Linking Features of Genomic Function to Fundamental Features of Learned Vocal Communication

  • Sarah E. LondonEmail author
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 71)


Learned vocal communication emerges from the coordination of sensory and motor learning, reflects the function of a distributed but integrated neural circuit, and unfolds across several timescales, often occurring in maturing animals. Because nearly all brain organization and function originates from patterns of genomic activation, it is crucial to understand principles of how the genome works in order to understand how learned vocal communication arises. In this chapter, the fact that genome functions have high evolutionary conservation will be leveraged to provide a conceptual guide for how research using a species of songbird, the zebra finch, can deepen and expand clinical findings from humans. Additionally, this chapter provides examples for how studies in the zebra finch can uncover fundamental processes of learned vocal communication that are of value for understanding human speech and language. Examples include the organization of specialized neural circuits, responses to social communication experiences, activation of motor plans, and consideration of how the age and sex of the individual intersect with vocal communication skills, all of which have potential to inform on vocal learning mechanisms in humans. Together, our current state of knowledge advances the idea that humans and songbirds do not simply share superficial parallels; rather, they share deep biological properties to accomplish the complex, multi-level processes required for learning and producing meaningful communication patterns.


Behavior Critical period Epigenetics Genome Histone Learning and memory mTOR Neural development Sensitive period Sex differences Song Songbird Zebra finch 


Compliance with Ethics Requirements

Sarah E. London declares that she has no conflict of interest.


  1. Abe K, Matsui S, Watanabe D (2015) Transgenic songbirds with suppressed or enhanced activity of CREB transcription factor. Proc Natl Acad Sci USA 112(24):7599–7604. Scholar
  2. Adam I, Mendoza E, Kobalz U, Wohlgemuth S, Scharff C (2017) CNTNAP2 is a direct FoxP2 target in vitro and in vivo in zebra finches: complex regulation by age and activity. Genes Brain Behav 16(6):635–642. Scholar
  3. Adkins-Regan E, Abdelnabi M, Mobarak M, Ottinger MA (1990) Sex steroid levels in developing and adult male and female zebra finches (Poephila guttata). Gen Comp Endo 78(1):93–109. Scholar
  4. Adkins-Regan E, Mansukhani V, Seiwert C, Thompson R (1994) Sexual differentiation of brain and behavior in the zebra finch: critical periods for effects of early estrogen treatment. J Neurobiol 25(7):865–877. Scholar
  5. Agate RJ, Grisham W, Wade J, Mann S, Wingfield J, Schanen C, Palotie A, Arnold AP (2003) Neural, not gonadal, origin of brain sex differences in a gynandromorphic finch. Proc Natl Acad Sci U S A 100(8):4873–4878. Scholar
  6. Agate RJ, Scott BB, Haripal B, Lois C, Nottebohm F (2009) Transgenic songbirds offer an opportunity to develop a genetic model for vocal learning. Proc Natl Acad Sci U S A 106(42):17963–17967. Scholar
  7. Ahmadiantehrani S, London SE (2017a) Bidirectional manipulation of mTOR signaling disrupts socially mediated vocal learning in juvenile songbirds. Proc Natl Acad Sci U S A 114(35):9463–9468. Scholar
  8. Ahmadiantehrani S, London SE (2017b) A reliable and flexible gene manipulation strategy in posthatch zebra finch brain. Sci Rep 7:43244. Scholar
  9. Ahmadiantehrani S, Gores EO, London SE (2018) A complex mTOR response in habituation paradigms for a social signal in adult songbirds. Learn Mem 25(6):273–282. Scholar
  10. Alberini CM (2009) Transcription factors in synaptic plasticity and learning and memory A2 - squire, Larry R. In: Encyclopedia of neuroscience. Academic, Oxford, pp 1081–1092. Scholar
  11. Allis CD, Jenuwein T (2016) The molecular hallmarks of epigenetic control. Nat Rev Genet 17(8):487–500. Scholar
  12. Arnold AP (1975) The effects of castration and androgen replacement on song, courtship, and aggression in zebra finches (Poephila guttata). J Exp Zool 191(3):309–326. Scholar
  13. Arnold AP, Chen X (2009) What does the “four core genotypes” mouse model tell us about sex differences in the brain and other tissues? Front Neuroendocrinol 30(1):1–9. Scholar
  14. Arnold AP, Schlinger BA (1993) Sexual differentiation of brain and behavior: the zebra finch is not just a flying rat. Brain Behav Evol 42(4–5):231–241. Scholar
  15. Arnold AP, Xu J, Grisham W, Chen X, Kim YH, Itoh Y (2004) Minireview: sex chromosomes and brain sexual differentiation. Endocrinology 145(3):1057–1062. Scholar
  16. Aronov D, Andalman AS, Fee MS (2008) A specialized forebrain circuit for vocal babbling in the juvenile songbird. Science (New York, NY) 320(5876):630–634. Scholar
  17. Barbu S, Nardy A, Chevrot J-P, Guellaï B, Glas L, Juhel J, Lemasson A (2015) Sex differences in language across early childhood: family socioeconomic status does not impact boys and girls equally. Front Psychol 6:1874–1874. Scholar
  18. Bolhuis JJ, Okanoya K, Scharff C (2010) Twitter evolution: converging mechanisms in birdsong and human speech. Nat Rev Neurosci 11(11):747–759. Scholar
  19. Boyden ES (2011) A history of optogenetics: the development of tools for controlling brain circuits with light. F1000 Biol Rep 3:11. Scholar
  20. Bozon B, Davis S, Laroche S (2002) Regulated transciption of the immediate-early gene Zif268: mechanisms and gene dosage-dependent function in synaptic plasticity and memory formation. Hippocampus 12(5):570–577. Scholar
  21. Braaten RF, Petzoldt M, Colbath A (2006) Song perception during the sensitive period of song learning in zebra finches (Taeniopygia guttata). J Comp Psychol 120(2):79–88. Scholar
  22. Braaten RF, Miner SS, Cybenko AK (2008) Song recognition memory in juvenile zebra finches: effects of varying the number of presentations of heterospecific and conspecific songs. Behav Proc 77(2):177–183. Scholar
  23. Burkett ZD, Day NF, Kimball TH, Aamodt CM, Heston JB, Hilliard AT, Xiao X, White SA (2018) FoxP2 isoforms delineate spatiotemporal transcriptional networks for vocal learning in the zebra finch. eLife 7:e30649. Scholar
  24. Carruth LL, Reisert I, Arnold AP (2002) Sex chromosome genes directly affect brain sexual differentiation. Nat Neurosci 5(10):933–934. Scholar
  25. Cheng HY, Clayton DF (2004) Activation and habituation of extracellular signal-regulated kinase phosphorylation in zebra finch auditory forebrain during song presentation. J Neurosci 24(34):7503–7513. Scholar
  26. Clayton DF (2000) The genomic action potential. Neurobiol Learn Mem 74(3):185–216. Scholar
  27. Clayton DF, Balakrishnan CN, London SE (2009) Integrating genomes, brain and behavior in the study of songbirds. Curr Biol 19(18):R865–R873. Scholar
  28. Cohen NJ, Vallance DD, Barwick M, Im N, Menna R, Horodezky NB, Isaacson L (2000) The Interface between ADHD and Language Impairment: An Examination of Language, Achievement, and Cognitive Processing. J Child Psychol Psychiatry and Allied Disc 41 (3):353–362. doi:undefinedGoogle Scholar
  29. Condro MC, White SA (2014) Distribution of language-related Cntnap2 protein in neural circuits critical for vocal learning. J Comp Neurol 522(1):169–185. Scholar
  30. Dewulf V, Bottjer SW (2005) Neurogenesis within the juvenile zebra finch telencephalic ventricular zone: a map of proliferative activity. J Comp Neurol 481(1):70–83. Scholar
  31. Dong S, Clayton DF (2008) Partial dissociation of molecular and behavioral measures of song habituation in adult zebra finches. Genes Brain Behav 7(7):802–809. Scholar
  32. Dong S, Clayton DF (2009) Habituation in songbirds. Neurobiol Learn Mem 92(2):183–188. Scholar
  33. Doupe AJ, Kuhl PK (1999) Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci 22:567–631. Scholar
  34. Dugas-Ford J, Rowell JJ, Ragsdale CW (2012) Cell-type homologies and the origins of the neocortex. Proc Natl Acad Sci U S A 109(42):16974–16979. Scholar
  35. Eales LA (1985) Song learning in zebra finches - some effects of song model availability on what is learnt and when. An Behav 33 (Nov):1293–1300. doi:Doi
  36. Eales LA (1987) Song learning in female-raised zebra finches - Another look at the sensitive phase. An Behav 35:1356–1365. doi:Doi
  37. Enard W, Przeworski M, Fisher SE, Lai CSL, Wiebe V, Kitano T, Monaco AP, Pääbo S (2002) Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418:869–872. Scholar
  38. Etchell A, Adhikari A, Weinberg LS, Choo AL, Garnett EO, Chow HM, Chang SE (2018) A systematic literature review of sex differences in childhood language and brain development. Neuropsychologia 114:19–31. Scholar
  39. Fisher SE, Scharff C (2009) FOXP2 as a molecular window into speech and language. Trends Genetics 25(4):166–177. Scholar
  40. Fisher SE, Vargha-Khadem F, Watkins KE, Monaco AP, Pembrey ME (1998) Localisation of a gene implicated in a severe speech and language disorder. Nat Genet 18(2):168–170. Scholar
  41. Fu Y, Dominissini D, Rechavi G, He C (2014a) Gene expression regulation mediated through reversible m6A RNA methylation. Nat Rev Genetics 15:293–306. Scholar
  42. Fu L, Shi Z, Luo G, Tu W, Wang X, Fang Z, Li X (2014b) Multiple microRNAs regulate human FOXP2 gene expression by targeting sequences in its 3′ untranslated region. Mol Brain 7:71. Scholar
  43. Gahr M, Metzdorf R (1999) The sexually dimorphic expression of androgen receptors in the song nucleus Hyperstriatalis Ventrale pars Caudale of the zebra finch develops independently of gonadal steroids. J Neurosci 19(7):2628–2636. Scholar
  44. Gebert LFR, MacRae IJ (2018) Regulation of microRNA function in animals. Nat Rev Mol Cell Biol 20:21–37. Scholar
  45. Gervain J, Vines BW, Chen LM, Seo RJ, Hensch TK, Werker JF, Young AH (2013) Valproate reopens critical-period learning of absolute pitch. Front Syst Neurosci 7:102. Scholar
  46. Gilad Y, Oshlack A, Smyth GP, Speed TP, White K (2006) Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature 440:242–245. Scholar
  47. 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
  48. Gunaratne PH, Lin YC, Benham AL, Drnevich J, et al. (2011) Song exposure regulates known and novel microRNAs in the zebra finch auditory forebrain. BMC genomics 12,
  49. Haesler S, Wada K, Nshdejan A, Morrisey EE, Lints T, Jarvis ED, Scharff C (2004) FoxP2 expression in avian vocal learners and non-learners. J Neurosci 24(13):3164–3175. Scholar
  50. Haesler S, Rochefort C, Georgi B, Licznerski P, Osten P, Scharff C (2007) Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus area X. PLoS Biol 5(12):e321. Scholar
  51. Halladay AK, Bishop S, Constantino JN, Daniels AM, Koenig K, Palmer K, Messinger D, Pelphrey K, Sanders SJ, Singer AT, Taylor JL, Szatmari P (2015) Sex and gender differences in autism spectrum disorder: summarizing evidence gaps and identifying emerging areas of priority. Mol Autism 6(1):36. Scholar
  52. Hammock EA, Young LJ (2005) Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308:1630–1634. Scholar
  53. Heston JB, White SA (2015) Behavior-linked foxP2 regulation enables zebra finch vocal learning. J Neurosci 35(7):2885–2894. Scholar
  54. Heston JB, Jt S, Day NF, Coleman MJ, White SA (2018) Bidirectional scaling of vocal variability by an avian cortico-basal ganglia circuit. Physiol Rep 6(8):e13638–e13638. Scholar
  55. Hisey E, Kearney MG, Mooney R (2018) A common neural circuit mechanism for internally guided and externally reinforced forms of motor learning. Nat Neurosci 21(4):589–597Google Scholar
  56. Hoeffer CA, Klann E (2010) mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci 33(2):67–75. Scholar
  57. Hollins SL, Cairns MJ (2016) MicroRNA: small RNA mediators of the brains genomic response to environmental stress. Prog Neurobiol 143:61–81. Scholar
  58. Horita H, Wada K, Rivas MV, Hara E, Jarvis ED (2010) The dusp1 immediate early gene is regulated by natural stimuli predominantly insensory input neurons. J Comp Neurol 518(14):2873–2901. Scholar
  59. Itoh Y, Melamed E, Yang X, Kampf K, Wang S, Yehya N, Van Nas A, Replogle K, Band MR, Clayton DF, Schadt EE, Lusis AJ, Arnold AP (2007) Dosage compensation is less effective in birds than in mammals. J Biol 6(1):2. Scholar
  60. Jarvis ED, Nottebohm F (1997) Motor-driven gene expression. Proc Natl Acad Sci U S 94(8):4097–4102. Scholar
  61. Jarvis ED, Scharff C, Grossman MR, Ramos JA, Nottebohm F (1998) For whom the bird sings: context-dependent gene expression. Neuron 21(4):775–788. Scholar
  62. Jin H, Clayton DF (1997) Localized changes in immediate-early gene regulation during sensory and motor learning in zebra finches. Neuron 19(5):1049–1059. Scholar
  63. Karten HJ (2013) Neocortical evolution: neuronal circuits arise independently of lamination. Curr Biol 23(1):R12–R15. Scholar
  64. Kelly TK, Ahmadiantehrani S, Blattler A, London SE (2018) Epigenetic regulation of transcriptional plasticity associated with developmental song learning. Proc Royal Soc B: Biol Sci 285(1878):20180160. Scholar
  65. Kim D, Sung YM, Park J, Kim S, Kim J, Park J, Ha H, Bae JY, Kim S, Baek D (2016) General rules for functional microRNA targeting. Nat Genetics 48:1517–1526. Scholar
  66. Kim YH, Perlman WR, Arnold AP (2004) Expression of androgen receptor mRNA in zebra finch song system: developmental regulation by estrogen. J Comp Neurol 469(4):535–547. Scholar
  67. Kimpo RR, Doupe AJ (1997) FOS is induced by singing in distinct neuronal populations in a motor network. Neuron 18(2):315–325. Scholar
  68. Knudsen EI (2004) Sensitive periods in the development of the brain and behavior. J Cog Neurosci 16(8):1412–1425. Scholar
  69. Kreitzer AC (2009) Physiology and pharmacology of striatal neurons. Ann Rev Neurosci 32(1):127–147. Scholar
  70. Kruse AA, Stripling R, Clayton DF (2004) Context-specific habituation of the zenk gene response to song in adult zebra finches. Neurobiol Learn Mem 82(2):99–108. Scholar
  71. Kvande MN, Belsky J, Wichstrøm L (2018) Selection for special education services: the role of gender and socio-economic status. European J Sp Needs Edu 33(4):510–524. Scholar
  72. Lai CS, Fisher SE, Hurst JA, Vargha-Khadem F, Monaco AP (2001) A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413(6855):519–523. Scholar
  73. Lin D, Hong P, Zhang S, Xu W, Jamal M, Yan K, Lei Y, Li L, Ruan Y, Fu ZF, Li G, Cao G (2018) Digestion-ligation-only hi-C is an efficient and cost-effective method for chromosome conformation capture. Nat Genetics 50(5):754–763. Scholar
  74. Lin LC, Vanier DR, London SE (2014) Social information embedded in vocalizations induces neurogenomic and behavioral responses. PLoS One 9(11):e112905. Scholar
  75. Liu W, Kohn J, Szwed SK, Pariser E, Sepe S, Haripal B, Oshimori N, Marsala M, Miyanohara A, Lee R (2015) Human mutant huntingtin disrupts vocal learning in transgenic songbirds. Nat Neurosci 18(11):1617–1622.
  76. London SE (2016) Influences of non-canonical neurosteroid signaling on developing neural circuits. Curr Opin Neurobiol 40:103–110. Scholar
  77. London SE (2017) Developmental song learning as a model to understand neural mechanisms that limit and promote the ability to learn. Behav Process 163:13–23. Scholar
  78. London SE, Clayton DF (2008) Functional identification of sensory mechanisms required for developmental song learning. Nat Neurosci 11(5):579–586. Scholar
  79. London SE, Schlinger BA (2007) Steroidogenic enzymes along the ventricular proliferative zone in the developing songbird brain. J Comp Neurol 502(4):507–521. Scholar
  80. London SE, Monks DA, Wade J, Schlinger BA (2006) Widespread capacity for steroid synthesis in the avian brain and song system. Endocrinology 147(12):5975–5987. Scholar
  81. London SE, Dong S, Replogle K, Clayton DF (2009a) Developmental shifts in gene expression in the auditory forebrain during the sensitive period for song learning. Dev Neurobiol 69(7):437–450. Scholar
  82. London SE, Remage-Healey L, Schlinger BA (2009b) Neurosteroid production in the songbird brain: a re-evaluation of core principles. Front Neuroendocrinol 30(3):302–314. Scholar
  83. Luo GZ, Hafner M, Shi Z, Brown M, Feng GH, Tuschl T, Wang XJ, Li X (2012) Genome-wide annotation and analysis of zebra finch microRNA repertoire reveal sex-biased expression. BMC Genomics 13(1):727. Scholar
  84. MacDermot KD, Bonora E, Sykes N, Coupe AM, Lai CS, Vernes SC, Vargha-Khadem F, McKenzie F, Smith RL, Monaco AP, Fisher SE (2005) Identification of FOXP2 truncation as a novel cause of developmental speech and language deficits. Am J Hum Genet 76(6):1074–1080. Scholar
  85. Marty V, Cavaillé J (2019) Imprinted small noncoding RNA genes in brain function and behaviour. Curr Opin Behav Sci 25:8–14. Scholar
  86. McQuown SC, Wood MA (2011) HDAC3 and the molecular brake pad hypothesis. Neurobiol Learn Mem 96(1):27–34. Scholar
  87. McQuown SC, Barrett RM, Matheos DP, Post RJ, Rogge GA, Alenghat T, Mullican SE, Jones S, Rusche JR, Lazar MA, Wood MA (2011) HDAC3 is a critical negative regulator of long-term memory formation. J Neurosci 31(2):764–774. Scholar
  88. Mello CV, Velho TAF, Pinaud R (2004) Song-induced gene expression: a window on wong auditory processing and perception. Ann N Y Acad Sci 1016(1):263–281. Scholar
  89. Minatohara K, Akiyoshi M, Okuno H (2016) Role of immediate-early genes in synaptic plasticity and neuronal ensembles underlying the memory trace. Front Mol Neurosci 8:78–78. Scholar
  90. Mooney R, Konishi M (1991) Two distinct inputs to an avian song nucleus activate different glutamate receptor subtypes on individual neurons. Proc Natl Acad Sci U S A 88(10):4075–4079CrossRefGoogle Scholar
  91. Mori C, Wada K (2015) Audition-independent vocal crystallization associated with intrinsic developmental gene expression dynamics. J Neurosci 35(3):878–889. Scholar
  92. Murugan M, Harward S, Scharff C, Mooney R (2013) Diminished FoxP2 levels affect dopaminergic modulation of corticostriatal signaling important to song variability. Neuron 80(6):1464–1476. Scholar
  93. Nguyen TC, Zaleta-Rivera K, Huang X, Dai X, Zhong S (2018) RNA, action through interactions. Trends Genetics 34(11):867–882. Scholar
  94. Nottebohm F, Arnold AP (1976) Sexual dimorphism in vocal control areas of the songbird brain. Science 194(4261):211–213.
  95. Nudel R, Newbury DF (2013) FOXP2. Wiley Interdiscip Rev Cogn Sci 4(5):547–560. Scholar
  96. O’Brien J, Hayder H, Zayed Y, Peng C (2018) Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol 9:402–402. Scholar
  97. O’Leary MA, Bloch JI, Flynn JJ, Gaudin TJ, Giallombardo A, Giannini NP, Goldberg SL, Kraatz BP, Luo Z-X, Meng J, Ni X, Novacek MJ, Perini FA, Randall ZS, Rougier GW, Sargis EJ, Silcox MT, Simmons NB, Spaulding M, Velazco PM, Weksler M, Wible JR, Cirranello AL (2013) The placental mammal ancestor and the post–K-Pg radiation of placentals. Science 339(6120):662–667. Scholar
  98. Panaitof SC, Abrahams BS, Dong H, Geschwind DH, White SA (2010) Language-related Cntnap2 gene is differentially expressed in sexually dimorphic song nuclei essential for vocal learning in songbirds. J Comp Neurol 518(11):1995–2018. Scholar
  99. Person AL, Gale SD, Farries MA, Perkel DJ (2008) Organization of the songbird basal ganglia, including area X. J Comp Neurol 508(5):840–866. Scholar
  100. Petkov CI, Jarvis ED (2012) Birds, primates, and spoken language origins: behavioral phenotypes and neurobiological substrates. Front Evol Neurosci 4:12. Scholar
  101. Pfenning AR, Hara E, Whitney O, Rivas MV, Wang R, Roulhac PL, Howard JT, Wirthlin M, Lovell PV, Ganapathy G, Mountcastle J, Moseley MA, Thompson JW, Soderblom EJ, Iriki A, Kato M, Gilbert MTP, Zhang G, Bakken T, Bongaarts A, Bernard A, Lein E, Mello CV, Hartemink AJ, Jarvis ED (2014) Convergent transcriptional specializations in the brains of humans and song-learning birds. Science 346(6215):1256846–1256846.
  102. Phan ML, Gergues MM, Mahidadia S, Jimenez-Castillo J, Vicario DS, Bieszczad KM (2017) HDAC3 inhibitor RGFP966 modulates neuronal memory for vocal communication signals in a songbird model. Front Sys Neurosci 11:65–65. Scholar
  103. Prum RO, Berv JS, Dornburg A, Field DJ, Townsend JP, Lemmon EM, Lemmon AR (2016) A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 534:S7–S8. Scholar
  104. Rankin CH, Abrams T, Barry RJ, Bhatnagar S, Clayton DF, Colombo J, Coppola G, Geyer MA, Glanzman DL, Marsland S, McSweeney FK, Wilson DA, Wu CF, Thompson RF (2009) Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol Learn Mem 92(2):135–138. Scholar
  105. Replogle K, Arnold AP, Ball GF, Band M, Bensch S, Brenowitz EA, Dong S, Drnevich J, Ferris M, George JM, Gong G, Hasselquist D, Hernandez AG, Kim R, Lewin HA, Liu L, Lovell PV, Mello CV, Naurin S, Rodriguez-Zas S, Thimmapuram J, Wade J, Clayton DF (2008) The songbird Neurogenomics (SoNG) initiative: community-based tools and strategies for study of brain gene function and evolution. BMC Genomics 9:131. Scholar
  106. Roberts TF, Gobes SMH, Murugan M, Ölveczky BP, Mooney R (2012) Motor circuits are required to encode a sensory model for imitative learning. Nat Neurosci 15(10):1454–1459. Scholar
  107. Roper A, Zann R (2006) The onset of song learning and song tutor selection in fledgling zebra finches. Ethology 112(5):458–470. Scholar
  108. Roth BL (2016) DREADDs for neuroscientists. Neuron 89(4):683–694. Scholar
  109. Sander JD, Joung JK (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotech 32:347–355. Scholar
  110. Scharff C, Adam I (2013) Neurogenetics of birdsong. Curr Opin Neurobiol 23(1):29–36. Scholar
  111. Scharff C, Haesler S (2005) An evolutionary perspective on FoxP2: strictly for the birds? Curr Opin Neurobiol 15(6):694–703. Scholar
  112. Schlinger BA, Arnold AP (1992) Circulating estrogens in a male songbird originate in the brain. Proc Natl Acad Sci U S A 89(16):7650–7653. Scholar
  113. Shi Z, Luo G, Fu L, Fang Z, Wang X, Li X (2013) miR-9 and miR-140-5p target FoxP2 and are regulated as a function of the social context of singing behavior in zebra finches. J Neurosci 33(42):16510–16521. Scholar
  114. Shukla GC, Singh J, Barik S (2011) MicroRNAs: processing, maturation. target recognition and regulatory functions Mol Cell Pharmacol 3(3):83–92PubMedGoogle Scholar
  115. Smith KS, Bucci DJ, Luikart BW, Mahler SV (2016) DREADDS: use and application in behavioral neuroscience. Behav Neurosci 130(2):137–155. Scholar
  116. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403(6765):41–45CrossRefGoogle Scholar
  117. Takesian AE, Hensch TK (2013) Balancing plasticity/stability across brain development. Prog Brain Res 207:3–34. Scholar
  118. Tanaka M, Sun F, Li Y, Mooney R (2018) A mesocortical dopamine circuit enables the cultural transmission of vocal behaviour. Nature 563(7729):117–120. Scholar
  119. Teramitsu I, Kudo LC, London SE, Geschwind DH, White SA (2004) Parallel FoxP1 and FoxP2 expression in songbird and human brain predicts functional interaction. J Neurosci 24(13):3152–3163. Scholar
  120. The ENCODE Project Consortium (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489:57–74. Scholar
  121. Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psych Rev 73(1):16–43. Scholar
  122. Tischmeyer W, Grimm R (1999) Activation of immediate early genes and memory formation. Cell Mol Life Sci CMLS 55(4):564–574. Scholar
  123. Urban DJ, Roth BL (2015) DREADDs (designer receptors exclusively activated by designer drugs): Chemogenetic tools with therapeutic utility. Ann Rev Pharm Toxicol 55(1):399–417. Scholar
  124. Van Hedger SC, Heald SLM, Koch R, Nusbaum HC (2015) Auditory working memory predicts individual differences in absolute pitch learning. Cognition 140:95–110. Scholar
  125. Vargha-Khadem F, Watkins KE, Price CJ, Ashburner J et al (1998) Neural basis of an inherited speech and language disorder. Proc Natl Acad Sci U S A 95(21):12695–12700. Scholar
  126. Vates GE, Broome BM, Mello CV, Nottebohm F (1996) Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches. J Comp Neurol 366(4):613–642. <613::AID-CNE5>3.0.CO;2-7CrossRefPubMedGoogle Scholar
  127. Venter JC, Adams MD, Myers EW, Li PW et al (2001) The sequence of the human genome. Science 291(5507):1304–1351. Scholar
  128. Vignal C, Andru J, Mathevon N (2005) Social context modulates behavioural and brain immediate early gene responses to sound in male songbird. Eur J Neurosci 22(4):949–955. Scholar
  129. Wade J, Arnold AP (2004) Sexual differentiation of the zebra finch song system. Ann N Y Acad Sci 1016:540–559. Scholar
  130. Walder DJ, Seidman LJ, Cullen N, Su J, Tsuang MT, Goldstein JM (2006) Sex differences in language dysfunction in schizophrenia. AmJ psychiatry 163(3):470–477. Scholar
  131. Wallentin M (2009) Putative sex differences in verbal abilities and language cortex: a critical review. Brain Lang 108:175–183. Scholar
  132. Wang W, Kwon EJ, Tsai L-H (2012) MicroRNAs in learning, memory, and neurological diseases. Learn Mem 19(9):359–368. Scholar
  133. Warren WC, Clayton DF, Ellegren H, Arnold AP et al (2010) The genome of a songbird. Nature 464(7289):757–762. Scholar
  134. Werker JF, Hensch TK (2015) Critical periods in speech perception: new directions. Annu Rev Psychol 66:173–196. Scholar
  135. Whitney O, Soderstrom K, Johnson F (2000) Post-transcriptional regulation of zenk expression associated with zebra finch vocal development. Brain Res Mol Brain Res 80(2):279–290. Scholar
  136. Whitney O, Pfenning AR, Howard JT, Blatti CA et al (2014) Core and region-enriched networks of behaviorally regulated genes and the singing genome. Science 346(6215):1256780. Scholar
  137. Woolley SC, Doupe AJ (2008) Social context–induced song variation affects female behavior and gene expression. PLoS Biol 6(3):e62. Scholar
  138. Xiao L, Chattree G, Oscos FG, Cao M, Wanat MJ, Roberts TF (2018) A Basal Ganglia circuit sufficient to guide birdsong learning. Neuron 98(1):208–221. e205. Scholar
  139. Zann RA (1996) The Zebra finch: a synthesis of Field and laboratory studies. Oxford University Press, New YorkGoogle Scholar
  140. Zhao BS, Roundtree IA, He C (2016) Post-transcriptional gene regulation by mRNA modifications. Nat Rev Mol Cell Biol18:31. doi:

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Authors and Affiliations

  1. 1.Department of Psychology, Institute for Mind and Biology, Grossman Institute for Neuroscience, Quantitative Biology and Human BehaviorUniversity of ChicagoChicagoUSA

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