Abstract
Premotor circuits help generate imitative behaviors and can be activated during observation of another animal′s behavior, leading to speculation that these circuits participate in sensory learning that is important to imitation. Here we tested this idea by focally manipulating the brain activity of juvenile zebra finches, which learn to sing by memorizing and vocally copying the song of an adult tutor. Tutor song–contingent optogenetic or electrical disruption of neural activity in the pupil′s song premotor nucleus HVC prevented song copying, indicating that a premotor structure important to the temporal control of birdsong also helps encode the tutor song. In vivo multiphoton imaging and neural manipulations delineated a pathway and a candidate synaptic mechanism through which tutor song information is encoded by premotor circuits. These findings provide evidence that premotor circuits help encode sensory information about the behavioral model before shaping and executing imitative behaviors.
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Acknowledgements
The authors thank H. Greenside, S. Lisberger, D. Purves, K. Tschida and F. Wang for reading and commenting on the manuscript, K. Hamaguchi (Duke University Medical Center) for data analysis software support and design of microdialysis probes, T. Otchy, K. Bohon, A. Bae and S. Lotfi for technical assistance and assistance with data processing and J. Baltzegar for animal husbandry and laboratory support. This research was supported by grants from the National Science Foundation (R.M.), the US National Institutes of Health (R.M. (R01 DC02524) and B.P.Ö. (R01 NS066408)), a Rubicon fellowship from the Netherlands Organization for Scientific Research (NWO) to S.M.H.G. and grants from the Klingenstein, Sloan and McKnight Foundations (B.P.Ö.).
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This manuscript combines the synergistic results of two independently conceived and executed research studies arriving at similar conclusions. T.F.R. and R.M. designed all experiments involving tutor song-contingent optogenetic or electrical manipulations of HVC activity, in vivo multiphoton imaging of HVC dendritic spines, pharmacological manipulations of NMDA receptors in HVC during tutoring and tutor song-contingent microstimulation of NIf and Field L. T.F.R. conducted all of the aforementioned experiments and analyzed resultant data with input from R.M., S.M.H.G. and B.P.Ö. designed, executed and analyzed the results of experiments involving permanent or reversible NIf lesions. M.M. adapted optogenetic methods for use in the zebra finch and characterized the effects of hChR2 activation on HVC neurons in brain slices. T.F.R. and R.M. wrote the manuscript with extensive input from B.P.Ö. and S.M.H.G. All authors read and commented on the manuscript.
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Supplementary Figures 1–7 and Table 1 (PDF 2434 kb)
Supplementary Video 1
Tutor song-triggered optogenetic disruption of neural activity in the pupils' HVC. Video of a juvenile zebra finch being tutored for the first time, using tutor song-contingent optogenetic methods to disrupt neural activity in HVC. The song of the tutor (bird on the right in this video) is detected by software and used to drive brief pulses of blue light delivered to the HVC of the pupil (bird on left in this video) via chronically implanted fiber optic cables (MOV 5127 kb)
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Roberts, T., Gobes, S., Murugan, M. et al. Motor circuits are required to encode a sensory model for imitative learning. Nat Neurosci 15, 1454–1459 (2012). https://doi.org/10.1038/nn.3206
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DOI: https://doi.org/10.1038/nn.3206
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