying the vocalizations of an older tutor in a process that parallels human speech acquisition. Brain pathways that control song production are well defined, but little is known about the sites and mechanisms of tutor song memorization. Here we test the hypothesis that molecular signaling in a sensory brain area outside of the song system is required for developmental song learning. Using controlled tutoring and a pharmacological inhibitor, we transiently suppressed the extracellular signal–regulated kinase signaling pathway in a portion of the auditory forebrain specifically during tutor song exposure. On maturation, treated birds produced poor copies of tutor song, whereas controls copied the tutor song effectively. Thus the foundation of normal song learning, the formation of a sensory memory of tutor song, requires a conserved molecular pathway in a brain area that is distinct from the circuit for song motor control.

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Figure 1: Experimental timeline.
Figure 2: Quantitative song analysis results.
Figure 3: Auditory lobule cannula placements and zenk in situ hybridization.
Figure 4: Plots of song similarity scores and position of cannula tips.
Figure 5: Test of U0126 effects on song discrimination.

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Acknowledgements

We thank O. Tchernichovski for consultation on experimental design and song analysis, C.D. Meliza for advice on operant training hardware and procedures, R. Stripling for Labview programming expertise, J. Lee for Matlab assistance and A. Feng, K. Christie and M. Monfils for consultations and technical support for the electrophysiology experiment. We also thank G. Robinson, T. Small and K. Replogle for manuscript comments. This work was supported by an Institute for Genomic Biology Postdoctoral Fellowship, a US National Institute on Deafness and Other Communication Disorders Sensory Neuroscience Postdoctoral Training Grant, a US National Institute of Neurological Disorders and Stroke Postdoctoral National Research Service Award (S.E.L.) and a US National Institutes of Health RO1 grant (NS045264, D.F.C.).

Author information

S.E.L. and D.F.C. designed the experiments, S.E.L. acquired and analyzed the data, and S.E.L. and D.F.C. wrote the manuscript.

Correspondence to Sarah E London or David F Clayton.

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Supplementary Figures 1–3, Table 1 and Methods (PDF 567 kb)

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