Neural Circuits Underlying Vocal Learning in Songbirds

  • Jon T. SakataEmail author
  • Yoko Yazaki-Sugiyama
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 71)


Songbirds have become the most prominent animal model to reveal the neural mechanisms underlying vocal learning. Similar to other forms of sensorimotor learning, vocal learning in songbirds entails acquiring a sensory representation of communicative sounds (songs) and learning the motor commands to produce the memorized sounds. The process of song learning in songbirds is highly similar to the process of speech acquisition in humans; as such, there are extensive efforts to discover and characterize the neural circuitry for song learning in songbirds to gain insight into potential mechanisms underlying speech acquisition in humans. This chapter provides a conceptual review of the neural circuits regulating the sensory and sensorimotor learning of birdsong as well as the mechanisms underlying variation in the extent and fidelity of vocal learning (e.g., timing of song learning, social interactions, and biological predispositions). Findings from various songbird species are integrated to provide a comparative perspective on neural mechanisms. In addition, outstanding questions and new research directions for birdsong research are considered.


Auditory feedback Birdsong Critical period Dopamine HVC Locus coeruleus NCM Norepinephrine Sensory learning Speech Ventral tegmental area Zebra finch 



We thank Mimi Kao for helpful comments on a previous version of the manuscrFipt.

Compliance With Ethics Requirements

Jon T. Sakata declares that he has no conflict of interest.

Yoko Yazaki-Sugiyama declares that she has no conflict of interest.


  1. Achiro JM, Bottjer SW (2013) Neural representation of a target auditory memory in a cortico-basal ganglia pathway. J Neurosci 33:14475–14488. Scholar
  2. Achiro JM, Shen J, Bottjer SW (2017) Neural activity in cortico-basal ganglia circuits of juvenile songbirds encodes performance during goal-directed learning. eLife 6:e26973. Scholar
  3. Adret P, Meliza CD, Margoliash D (2012) Song tutoring in presinging zebra finch juveniles biases a small population of higher-order song-selective neurons toward the tutor song. J Neurophysiol 108:1977–1987. Scholar
  4. Akutagawa E, Konishi M (2010) New brain pathways found in the vocal control system of a songbird. J Comp Neurol 518:3086–3100. Scholar
  5. Ali F, Otchy TM, Pehlevan C, Fantana AL, Burak Y, Ölveczky BP (2013) The basal ganglia is necessary for learning spectral, but not temporal, features of birdsong. Neuron 80:494–506. Scholar
  6. Alliende JA, Méndez JM, Goller F, Mindlin GB (2010) Hormonal acceleration of song development illuminates motor control mechanism in canaries. Dev Neurobiol 70:943–960. Scholar
  7. Andalman AS, Fee MS (2009) A basal ganglia-forebrain circuit in the songbird biases motor output to avoid vocal errors. PNAS USA 106:12518–12523. Scholar
  8. Araki M, Bandi MM, Yazaki-Sugiyama Y (2016) Mind the gap: neural coding of species identity in birdsong prosody. Science 354:1282–1287. Scholar
  9. Aronov D, Andalman AS, Fee MS (2008) A specialized forebrain circuit for vocal babbling in the juvenile songbird. Science 320:630–634. Scholar
  10. Balmer TS, Carels VM, Frisch JL, Nick TA (2009) Modulation of perineuronal nets and parvalbumin with developmental song learning. J Neurosci 29:12878–12885. Scholar
  11. Basham ME, Nordeen EJ, Nordeen KW (1996) Blockade of nmda receptors in the anterior forebrain impairs sensory acquisition in the zebra finch (Poephila guttata). Neurobiol Learn Mem 66:295–304. Scholar
  12. Bateson PPG (1966) The characteristics and context of imprinting. Biol Rev 41:177–217. Scholar
  13. Beecher MD (2017) Birdsong learning as a social process. Anim Behav 124:233–246. Scholar
  14. Benichov JI, Benezra SE, Vallentin D, Globerson E, Long MA, Tchernichovski O (2016) The forebrain song system mediates predictive call timing in female and male zebra finches. Curr Biol 26:309–318. Scholar
  15. Bolhuis JJ, Gahr M (2006) Neural mechanisms of birdsong memory. Nat Rev Neurosci 7:347–357. Scholar
  16. Bolhuis JJ, Moorman S (2015) Birdsong memory and the brain: in search of the template. Neurosci Biobehav Rev 50:41–55. Scholar
  17. Bottjer SW, Alderete TL, Chang D (2010) Conjunction of vocal production and perception regulates expression of the immediate early gene ZENK in a novel cortical region of songbirds. J Neurophysiol 103(4):1833–1842.
  18. Bottjer SW, Altenau B (2010) Parallel pathways for vocal learning in basal ganglia of songbirds. Nature Neurosci 13:153–155. Scholar
  19. Bottjer SW, Miesner EA, Arnold AP (1984) Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224:901–903. Scholar
  20. Bradbury JW, Vehrencamp SL (2011) Principles of animal communication, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  21. Brainard MS, Doupe AJ (2000) Auditory feedback in learning and maintenance of vocal behaviour. Nat Rev Neurosci 1:31–40. Scholar
  22. Brainard MS, Doupe AJ (2002) What songbirds teach us about learning. Nature 417:351–358. Scholar
  23. Brainard MS, Doupe AJ (2013) Translating birdsong: songbirds as a model for basic and applied medical research. Annu Rev Neurosci 36:489–517. Scholar
  24. Canopoli A, Herbst JA, Hahnloser RHR (2014) A higher sensory brain region is involved in reversing reinforcement-induced vocal changes in a songbird. J Neurosci 34:7018–7026. Scholar
  25. Canopoli A, Zai A, Hahnloser R (2016) Lesions of a higher auditory brain area during a sensorimotor period do not impair birdsong learning. Matters (Zürich).
  26. Carouso-Peck S, Goldstein MH (2019) Female social feedback reveals non-imitative mechanisms of vocal learning in zebra finches. Curr Biol 29:631–636. Scholar
  27. Castelino CB, Schmidt MF (2010) What birdsong can teach us about the central noradrenergic system. J Chem Neuroanat 39:96–111. Scholar
  28. Catchpole CK, Slater PJB (2008) Bird song: biological themes and variations. Cambridge University PressGoogle Scholar
  29. Charlesworth JD, Tumer EC, Warren TL, Brainard MS (2011) Learning the microstructure of successful behavior. Nature Neurosci 14:373–380. Scholar
  30. Charlesworth JD, Warren TL, Brainard MS (2012) Covert skill learning in a cortical-basal ganglia circuit. Nature 486:251–255. Scholar
  31. Chen Y, Matheson LE, Sakata JT (2016) Mechanisms underlying the social enhancement of vocal learning in songbirds. PNAS USA 113:6641–6646. Scholar
  32. Chen R, Puzerey PA, Roeser AC, Riccelli TE, Podury A, Maher K, Farhang A, Goldberg J (2019) Songbird ventral basal ganglia sends performance error signals to dopaminergic midbrain. Neuron 103:266–276.
  33. Clayton NS (1989) The effects of cross-fostering on selective song learning in estrildid finches. Behav 109:163–175.
  34. Cornez G, ter Haar SM, Cornil CA, Balthazart J (2015) Anatomically discrete sex differences in neuroplasticity in zebra finches as reflected by perineuronal nets. PLoS One 10:e0123199. Scholar
  35. Cornez G, Madison FN, Van A d L, Cornil C, Yoder KM, Ball GF, Balthazart J (2017) Perineuronal nets and vocal plasticity in songbirds: a proposed mechanism to explain the difference between closed-ended and open-ended learning. Dev Neurobiol 77:975–994. Scholar
  36. Cornez G, Jonckers E, ter Haar SM, Van der Linden A, Cornil CA, Balthazart J (2018) Timing of perineuronal net development in the zebra finch song control system correlates with developmental song learning. Proc Royal Soc B Biol Sci 285:20180849. Scholar
  37. de Villers-Sidani E, Chang EF, Bao S, Merzenich MM (2007) Critical period window for spectral tuning defined in the primary auditory cortex (a1) in the rat. J Neurosci 27:180–189.
  38. Dhawale AK, Smith MA, Ölveczky BP (2017) The role of variability in motor learning. Ann Rev Neurosci 40:479–498. Scholar
  39. Doupe AJ, Kuhl PK (1999) Birdsong and human speech: common themes and mechanisms. Ann Rev Neurosci 22:567–631. Scholar
  40. Doupe AJ, Solis MM (1997) Song- and order-selective neurons develop in the songbird anterior forebrain during vocal learning. J Neurobiol 33:694–709.<694::AID-NEU13>3.0.CO;2-9CrossRefPubMedGoogle Scholar
  41. Doupe AJ, Perkel DJ, Reiner A, Stern EA (2005) Birdbrains could teach basal ganglia research a new song. TINS 28:353–363. Scholar
  42. Doya K, Sejnowski TJ (1995) A novel reinforcement model of birdsong vocalization learning. In: Advances in neural information processing. MIT Press, pp 101–108Google Scholar
  43. Düring DN, Elemans CP (2016) Embodied motor control of avian vocal production. In Vertebrate sound production and acoustic communication. Springer, Cham. pp 119–157Google Scholar
  44. Fagiolini M, Hensch TK (2000) Inhibitory threshold for critical-period activation in primary visual cortex. Nature 404:183–186. Scholar
  45. Fee MS, Goldberg JH (2011) A hypothesis for basal ganglia-dependent reinforcement learning in the songbird. Neurosci 198:152–170. Scholar
  46. Fehér O, Wang H, Saar S, Mitra PP, Tchernichovski O (2009) De novo establishment of wild-type song culture in the zebra finch. Nature 459:564–568. Scholar
  47. Fields HL, Hjelmstad GO, Margolis EB, Nicola SM (2007) Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Ann Rev Neurosci 30:289–316. Scholar
  48. Funabiki Y, Konishi M (2003) Long memory in song learning by zebra finches. J Neurosci 23:6928–6935. Scholar
  49. Gadagkar V, Puzerey PA, Chen R, Baird-Daniel E, Farhang AR, Goldberg JH (2016) Dopamine neurons encode performance error in singing birds. Science 354:1278–1282. Scholar
  50. Gahr M, Metzdorf R (1997) Distribution and dynamics in the expression of androgen and estrogen receptors in vocal control systems of songbirds. Brain Res Bull 44:509–517. Scholar
  51. Gale SD, Perkel DJ (2010) A basal ganglia pathway drives selective auditory responses in songbird dopaminergic neurons via disinhibition. J Neurosci 30:1027–1037. Scholar
  52. Gale SD, Person AL, Perkel DJ (2008) A novel basal ganglia pathway forms a loop linking a vocal learning circuit with its dopaminergic input. J Comp Neurol 508:824–839. Scholar
  53. Gardner TJ, Naef F, Nottebohm F (2005) Freedom and rules: the acquisition and reprogramming of a bird’s learned song. Science 308:1046–1049. Scholar
  54. George JM, Jin H, Woods WS, Clayton DF (1995) Characterization of a novel protein regulated during the critical period for song learning in the zebra finch. Neuron 15:361–372. Scholar
  55. Gobes SMH, Bolhuis JJ (2007) Birdsong memory: a neural dissociation between song recognition and production. Curr Biol 17:789–793. Scholar
  56. Gobes SMH, Jennings RB, Maeda RK (2017) The sensitive period for auditory-vocal learning in the zebra finch: consequences of limited-model availability and multiple-tutor paradigms on song imitation. Behav Process 163:5–12. Scholar
  57. Goldstein MH, Schwade JA (2008) Social feedback to infants’ babbling facilitates rapid phonological learning. Psychol Sci 19:515–523. Scholar
  58. Goldstein MH, King AP, West MJ (2003) Social interaction shapes babbling: testing parallels between birdsong and speech. PNAS USA 100:8030–8035. Scholar
  59. Hahnloser RH, Kotowicz A (2010) Auditory representations and memory in birdsong learning. Curr Opin Neurobiol 20:332–339. Scholar
  60. Hamilton KS, King AP, Sengelaub DR, West MJ (1997) A brain of her own: a neural correlate of song assessment in a female songbird. Neurobiol Learn Mem 68:325–332. Scholar
  61. Happel MFK, Niekisch H, Castiblanco Rivera LL, Ohl FW, Deliano M, Frischknecht R (2014) Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex. PNAS USA 111:2800–2805. Scholar
  62. Hayase S, Wang H, Ohgushi E, Kobayashi M, Mori C, Horita H, Mineta K, Liu W, Wada K (2018) Vocal practice regulates singing activity–dependent genes underlying age-independent vocal learning in songbirds. PLoS Biol 16:e2006537. Scholar
  63. Heinrich JE, Singh TD, Sohrabji F, Nordeen KW, Nordeen EJ (2002) Developmental and hormonal regulation of NR2A mRNA in forebrain regions controlling avian vocal learning. J Neurobiol 51:149–159.
  64. Heinrich J, Nordeen K, Nordeen E (2005) Dissociation between extension of the sensitive period for avian vocal learning and dendritic spine loss in the song nucleus LMAN. Neurobiol Learn Mem 83:143–150. Scholar
  65. Hensch TK (2004) Critical period regulation. Ann Rev Neurosci 27:549–579. Scholar
  66. Hickok G, Houde J, Rong F (2011) Sensorimotor integration in speech processing: computational basis and neural organization. Neuron 69:407–422. Scholar
  67. Hikosaka O, Bromberg-Martin E, Hong S, Matsumoto M (2008) New insights on the subcortical representation of reward. Curr Opin Neurobiol 18:203–208. Scholar
  68. Hisey E, Kearney MG, Mooney R (2018) A common neural circuit mechanism for internally guided and externally reinforced forms of motor learning. Nature Neurosci 21:589–597. Scholar
  69. Hoffmann LA, Sober SJ (2014) Vocal generalization depends on gesture identity and sequence. J Neurosci 34:5564–5574. Scholar
  70. Hoffmann LA, Saravanan V, Wood AN, He L, Sober SJ (2016) Dopaminergic contributions to vocal learning. J Neurosci 36:2176–2189. Scholar
  71. Horn G (2004) Pathways of the past: the imprint of memory. Nat Rev Neurosci 5:108–120CrossRefGoogle Scholar
  72. Houx BB, Cate CT (1998) Do contingencies with tutor behaviour influence song learning in zebra finches? Behaviour 135:599–614. Scholar
  73. Ikeda MZ, Jeon SD, Cowell RA, Remage-Healey L (2015) Norepinephrine modulates coding of complex vocalizations in the songbird auditory cortex independent of local neuroestrogen synthesis. J Neurosci 35:9356–9368. Scholar
  74. Iyengar S, Bottjer SW (2002) The role of auditory experience in the formation of neural circuits underlying vocal learning in zebra finches. J Neurosci 22:946–958. Scholar
  75. James LS, Sakata JT (2017) Learning biases underlie “universals” in avian vocal sequencing. Curr Biol 27:3676–3682.e4. Scholar
  76. Jin H, Clayton DF (1997) Localized changes in immediate-early gene regulation during sensory and motor learning in zebra finches. Neuron 19:1049–1059. Scholar
  77. Kao MH, Doupe AJ, Brainard MS (2005) Contributions of an avian basal ganglia–forebrain circuit to real-time modulation of song. Nature 433:638–643CrossRefGoogle Scholar
  78. Keller GB, Hahnloser RHR (2009) Neural processing of auditory feedback during vocal practice in a songbird. Nature 457:187–190. Scholar
  79. Knudsen EI (2004) Sensitive periods in the development of the brain and behavior. J Cogn Neurosci 16:1412–1425. Scholar
  80. Konishi M (2004) The role of auditory feedback in birdsong. Ann N Y Acad Sci 1016:463–475. Scholar
  81. Kozhevnikov AA, Fee MS (2007) Singing-related activity of identified HVC neurons in the zebra finch. J Neurophysiol 97:4271–4283.
  82. Kuhl PK (2007) Is speech learning ‘gated’ by the social brain? Dev Science 10:110–120. Scholar
  83. Kuhl PK (2010) Brain mechanisms in early language acquisition. Neuron 67:713–727. Scholar
  84. Kuhl PK, Tsao F-M, Liu H-M (2003) Foreign-language experience in infancy: effects of short-term exposure and social interaction on phonetic learning. PNAS USA 100:9096–9101. Scholar
  85. Lachlan RF, van Heijningen CAA, ter Haar SM, ten Cate C (2016) Zebra finch song phonology and syntactical structure across populations and continents—a computational comparison. Front Psychol 7:980. Scholar
  86. Lei H, Mooney R (2010) Manipulation of a central auditory representation shapes learned vocal output. Neuron 65:122–134. Scholar
  87. Leonardo A (2004) Experimental test of the birdsong error-correction model. Proc Natl Acad Sci 101:16935–16940.
  88. Leonardo A, Konishi M (1999) Decrystallization of adult birdsong by perturbation of auditory feedback. Nature 399:466–470. Scholar
  89. Lewandowski B, Vyssotski A, Hahnloser RHR, Schmidt M (2013) At the interface of the auditory and vocal motor systems: NIf and its role in vocal processing, production and learning. J Physiol-Paris 107:178–192. Scholar
  90. Li R, Sakaguchi H (1997) Cholinergic innervation of the song control nuclei by the ventral paleostriatum in the zebra finch: a double-labeling study with retrograde fluorescent tracers and choline acetyltransferase immunohistochemistry. Brain Res 763:239–246. Scholar
  91. Lipkind D, Marcus GF, Bemis DK, Sasahara K, Jacoby N, Takahasi M, Suzuki K, Fehér O, Ravbar P, Okanoya K, Tchernichovski O (2013) Stepwise acquisition of vocal combinatorial capacity in songbirds and human infants. Nature 498:104–108. Scholar
  92. Livingston FS, Mooney R (1997) Development of intrinsic and synaptic properties in a forebrain nucleus essential to avian song learning. J Neurosci 17:8997–9009. Scholar
  93. London SE, Clayton DF (2008) Functional identification of sensory mechanisms required for developmental song learning. Nature Neurosci 11:579–586. Scholar
  94. Lorenz KZ (1935) Der kumpan in der umwelt des vogels. der artgenosse als auslösendes moment sozialer verhaltensweisen. J Ornithologie 83: 137–215, 289–413.
  95. Lytle SR, Kuhl PK (2017) Social interaction and language acquisition: toward a neurobiological view. In: Fernández EM, Cairns HS (eds) The handbook of psycholinguistics. John Wiley & Sons, Inc., Hoboken, pp 615–634CrossRefGoogle Scholar
  96. Mandelblat-Cerf Y, Las L, Denisenko N, Fee MS (2014) A role for descending auditory cortical projections in songbird vocal learning. eLife 3.
  97. Margoliash D, Schmidt MF (2010) Sleep, off-line processing, and vocal learning. Brain Lang 115:45–58. Scholar
  98. Marler P (1997) Three models of song learning: evidence from behavior. J Neurobiol 33:501–516CrossRefGoogle Scholar
  99. Mets DG, Brainard MS (2018) Genetic variation interacts with experience to determine interindividual differences in learned song. PNAS USA 115:421–426. Scholar
  100. Mets DG, Brainard MS (2019) Learning is enhanced by tailoring instruction to individual genetic differences. eLife 8.
  101. Michel GF, Tyler AN (2005) Critical period: a history of the transition from questions of when, to what, to how. Dev Psychobiol 46:156–162. Scholar
  102. Mooney R (2009) Neurobiology of song learning. Curr Opin Neurobiol 19:654–660. Scholar
  103. Moore JM, Woolley SM (2019) Emergent tuning for learned vocalizations in auditory cortex. Nat Neurosci 22:1469–1476.
  104. Morales M, Margolis EB (2017) Ventral tegmental area: cellular heterogeneity, connectivity and behaviour. Nat Rev Neurosci 18:73–85. Scholar
  105. Moseley DL, Joshi NR, Prather JF, Podos J, Remage-Healey L (2017) A neuronal signature of accurate imitative learning in wild-caught songbirds (swamp sparrows, Melospiza georgiana). Sci Reports 7:17320. Scholar
  106. Murphy K, James LS, Sakata JT, Prather JF (2017) Advantages of comparative studies in songbirds to understand the neural basis of sensorimotor integration. J Neurophysiol 118:800–816. Scholar
  107. Nelson DA (2000) A preference for own-subspecies’ song guides vocal learning in a song bird. PNAS USA 97:13348–13353. Scholar
  108. Nicholson DA, Roberts TF, Sober SJ (2018) Thalamostriatal and cerebellothalamic pathways in a songbird, the Bengalese finch. J Comp Neurol 526:1550–1570. Scholar
  109. Nick TA (2015) Models of vocal learning in the songbird: historical frameworks and the stabilizing critic. Dev Neurobiol 75:1091–1113. Scholar
  110. Nick TA, Konishi M (2005) Neural song preference during vocal learning in the zebra finch depends on age and state. J Neurobiol 62:231–42.
  111. Nordeen KW, Nordeen EJ (1992) Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behav Neural Biol 57:58–66. Scholar
  112. Nordeen EJ, Holtzman DA, Nordeen KW (2009) Increased Fos expression among midbrain dopaminergic cell groups during birdsong tutoring. Eur J Neurosci 30:662–670. Scholar
  113. Nowicki S, Searcy WA (2014) The evolution of vocal learning. Curr Opin Neurobiol 28:48–53. Scholar
  114. O’Connell LA, Hofmann HA (2011) The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 519:3599–3639. Scholar
  115. Odom KJ, Hall ML, Riebel K, Omland KE, Langmore NE (2014) Female song is widespread and ancestral in songbirds. Nature Comm 5:3379. Scholar
  116. Okubo TS, Mackevicius EL, Payne HL, Lynch GF, Fee MS (2015) Growth and splitting of neural sequences in songbird vocal development. Nature 528:352–357. Scholar
  117. Petkov CI, Jarvis ED (2012) Birds, primates, and spoken language origins: behavioral phenotypes and neurobiological substrates. Front Evol Neurosci 4.
  118. Phan ML, Pytte CL, Vicario DS (2006) Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds. PNAS USA 103:1088–1093. Scholar
  119. Pidoux L, Le Blanc P, Levenes C, Leblois A (2018) A subcortical circuit linking the cerebellum to the basal ganglia engaged in vocal learning. eLife 7.
  120. Pizzorusso T, Medini P, Landi S, Baldini S, Berardi N, Maffei L (2006) Structural and functional recovery from early monocular deprivation in adult rats. PNAS USA 103:8517–8522. Scholar
  121. Plamondon SL, Rose GJ, Goller F (2010) Roles of syntax information in directing song development in white-crowned sparrows (Zonotrichia leucophrys). J Comp Psychol 124:117–132. Scholar
  122. Prather JF (2013) Auditory signal processing in communication: perception and performance of vocal sounds. Hearing Res 305:144–155. Scholar
  123. Riede T, Goller F (2014) Morphological basis for the evolution of acoustic diversity in oscine songbirds. Proc R Soc B Biol Sci 281:20132306–20132306. Scholar
  124. Roberts TF, Mooney R (2013) Motor circuits help encode auditory memories of vocal models used to guide vocal learning. Hearing Res 303:48–57. Scholar
  125. Roberts TF, Tschida KA, Klein ME, Mooney R (2010) Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning. Nature 463:948–952. Scholar
  126. Roberts TF, Gobes SMH, Murugan M, Ölveczky BP, Mooney R (2012) Motor circuits are required to encode a sensory model for imitative learning. Nature Neurosci 15:1454–1459. Scholar
  127. Roberts TF, Hisey E, Tanaka M, Kearney MG, Chattree G, Yang CF, Shah NM, Mooney R (2017) Identification of a motor-to-auditory pathway important for vocal learning. Nature Neurosci 20:978–986. Scholar
  128. Sakaguchi H (1996) Sex differences in the developmental changes of GABAergic neurons in zebra finch song control nuclei. Exp Brain Res 108:62–68.
  129. Sakata JT, Brainard MS (2006) Real-time contributions of auditory feedback to avian vocal motor control. J Neurosci 26:9619–9628. Scholar
  130. Sakata JT, Brainard MS (2008) Online contributions of auditory feedback to neural activity in avian song control circuitry. J Neurosci 28:11378–11390. Scholar
  131. Sara SJ, Bouret S (2012) Orienting and reorienting: the locus coeruleus mediates cognition through arousal. Neuron 76:130–141. Scholar
  132. Sasaki A, Sotnikova TD, Gainetdinov RR, Jarvis ED (2006) Social context-dependent singing-regulated dopamine. J Neurosci 26:9010–9014. Scholar
  133. Sato D, Mori C, Sawai A, Wada K (2016) Familial bias and auditory feedback regulation of vocal babbling patterns during early song development. Sci Reports 6.
  134. Scharff C, Nottebohm F (1991) 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. Scholar
  135. Schultz W (2017) Reward prediction error. Curr Biol 27:R369–R371. Scholar
  136. Shea SD, Margoliash D (2003) Basal forebrain cholinergic modulation of auditory activity in the zebra finch song system. Neuron 40:1213–1226. Scholar
  137. Singh TD, Basham ME, Nordeen EJ, Nordeen KW (2000) Early sensory and hormonal experience modulate age-related changes in NR2B mRNA within a forebrain region controlling avian vocal learning. J Neurobiol 44:82–94.<82::AID-NEU8>3.0.CO;2-WCrossRefPubMedGoogle Scholar
  138. Snowdon CT, Hausberger M (1997) Social influences on vocal development. Cambridge University PressGoogle Scholar
  139. Sober SJ, Brainard MS (2009) Adult birdsong is actively maintained by error correction. Nature Neurosci 12:927–931. Scholar
  140. Solis MM, Doupe AJ (1999) Contributions of tutor and bird’s own song experience to neural selectivity in the songbird anterior forebrain. J Neurosci 19:4559–4584. Scholar
  141. Sonntag M, Blosa M, Schmidt S, Rübsamen R, Morawski M (2015) Perineuronal nets in the auditory system. Hearing Res 329:21–32. Scholar
  142. Southwell DG, Froemke RC, Alvarez-Buylla A, Stryker MP, Gandhi SP (2010) Cortical plasticity induced by inhibitory neuron transplantation. Science 327:1145–1148. Scholar
  143. Stockard C (1921) Developmental rate and structural expression: an experimental study of twins, ‘double monsters’ and single deformities, and the interaction among embryonic organs during their origin and development. Am J Anat 28:115–277.
  144. Sutton RS, Barto AG (1998) Reinforcement learning: an introduction. MIT PressGoogle Scholar
  145. Tachibana RO, Takahasi M, Hessler NA, Okanoya K (2017) Maturation-dependent control of vocal temporal plasticity in a songbird: maturation effect on temporal plasticity. Dev Neurobiol 77:995–1006. Scholar
  146. Takesian AE, Hensch TK (2013) Balancing plasticity/stability across brain development. Prog Brain Res 207:3–34. Scholar
  147. Tanaka M, Sun F, Li Y, Mooney R (2018) A mesocortical dopamine circuit enables the cultural transmission of vocal behaviour. Nature 563:117–120. Scholar
  148. Tang Y, Stryker MP, Alvarez-Buylla A, Espinosa JS (2014) Cortical plasticity induced by transplantation of embryonic somatostatin or parvalbumin interneurons. PNAS USA 111:18339–18344. Scholar
  149. Tchernichovski O, Marcus G (2014) Vocal learning beyond imitation: mechanisms of adaptive vocal development in songbirds and human infants. Curr Opin Neurobiol 28:42–47. Scholar
  150. Tchernichovski O, Mitra PP, Lints T, Nottebohm F (2001) Dynamics of the vocal imitation process: how a zebra finch learns its song. Science 291:2564–2569. Scholar
  151. ter Haar SM, Kaemper W, Stam K, Levelt CC, ten Cate C (2014) The interplay of within-species perceptual predispositions and experience during song ontogeny in zebra finches (Taeniopygia guttata). Proc R Soc B Biol Sci 281:20141860–20141860. Scholar
  152. Thorpe WH (2008) The learning of song patterns by birds, with especial reference to the song of the chaffinch Fringilla coelebs. Ibis 100:535–570. Scholar
  153. Troyer TW, Doupe AJ (2000) An associational model of birdsong sensorimotor learning I. efference copy and the learning of song syllables. J Neurophysiol 84:1204–1223. Scholar
  154. Tumer EC, Brainard MS (2007) Performance variability enables adaptive plasticity of ‘crystallized’ adult birdsong. Nature 450:1240–1244. Scholar
  155. Vallentin D, Kosche G, Lipkind D, Long MA (2016) Inhibition protects acquired song segments during vocal learning in zebra finches. Science 351:267–271. Scholar
  156. Velho TAF, Lu K, Ribeiro S, Pinaud R, Vicario D, Mello CV (2012) Noradrenergic control of gene expression and long-term neuronal adaptation evoked by learned vocalizations in songbirds. PLoS One 7:e36276. Scholar
  157. Vyssotski AL, Stepien AE, Keller GB, Hahnloser RHR (2016) A neural code that is isometric to vocal output and correlates with its sensory consequences. PLoS Biol 14:e2000317. Scholar
  158. Wang Y, Brzozowska-Prechtl A, Karten HJ (2010) Laminar and columnar auditory cortex in avian brain. PNAS USA 107:12676–12681. Scholar
  159. Wang H, Sawai A, Toji N, Sugioka R, Shibata Y, Suzuki Y, Ji Y, Hayase S, Akama S, Sese J, Wada K (2019) Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds. PLoS Biol 17.
  160. Warren TL, Tumer EC, Charlesworth JD, Brainard MS (2011) Mechanisms and time course of vocal learning and consolidation in the adult songbird. J Neurophysiol 106:1806–1821.
  161. Warren TL, Charlesworth JD, Tumer EC, Brainard MS (2012) Variable sequencing is actively maintained in a well learned motor skill. J Neurosci 32:15414–15425. Scholar
  162. Werker JF, Hensch TK (2015) Critical periods in speech perception: new directions. Ann Rev Psychol 66:173–196. Scholar
  163. West MJ, King AP (1988) Female visual displays affect the development of male song in the cowbird. Nature 334:244–246. Scholar
  164. West MJ, King AP, Eastzer DH (1981) Validating the female bioassay of cowbird song: relating differences in song potency to mating success. Anim Behav 29:490–501. Scholar
  165. Westermann G, Miranda E (2004) A new model of sensorimotor coupling in the development of speech. Brain Lang 89:393–400. Scholar
  166. Whaling CS, Solis MM, Doupe AJ, Soha JA, Marler P (1997) Acoustic and neural bases for innate recognition of song. PNAS USA 94:12694–12698. Scholar
  167. Wheatcroft D, Qvarnström A (2015) A blueprint for vocal learning: auditory predispositions from brains to genomes. Biol Lett 11:20150155. Scholar
  168. White SA, Livingston FS, Mooney R (1999) Androgens modulate NMDA receptor–mediated EPSCs in the zebra finch song system. J Neurophysiol 82:2221–2234. Scholar
  169. Woolley SMN (2017) Early experience and auditory development in songbirds. In: Cramer KS, Coffin AB, Fay RR, Popper AN (eds) Auditory development and plasticity: in honor of Edwin W Rubel. Springer International Publishing, Cham, pp 193–217CrossRefGoogle Scholar
  170. Xiao L, Chattree G, Oscos FG, Cao M, Wanat MJ, Roberts TF (2018) A basal ganglia circuit sufficient to guide birdsong learning. Neuron 98:208–221.e5. Scholar
  171. Yanagihara S, Hessler NA (2006) Modulation of singing-related activity in the songbird ventral tegmental area by social context. Eur J Neurosci 24:3619–3627. Scholar
  172. Yanagihara S, Yazaki-Sugiyama Y (2016) Auditory experience-dependent cortical circuit shaping for memory formation in bird song learning. Nature Comm 7:11946. Scholar
  173. Yazaki-Sugiyama Y (2019) Neuronal mechanisms regulating the critical period of sensory experience-dependent song learning. Neurosci Res 140:53–58.
  174. Yazaki-Sugiyama Y, Mooney R (2004) Sequential learning from multiple tutors and serial retuning of auditory neurons in a brain area important to birdsong learning. J Neurophysiol 92:2771–2788. Scholar
  175. Zann R (1993) Structure, sequence and evolution of song elements in wild Australian zebra finches. Auk 110:702–715. Scholar
  176. Zevin JD, Seidenberg MS, Bottjer SW (2004) Limits on reacquisition of song in adult zebra finches exposed to white noise. J Neurosci 24:5849–5862.
  177. Zhao W, Garcia-Oscos F, Dinh D, Roberts TF (2019) Inception of memories that guide vocal learning in the songbird. Science 366:83–89.

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Biology and Centre for Research in Brain, Language, and MusicMcGill UniversityMontrealCanada
  2. 2.Okinawa Institute of Science and Technology (OIST) Graduate UniversityOkinawaJapan
  3. 3.International Research Center for Neurointelligence (IRCN)The University of TokyoTokyoJapan

Personalised recommendations