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Motor circuits are required to encode a sensory model for imitative learning

Nature Neuroscience volume 15, pages 1454–1459 (2012)Cite this article

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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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Figure 1: Testing the role of premotor circuits in sensory learning in songbirds.
Figure 2: Optogenetic disruption of neural activity in the pupil's HVC during tutoring impairs copying.
Figure 3: Microstimulation of HVC triggered by tutor song syllable disrupts copying of the targeted syllable.
Figure 4: Blocking NMDA receptors in HVC during tutoring prevents spine enlargement and disrupts copying of the tutor song.
Figure 5: The tutor experience is conveyed to HVC from the nucleus NIf.

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References

  1. Dehaene-Lambertz, G. et al. Functional organization of perisylvian activation during presentation of sentences in preverbal infants. Proc. Natl. Acad. Sci. USA 103, 14240–14245 (2006).

    Article  CAS  Google Scholar 

  2. Ferrari, P.F., Gallese, V., Rizzolatti, G. & Fogassi, L. Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. Eur. J. Neurosci. 17, 1703–1714 (2003).

    Article  Google Scholar 

  3. Gallese, V., Fadiga, L., Fogassi, L. & Rizzolatti, G. Action recognition in the premotor cortex. Brain 119, 593–609 (1996).

    Article  Google Scholar 

  4. Prather, J.F., Peters, S., Nowicki, S. & Mooney, R. Precise auditory-vocal mirroring in neurons for learned vocal communication. Nature 451, 305–310 (2008).

    Article  CAS  Google Scholar 

  5. Prather, J.F., Peters, S., Nowicki, S. & Mooney, R. Persistent representation of juvenile experience in the adult songbird brain. J. Neurosci. 30, 10586–10598 (2010).

    Article  CAS  Google Scholar 

  6. Arbib, M.A., Liebal, K. & Pika, S. Primate vocalization, gesture, and the evolution of human language. Curr. Anthropol. 49, 1053–1063 discussion 1063–1076 (2008).

    Article  Google Scholar 

  7. Iacoboni, M. et al. Cortical mechanisms of human imitation. Science 286, 2526–2528 (1999).

    Article  CAS  Google Scholar 

  8. Rizzolatti, G. & Arbib, M.A. Language within our grasp. Trends Neurosci. 21, 188–194 (1998).

    Article  CAS  Google Scholar 

  9. Rizzolatti, G., Fogassi, L. & Gallese, V. Neurophysiological mechanisms underlying the understanding and imitation of action. Nat. Rev. Neurosci. 2, 661–670 (2001).

    Article  CAS  Google Scholar 

  10. Doupe, A.J. & Kuhl, P.K. Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 22, 567–631 (1999).

    Article  CAS  Google Scholar 

  11. Immelman, K. Song development in the zebra finch and other estrildid finches. in Bird Vocalizations (ed. Hinde, R.A.), 61–74 (Cambridge University Press, 1969).

  12. Marler, P. & Tamura, M. Culturally transmitted patterns of vocal behavior in sparrows. Science 146, 1483–1486 (1964).

    Article  CAS  Google Scholar 

  13. Mooney, R. Neural mechanisms for learned birdsong. Learn. Mem. 16, 655–669 (2009).

    Article  Google Scholar 

  14. Hahnloser, R.H. & Kotowicz, A. Auditory representations and memory in birdsong learning. Curr. Opin. Neurobiol. 20, 332–339 (2010).

    Article  CAS  Google Scholar 

  15. London, S.E. & Clayton, D.F. Functional identification of sensory mechanisms required for developmental song learning. Nat. Neurosci. 11, 579–586 (2008).

    Article  CAS  Google Scholar 

  16. Bolhuis, J.J., Hetebrij, E., Den Boer-Visser, A.M., De Groot, J.H. & Zijlstra, G.G. Localized immediate early gene expression related to the strength of song learning in socially reared zebra finches. Eur. J. Neurosci. 13, 2165–2170 (2001).

    Article  CAS  Google Scholar 

  17. Gobes, S.M. & Bolhuis, J.J. Birdsong memory: a neural dissociation between song recognition and production. Curr. Biol. 17, 789–793 (2007).

    Article  CAS  Google Scholar 

  18. Phan, M.L., Pytte, C.L. & Vicario, D.S. Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds. Proc. Natl. Acad. Sci. USA 103, 1088–1093 (2006).

    Article  CAS  Google Scholar 

  19. Terpstra, N.J. & Bolhuis, J.J. & den Boer-Visser, A.M. An analysis of the neural representation of birdsong memory. J. Neurosci. 24, 4971–4977 (2004).

    Article  CAS  Google Scholar 

  20. Akutagawa, E. & Konishi, M. New brain pathways found in the vocal control system of a songbird. J. Comp. Neurol. 518, 3086–3100 (2010).

    Article  Google Scholar 

  21. Bauer, E.E. et al. A synaptic basis for auditory-vocal integration in the songbird. J. Neurosci. 28, 1509–1522 (2008).

    Article  CAS  Google Scholar 

  22. Nottebohm, F., Stokes, T.M. & Leonard, C.M. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165, 457–486 (1976).

    Article  CAS  Google Scholar 

  23. Hahnloser, R.H., Kozhevnikov, A.A. & Fee, M.S. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419, 65–70 (2002).

    Article  CAS  Google Scholar 

  24. Long, M.A. & Fee, M.S. Using temperature to analyse temporal dynamics in the songbird motor pathway. Nature 456, 189–194 (2008).

    Article  CAS  Google Scholar 

  25. Nick, T.A. & Konishi, M. Neural song preference during vocal learning in the zebra finch depends on age and state. J. Neurobiol. 62, 231–242 (2005).

    Article  Google Scholar 

  26. Roberts, T.F., Tschida, K.A., Klein, M.E. & Mooney, R. Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning. Nature 463, 948–952 (2010).

    Article  CAS  Google Scholar 

  27. Basham, M.E., Nordeen, E.J. & Nordeen, K.W. Blockade of NMDA receptors in the anterior forebrain impairs sensory acquisition in the zebra finch (Poephila guttata). Neurobiol. Learn. Mem. 66, 295–304 (1996).

    Article  CAS  Google Scholar 

  28. Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263–1268 (2005).

    Article  CAS  Google Scholar 

  29. Nagel, G. et al. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15, 2279–2284 (2005).

    Article  CAS  Google Scholar 

  30. Yizhar, O., Fenno, L.E., Davidson, T.J., Mogri, M. & Deisseroth, K. Optogenetics in neural systems. Neuron 71, 9–34 (2011).

    Article  CAS  Google Scholar 

  31. Zhang, F. et al. Multimodal fast optical interrogation of neural circuitry. Nature 446, 633–639 (2007).

    Article  CAS  Google Scholar 

  32. Kelley, D.B. & Nottebohm, F. Projections of a telencephalic auditory nucleus-field L-in the canary. J. Comp. Neurol. 183, 455–469 (1979).

    Article  CAS  Google Scholar 

  33. Vates, G.E., Broome, B.M., Mello, C.V. & Nottebohm, F. Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches. J. Comp. Neurol. 366, 613–642 (1996).

    Article  CAS  Google Scholar 

  34. Wild, J.M., Williams, M.N., Howie, G.J. & Mooney, R. Calcium-binding proteins define interneurons in HVC of the zebra finch (Taeniopygia guttata). J. Comp. Neurol. 483, 76–90 (2005).

    Article  CAS  Google Scholar 

  35. Mooney, R. & Prather, J.F. The HVC microcircuit: the synaptic basis for interactions between song motor and vocal plasticity pathways. J. Neurosci. 25, 1952–1964 (2005).

    Article  CAS  Google Scholar 

  36. Tumer, E.C. & Brainard, M.S. Performance variability enables adaptive plasticity of 'crystallized' adult birdsong. Nature 450, 1240–1244 (2007).

    Article  CAS  Google Scholar 

  37. Vu, E.T., Mazurek, M.E. & Kuo, Y.C. Identification of a forebrain motor programming network for the learned song of zebra finches. J. Neurosci. 14, 6924–6934 (1994).

    Article  CAS  Google Scholar 

  38. Yu, A.C. & Margoliash, D. Temporal hierarchical control of singing in birds. Science 273, 1871–1875 (1996).

    Article  CAS  Google Scholar 

  39. Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66–70 (1999).

    Article  CAS  Google Scholar 

  40. Matsuzaki, M., Honkura, N., Ellis-Davies, G.C. & Kasai, H. Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761–766 (2004).

    Article  CAS  Google Scholar 

  41. Fortune, E.S. & Margoliash, D. Parallel pathways and convergence onto HVc and adjacent neostriatum of adult zebra finches (Taeniopygia guttata). J. Comp. Neurol. 360, 413–441 (1995).

    Article  CAS  Google Scholar 

  42. Cardin, J.A., Raksin, J.N. & Schmidt, M.F. Sensorimotor nucleus NIf is necessary for auditory processing but not vocal motor output in the avian song system. J. Neurophysiol. 93, 2157–2166 (2005).

    Article  Google Scholar 

  43. Coleman, M.J. & Mooney, R. Synaptic transformations underlying highly selective auditory representations of learned birdsong. J. Neurosci. 24, 7251–7265 (2004).

    Article  CAS  Google Scholar 

  44. Hahnloser, R.H. & Fee, M.S. Sleep-related spike bursts in HVC are driven by the nucleus interface of the nidopallium. J. Neurophysiol. 97, 423–435 (2007).

    Article  Google Scholar 

  45. Roy, A. & Mooney, R. Song decrystallization in adult zebra finches does not require the song nucleus NIf. J. Neurophysiol. 102, 979–991 (2009).

    Article  Google Scholar 

  46. Fortune, E.S. & Margoliash, D. Cytoarchitectonic organization and morphology of cells of the field L complex in male zebra finches (Taenopygia guttata). J. Comp. Neurol. 325, 388–404 (1992).

    Article  CAS  Google Scholar 

  47. Bolhuis, J.J. & Gahr, M. Neural mechanisms of birdsong memory. Nat. Rev. Neurosci. 7, 347–357 (2006).

    Article  CAS  Google Scholar 

  48. Arbib, M.A. From grasp to language: embodied concepts and the challenge of abstraction. J. Physiol. Paris 102, 4–20 (2008).

    Article  Google Scholar 

  49. Fabbri-Destro, M. & Rizzolatti, G. Mirror neurons and mirror systems in monkeys and humans. Physiology (Bethesda) 23, 171–179 (2008).

    Google Scholar 

  50. Roberts, T.F., Klein, M.E., Kubke, M.F., Wild, J.M. & Mooney, R. Telencephalic neurons monosynaptically link brainstem and forebrain premotor networks necessary for song. J. Neurosci. 28, 3479–3489 (2008).

    Article  CAS  Google Scholar 

  51. Ölveczky, B.P., Andalman, A.S. & Fee, M.S. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol. 3, e153 (2005).

    Article  Google Scholar 

  52. Dutar, P., Vu, H.M. & Perkel, D.J. Multiple cell types distinguished by physiological, pharmacological and anatomic properties in nucleus HVC of the adult zebra finch. J. Neurophysiol. 80, 1828–1838 (1998).

    Article  CAS  Google Scholar 

  53. Cardin, J.A., Raksin, J.N. & Schmidt, M.F. Sensorimotor nucleus NIf is necessary for auditory processing but not vocal motor output in the avian song system. J. Neurophysiol. 93, 2157–2166 (2005).

    Article  Google Scholar 

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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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Authors and Affiliations

  1. Department of Neurobiology, Duke University Medical Center, Durham, North Carolina, USA

    Todd F Roberts, Malavika Murugan & Richard Mooney

  2. Department of Organismic and Evolutionary Biology, Harvard University, Boston, Massachusetts, USA

    Sharon M H Gobes & Bence P Ölveczky

  3. Neuroscience Program, Wellesley College, Wellesley, Massachusetts, USA

    Sharon M H Gobes

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Contributions

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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Correspondence to Richard Mooney.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

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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