Identification of a motor-to-auditory pathway important for vocal learning (original) (raw)

References

  1. Eliades, S.J. & Wang, X. Neural substrates of vocalization feedback monitoring in primate auditory cortex. Nature 453, 1102–1106 (2008).
    Article CAS PubMed Google Scholar
  2. Schneider, D.M., Nelson, A. & Mooney, R. A synaptic and circuit basis for corollary discharge in the auditory cortex. Nature 513, 189–194 (2014).
    Article CAS PubMed PubMed Central Google Scholar
  3. Lee, S., Kruglikov, I., Huang, Z.J., Fishell, G. & Rudy, B. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat. Neurosci. 16, 1662–1670 (2013).
    Article CAS PubMed PubMed Central Google Scholar
  4. Niell, C.M. & Stryker, M.P. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65, 472–479 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  5. Wang, J. et al. Action planning and predictive coding when speaking. Neuroimage 91, 91–98 (2014).
    Article PubMed Google Scholar
  6. Hickok, G., Houde, J. & Rong, F. Sensorimotor integration in speech processing: computational basis and neural organization. Neuron 69, 407–422 (2011).
    Article CAS PubMed PubMed Central Google Scholar
  7. Crapse, T.B. & Sommer, M.A. Corollary discharge across the animal kingdom. Nat. Rev. Neurosci. 9, 587–600 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  8. Houde, J.F. & Chang, E.F. The cortical computations underlying feedback control in vocal production. Curr. Opin. Neurobiol. 33, 174–181 (2015).
    Article CAS PubMed PubMed Central Google Scholar
  9. Cullen, K.E. Sensory signals during active versus passive movement. Curr. Opin. Neurobiol. 14, 698–706 (2004).
    Article CAS PubMed Google Scholar
  10. Sperry, R.W. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43, 482–489 (1950).
    Article CAS PubMed Google Scholar
  11. Poulet, J.F. & Hedwig, B. The cellular basis of a corollary discharge. Science 311, 518–522 (2006).
    Article CAS PubMed Google Scholar
  12. von Holst, E. & Mittelstaedt, H. Das reaferenzprinzip. [The principle of reafference]. Naturwissenschaften 37, 464–476 (1950).
    Article Google Scholar
  13. Bell, C.C. An efference copy which is modified by reafferent input. Science 214, 450–453 (1981).
    Article CAS PubMed Google Scholar
  14. Doupe, A.J. & Kuhl, P.K. Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 22, 567–631 (1999).
    Article CAS PubMed Google Scholar
  15. Immelmann, K. in Bird Vocalisations (ed. Hinde, R.A.) 61–74 (Cambridge University Press, 1969).
  16. Ali, F. et al. The basal ganglia is necessary for learning spectral, but not temporal, features of birdsong. Neuron 80, 494–506 (2013).
    Article CAS PubMed PubMed Central Google Scholar
  17. Eales, L.A. Song learning in zebra finches: some effects of song model availability on what is learnt and when. Anim. Behav. 33, 1293–1300 (1985).
    Article Google Scholar
  18. Tumer, E.C. & Brainard, M.S. Performance variability enables adaptive plasticity of 'crystallized' adult birdsong. Nature 450, 1240–1244 (2007).
    Article CAS PubMed Google Scholar
  19. Roberts, T.F., Gobes, S.M., Murugan, M., Ölveczky, B.P. & Mooney, R. Motor circuits are required to encode a sensory model for imitative learning. Nat. Neurosci. 15, 1454–1459 (2012).
    Article CAS PubMed PubMed Central Google Scholar
  20. Long, M.A. & Fee, M.S. Using temperature to analyse temporal dynamics in the songbird motor pathway. Nature 456, 189–194 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  21. Vallentin, D., Kosche, G., Lipkind, D. & Long, M.A. Neural circuits. Inhibition protects acquired song segments during vocal learning in zebra finches. Science 351, 267–271 (2016).
    Article CAS PubMed PubMed Central Google Scholar
  22. Keller, G.B. & Hahnloser, R.H. Neural processing of auditory feedback during vocal practice in a songbird. Nature 457, 187–190 (2009).
    Article CAS PubMed Google Scholar
  23. Heinks-Maldonado, T.H., Mathalon, D.H., Gray, M. & Ford, J.M. Fine-tuning of auditory cortex during speech production. Psychophysiology 42, 180–190 (2005).
    Article PubMed Google Scholar
  24. 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 PubMed Google Scholar
  25. Hamaguchi, K., Tanaka, M. & Mooney, R. A distributed recurrent network contributes to temporally precise vocalizations. Neuron 91, 680–693 (2016).
    Article CAS PubMed PubMed Central Google Scholar
  26. Alvarez-Buylla, A., Kirn, J.R. & Nottebohm, F. Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science 249, 1444–1446 (1990).
    Article CAS PubMed Google Scholar
  27. Sohrabji, F., Nordeen, E.J. & Nordeen, K.W. Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. Behav. Neural Biol. 53, 51–63 (1990).
    Article CAS PubMed Google Scholar
  28. Scharff, C. & Nottebohm, F. A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning. J. Neurosci. 11, 2896–2913 (1991).
    Article CAS PubMed PubMed Central Google Scholar
  29. Akutagawa, E. & Konishi, M. New brain pathways found in the vocal control system of a songbird. J. Comp. Neurol. 518, 3086–3100 (2010).
    Article PubMed Google Scholar
  30. Mooney, R. Different subthreshold mechanisms underlie song selectivity in identified HVc neurons of the zebra finch. J. Neurosci. 20, 5420–5436 (2000).
    Article CAS PubMed PubMed Central Google Scholar
  31. Tschida, K.A. & Mooney, R. Deafening drives cell-type-specific changes to dendritic spines in a sensorimotor nucleus important to learned vocalizations. Neuron 73, 1028–1039 (2012).
    Article CAS PubMed PubMed Central Google Scholar
  32. 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 PubMed Google Scholar
  33. 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 PubMed Google Scholar
  34. Hattox, A.M. & Nelson, S.B. Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. J. Neurophysiol. 98, 3330–3340 (2007).
    Article PubMed Google Scholar
  35. Kim, E.J., Juavinett, A.L., Kyubwa, E.M., Jacobs, M.W. & Callaway, E.M. Three types of cortical layer 5 neurons that differ in brain-wide connectivity and function. Neuron 88, 1253–1267 (2015).
    Article CAS PubMed PubMed Central Google Scholar
  36. Long, M.A., Jin, D.Z. & Fee, M.S. Support for a synaptic chain model of neuronal sequence generation. Nature 468, 394–399 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  37. Liberti, W.A., III et al. Unstable neurons underlie a stable learned behavior. Nat. Neurosci. 19, 1665–1671 (2016).
    Article CAS PubMed PubMed Central Google Scholar
  38. Picardo, M.A. et al. Population-level representation of a temporal sequence underlying song production in the zebra finch. Neuron 90, 866–876 (2016).
    Article CAS PubMed PubMed Central Google Scholar
  39. Hamaguchi, K., Tschida, K.A., Yoon, I., Donald, B.R. & Mooney, R. Auditory synapses to song premotor neurons are gated off during vocalization in zebra finches. Elife 3, e01833 (2014).
    Article PubMed PubMed Central CAS Google Scholar
  40. Zhou, P., Resendez, S.L., Stuber, G.D., Kass, R.E. & Paninski, L. Efficient and accurate extraction of in vivo calcium signals from microendoscope video data. Preprint at https://arxiv.org/abs/1605.07266 (2016).
  41. 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 PubMed Google Scholar
  42. 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 PubMed PubMed Central Google Scholar
  43. Yang, C.F. et al. Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell 153, 896–909 (2013).
    Article CAS PubMed PubMed Central Google Scholar
  44. Nordeen, K.W. & Nordeen, E.J. Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behav. Neural Biol. 57, 58–66 (1992).
    Article CAS PubMed Google Scholar
  45. Brainard, M.S. & Doupe, A.J. Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404, 762–766 (2000).
    Article CAS PubMed Google Scholar
  46. Williams, H., Crane, L.A., Hale, T.K., Esposito, M.A. & Nottebohm, F. Right-side dominance for song control in the zebra finch. J. Neurobiol. 23, 1006–1020 (1992).
    Article CAS PubMed Google Scholar
  47. Bauer, E.E. et al. A synaptic basis for auditory-vocal integration in the songbird. J. Neurosci. 28, 1509–1522 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  48. Nelson, A. et al. A circuit for motor cortical modulation of auditory cortical activity. J. Neurosci. 33, 14342–14353 (2013).
    Article CAS PubMed PubMed Central Google Scholar
  49. Mandelblat-Cerf, Y., Las, L., Denisenko, N. & Fee, M.S. A role for descending auditory cortical projections in songbird vocal learning. Elife 3 (2014).
  50. Gale, S.D., Person, A.L. & Perkel, D.J. A novel basal ganglia pathway forms a loop linking a vocal learning circuit with its dopaminergic input. J. Comp. Neurol. 508, 824–839 (2008).
    Article PubMed Google Scholar

Download references