Neurogenesis in the adult avian song-control system

Cold Spring Harbor Perspectives in Biology

Volumn 7, Issue 6, 2015, Pages 1-24

  Brenowitz, Eliot A ^a   Larson, Tracy A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AVES;

ANIMAL; BIRD; BRAIN; CELL DEATH; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; SOCIAL BEHAVIOR; VOCALIZATION;

ANIMALS; BIRDS; BRAIN; CELL DEATH; NEUROGENESIS; NEURONAL PLASTICITY; SOCIAL BEHAVIOR; VOCALIZATION, ANIMAL;

EID: 84930456600     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a019000     Document Type: Article

References (164)

1. Abrous DN, Wojtowicz JM. 2008. Neurogenesis and hippo-campal memory system. In Adult neurogenesis (ed. Gage FH, Kempermann G, Song HJ), pp. 445–461. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Adar E, Nottebohm F, Barnea A. 2008a. The relationship between nature of social change, age, and position of new neurons and their survival in adult zebrafinch brain. J Neurosci 28: 5394–5400.
3. Adar E, Lotem A, Barnea A. 2008b. The effect of social environment on singing behavior in the zebra finch (Tae-niopygia guttata) and its implication for neuronal recruitment. Behav Brain Res 187: 178–184.
4. Altman J, Das GD. 1965. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124: 319–335.
5. Alvarez-Borda B, Nottebohm F. 2002. Gonads and singing play separate, additive roles in new neuron recruitment in adult canary brain. J Neurosci 22: 8684–8690.
6. Alvarez-Borda B, Haripal B, Nottebohm F. 2004. Timing of brain-derived neurotrophic factor exposure affects life expectancy of new neurons. Proc Natl Acad Sci 101: 3957–3961.
7. Alvarez-Buylla A, Kirn JR. 1997. Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J Neurobiol 33: 585–601.
8. Alvarez-Buylla A, Nottebohm F. 1988. Migration of young neurons in adult avian brain. Nature 335: 353–354.
9. Alvarez-Buylla A, Kirn JR, Nottebohm F. 1990. Birth of projection neurons in adult avian brain may be related to perceptual or motor learning [published erratum appears in Science 250: 360, 1990]. Science 249: 1444–1446.
10. Alvarez-Buylla A, Ling CY, Yu WS. 1994. Contribution of neurons born during embryonic, juvenile, and adult life to the brain of adult canaries: Regional specificity and delayed birth of neurons in the song-control nuclei. J Comp Neurol 347: 233–248.
11. Alvarez-Buylla A, Seri B, Doetsch F. 2002. Identification of neural stem cells in the adult vertebrate brain. Brain Res Bull 57: 751–758.
12. Ames A III. 2000. CNS energy metabolism as related to function. Brain Res Brain Res Rev 34: 42–68.
13. Barami K, Kirschenbaum B, Lemmon V, Goldman SA.1994. N-cadherin and Ng-CAM/8D9 are involved serially in the migration of newly generated neurons into the adult songbird brain. Neuron 13: 567–582.
14. Barami K, Iversen K, Furneaux H, Goldman SA. 1995. Hu protein as an early marker of neuronal phenotypic differentiation by subependymal zone cells of the adult songbird forebrain. J Neurobiol 28: 82–101.
15. Barnea A, Nottebohm F. 1994. Seasonal recruitment of hip-pocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci 91: 11217–11221.
16. Barnea A, Pravosudov V. 2011. Birds as a model to study adult neurogenesis: Bridging evolutionary, comparative and neuroethological approaches. Eur J Neurosci 34: 884–907.
17. Barnea A, Mishal A, Nottebohm F. 2006. Social and spatial changes induce multiple survival regimes for new neurons in two regions of the adult brain: An anatomical representation of time? Behav Brain Res 167: 63–74.
18. Beecher MD, Brenowitz EA. 2005. Functional aspects of song learning in the songbirds. Trends Ecol Evol 20: 143–149.
19. Bingman VP, Able KP. 2002. Maps in birds: Representational mechanisms and neural bases. Curr Opin Neurobiol 12: 745–750.
20. Bingman VP, Hough GE II, Kahn MC, Siegel JJ. 2003. The homing pigeon hippocampus and space: In search of adaptive specialization. Brain Behav Evol 62: 117–127.
21. Bingman VP, Gagliardo AA, Hough GEII, Ioale P, Kahn MC, Siegel JJ. 2005. The avian hippocampus, homing in pigeons and the memory representation of large-scale space. Integrat Comp Biol 45: 555–564.
22. Boddy AM, McGowen MR, Sherwood CC, Grossman LI, Goodman M, Wildman DE. 2012. Comparative analysis of encephalization in mammals reveals relaxed constraints on anthropoid primate and cetacean brain scaling. J Evol Biol 25: 981–994.
23. Brainard MS. 2008. The anterior forebrain pathway and vocal plasticity. In Neuroscience of birdsong (ed. Zeigler HP, Marler P), pp. 240–255. Cambridge University Press, Cambridge.
24. Brenowitz EA. 1991. Altered perception of species-specific song by female birds after lesions of a forebrain nucleus. Science 251: 303–305.
25. Brenowitz EA. 1997. Comparative approaches to the avian song system. J Neurobiol 33: 517–531.
26. Brenowitz EA. 2008. Plasticity of the song control system in adult birds. In Neuroscience of birdsong (ed. Zeigler HP, Marler P), pp. 332–349. Cambridge University Press, Cambridge.
27. Brenowitz EA, Beecher MD. 2005. Song learning in birds: Diversity and plasticity, opportunities and challenges. Trends Neurosci 28: 127–132.
28. Brenowitz EA, Lent K. 2001. Afferent input is necessary for seasonal growth and maintenance of adult avian song control circuits. J Neurosci 21: 2320–2329.
29. Brenowitz EA, Lent K. 2002. Act locally and think globally: Intracerebral testosterone implants induce seasonal-like growth of adult avian song control circuits. Proc Natl Acad Sci 99: 12421–12426.
30. Brown ES, Rush AJ, McEwen BS. 1999. Hippocampal remodeling and damage by corticosteroids: Implications for mood disorders. Neuropsychopharmacology 21: 474–484.
31. Burd GD, Nottebohm F. 1985. Ultrastructural characterization of synaptic terminals formed on newly generated neurons in a song control nucleus of the adult canary forebrain. J Comp Neurol 240: 143–152.
32. Calder WA, King JR. 1974. Thermal and caloric relations in birds. In Avian biology (ed. Farner DS, King JR, Parkes KC), pp. 259–413. Academic, New York.
33. Cameron HA, Gould E. 1994. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neurosci-ence 61: 203–209.
34. Cameron HA, McKay RD. 2001. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435: 406–417.
35. Chen Z, Ye R, Goldman SA. 2013. Testosterone modulation of angiogenesis and neurogenesis in the adult songbird brain. Neuroscience 239: 139–148.
36. Cheng MF, Alexander K, Zhou S, Bonder E, Chuang LS. 2011. Newborn GnRH neurons in the adult forebrain of the ring dove. Horm Behav 60: 94–104.
37. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Frag-niere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, et al. 2009. A functional role for adult hippo-campal neurogenesis in spatial pattern separation. Science 325: 210–213.
38. Corotto FS, Henegar JR, Maruniak JA. 1994. Odor deprivation leadsto reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neuro-science 61: 739–744.
39. De Marchis S, Bovetti S, Carletti B, Hsieh YC, Garzotto D, Peretto P, Fasolo A, Puche AC, Rossi F. 2007. Generation of distinct types of periglomerular olfactory bulb inter-neurons during development and in adult mice: Implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci 27: 657–664.
40. Ding L, Perkel DJ, Farries MA. 2003. Presynaptic depression of glutamatergic synaptic transmission by D1-like dop-amine receptor activation in the avian basal ganglia. J Neurosci 23: 6086–6095.
41. Dittrich F, Feng Y, Metzdorf R, Gahr M. 1999. Estrogen-inducible, sex-specific expression of brain-derived neu-rotrophic factor mRNA in a forebrain song control nucleus of the juvenile zebra finch. Proc Natl Acad Sci 96: 8241–8246.
42. Dutar P, Petrozzino JJ, Vu HM, Schmidt MF, Perkel DJ. 2000. Slow synaptic inhibition mediated by metabotropic glu-tamate receptor activation of GIRK channels. J Neuro-physiol 84: 2284–90.
43. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med 4: 1313–1317.
44. Fee MS, Kozhevnikov AA, Hahnloser RH. 2004. Neural mechanisms of vocal sequence generation in the songbird. Ann NYAcad Sci 1016: 153–170.
45. Fraley GS, Steiner RA, Lent K, Brenowitz EA. 2010. Seasonal changes in androgen receptor mRNA in the brain of the white-crowned sparrow. Gen Comp Endocrinol 166: 66–71.
46. Fusani L, Van’t Hoft, Hutchison JB, Gahr M.2000. Seasonal expression of androgen receptors, estrogen receptors, and aromatase in the canary brain in relation to circulating androgens and estrogens. J Neurobiol 43: 254–268.
47. Gage FH, Song H, Kempermann G. 2008. Adult neurogen-esis: A prologue. In Adult neurogenesis (ed. Gage FH, Song H, Kempermann G), pp. 1–5. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Gahr M, Garcia-Segura LM. 1996. Testosterone-dependent increase of gap-junctions in HVC neurons of adult female canaries. Brain Res 712: 69–73.
49. Gahr M, Leitner S, Fusani L, Rybak F. 2002. What is the adaptive role of neurogenesis in adult birds? Prog Brain Res 138: 233–254.
50. Gaunt AS, Hikida RS, Jehl JR, Fenbert L. 1990. Rapid atrophy and hypertrophy of an avian flight muscle. Auk 107: 649–659.
51. Gentner TQ, Hulse SH, Bentley GE, Ball GF. 2000. Individual vocal recognition and the effect of partial lesions to HVc on discrimination, learning, and categorization of conspecific song in adult songbirds. J Neurobiol 42: 117–133.
52. Gheusi G, Ortega-Perez I, Murray K, Lledo PM. 2009. A niche for adult neurogenesis in social behavior. Behav Brain Res 200: 315–322.
53. Goldman SA. 1990. Neuronal development and migration in explant cultures of the adult canary forebrain. J Neuro-sci 10: 2931–2939.
54. Goldman SA, Nottebohm F. 1983. Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci 80: 2390–2394.
55. Goldman SA, Lemmon V, Chin SS. 1993. Migrationof newly generated neurons upon ependymally derived radial guide cells in explant cultures of the adult songbird fore-brain. Glia 8: 150–160.
56. Goldman SA, Zukhar A, Barami K, Mikawa T, Niedzwiecki D. 1996. Ependymal/subependymal zone cells of postnatal and adult songbird brain generate both neurons and nonneuronal siblings in vitro and in vivo. J Neurobiol 30: 505–520.
57. Gottschalk WA, Jiang H, Tartaglia N, Feng L, Figurov A, Lu B. 1999. Signaling mechanisms mediating BDNF modulation of synaptic plasticity in the hippocampus. Learn Mem 6: 243–256.
58. Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E. 1997. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17: 2492–2498.
59. Gould E, Reeves AJ, Fallah M, Tanapat P, Gross CG, Fuchs E. 1999a. Hippocampal neurogenesis in adult Old World primates. Proc Natl Acad Sci 96: 5263–5267.
60. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999b. Learning enhances adult neurogenesis in the hippocam-pal formation. Nat Neurosci 2: 260–265.
61. Gray GE, Sanes JR. 1992. Lineage ofradial glia inthe chicken optic tectum. Development 114: 271–283.
62. Gross CG. 2000. Neurogenesis in the adult brain: Death of a dogma. Nat Rev Neurosci 1: 67–73.
63. Hahn TP, Ball GF. 1995. Changes in brain GnRH associated with photorefractoriness in house sparrows (Passer do-mesticus). Gen Comp Endocrinol 99: 349–363.
64. Hartog TE, Dittrich F, Pieneman AW, Jansen RF, Frankl-Vilches C, Lessmann V, Lilliehook C, Goldman SA, Gahr M. 2009. Brain-derived neurotrophic factor signaling in the HVC is required for testosterone-induced song of female canaries. J Neurosci 29: 15511–15519.
65. Hidalgo A, Barami K, Iversen K, Goldman SA. 1995. Estrogens and non-estrogenic ovarian influences combine to promote the recruitment and decrease the turnover of new neurons in the adult female canary brain. J Neurobiol 27: 470–487.
66. Hoshooley JS, Phillmore LS, Sherry DF, Macdougall-Shack-leton SA. 2007. Annual cycle of the black-capped chickadee: Seasonality of food storing and the hippocampus. Brain Behav Evol 69: 161–168.
67. Jabés A, Lavenex PB, Amaral DG, Lavenex P. 2010. Quantitative analysis of postnatal neurogenesis and neuron number in the macaque monkey dentate gyrus. Eur J Neurosci 31: 273–285.
68. Jarvis ED. 2009. Evolution of the pallium in birds and reptiles. In New encyclopedia of neuroscience (ed. Binder MD, Hirokawa N, Windhorst U), pp. 1390–1400. Springer-Verlag, Berlin.
69. Jezierski MK, Sohrabji F. 2003. Estrogen enhances retrograde transport of brain-derived neurotrophic factor in the rodent forebrain. Endocrinology 144: 5022–5029.
70. Jiang J, McMurtry J, Niedzwiecki D, Goldman SA. 1998. Insulin-like growth factor-1 is a radial cell-associated neurotrophin that promotes neuronal recruitment from the adult songbird edpendyma/subependyma. J Neuro-biol 36: 1–15.
71. Kaplan MS, Hinds JW. 1977. Neurogenesis in the adult rat: Electron microscopic analysis of light radioautographs. Science 197: 1092–1094.
72. Katz A, Mirzatoni A, Zhen Y, Schlinger BA. 2008. Sex differences in cell proliferation and glucocorticoid responsiveness in the zebra finch brain. Eur J Neurosci 28: 99–106.
73. Kay L, Humphreys L, Eickholt BJ, Burrone J. 2011. Neuronal activity drives matching of pre- and postsynaptic function during synapse maturation. Nat Neurosci 14: 688–690.
74. Kempermann G. 2008. The neurogenic reserve hypothesis: What is adult hippocampal neurogenesis good for? Trends Neurosci 31: 163–169.
75. Kempermann G, Fabel K, Ehninger D, Babu H, Leal-Galicia P, Garthe A, Wolf S. 2010. Why and how physical activity promotes experience-induced brain plasticity. Front Neurosci 4: 189.
76. Kim SH, Lu HF, Alano CC. 2011. Neuronal Sirt3 protects against excitotoxic injury in mouse cortical neuron culture. PLoS ONE 6: e14731.
77. Kirn JR, Alvarez-Buylla A, Nottebohm F. 1991. Production and survival of projection neurons in a forebrain vocal center of adult male canaries. J Neurosci 11: 1756–1762.
78. Kirn J, O’Loughlin B, Kasparian S, Nottebohm F. 1994. Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song. Proc Natl Acad Sci 91: 7844–7848.
79. Kirn JR, Fishman Y, Sasportas K, Alvarez-Buylla A, Notte-bohm F. 1999. Fate of new neurons in adult canary high vocal center during the first 30 days after their formation. J Comp Neurol 411: 487–494.
80. Konkel A, Cohen NJ. 2009. Relational memory and the hippocampus: Representations and methods. Front Neurosci 3: 166–174.
81. LaDage LD, Roth TC II, Fox RA, Pravosudov VV. 2010. Ecologically relevant spatial memory use modulates hip-pocampal neurogenesis. Proc Biol Sci 277: 1071–1079.
82. LaDage LD, Roth TC, Pravosudov VV. 2011. Hippocampal neurogenesis is associated with migratory behaviour in adult but not juvenile sparrows (Zonotrichia leucophrys ssp.). Proc R Soc B Biol Sci 278: 138–143.
83. Larson TA, Wang TW, Gale SD, Miller KE, Thatra NM, Caras ML, Perkel DJ, Brenowitz EA. 2013. Postsynaptic neural activity regulates neuronal addition in the adult avian song control system. Proc Natl Acad Sci 110: 16640–16644.
84. Larson TA, Thatra NM, Lee BH, Brenowitz EA. 2014. Reactive neurogenesis in response to naturally occurring ap-optosis in an adult brain. J Neurosci 34: 13066–13076.
85. Leonardo A, Konishi M. 1999. Decrystallization of adult birdsong by perturbation of auditory feedback. Nature 399: 466–470.
86. Li XC, Jarvis ED, Alvarez-Borda B, Lim DA, Nottebohm F. 2000. A relationship between behavior, neurotrophin expression, and new neuron survival. Proc Natl Acad Sci 97: 8584–8589.
87. Lim DA, Fishell GJ, Alvarez-Buylla A.1997. Postnatal mouse subventricular zone neuronal precursors can migrate and differentiate within multiple levelsof the developing neu-raxis. Proc Natl Acad Sci 94: 14832–14836.
88. Lipkind D, Nottebohm F, Rado R, Barnea A. 2002. Social change affects the survival of new neurons in the fore-brain of adult songbirds. Behav Brain Res 133: 31–43.
89. Lledo PM, Alonso M, Grubb MS. 2006. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7: 179–193.
90. Lombardino AJ, Nottebohm F. 2000. Ageatdeafening affects the stability of learned song in adult male zebra finches. J Neurosci 20: 5054–5064.
91. Louissaint A Jr, Rao S, Leventhal C, Goldman SA. 2002. Coordinated interaction of neurogenesis and angiogene-sis in the adult songbird brain. Neuron 34: 945–960.
92. Malberg JE, Eisch AJ, Nestler EJ, Duman RS. 2000. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20: 9104–9110.
93. Massieu L, Haces ML, Montiel T, Hernández-Fonseca K. 2003. Acetoacetate protects hippocampal neurons against glutamate-mediated neuronal damage during glycolysis inhibition. Neuroscience 120: 365–378.
94. Meitzen J, Moore IT, Lent K, Brenowitz EA, Perkel DJ. 2007a. Steroid hormones act transsynaptically within the fore-brain to regulate neuronal phenotype and song stereo-typy. J Neurosci 27: 12045–12057.
95. Meitzen J, Perkel DJ, Brenowitz EA. 2007b. Seasonal changes in intrinsic electrophysiological activity of song control neurons in wild song sparrows. J Comp Physiol A Neuro-ethol Sens Neural Behav Physiol 193: 677–683.
96. Meitzen J, Weaver AL, Brenowitz EA, Perkel DJ. 2009a. Plastic and stable electrophysiological properties of adult avian forebrain song-control neurons across changing breeding conditions. J Neurosci 29: 6558–6567.
97. Meitzen J, Thompson CK, Choi H, Perkel DJ, Brenowitz EA. 2009b. Time course of changes in Gambel’s white-crowned sparrow song behavior following transitions in breeding condition. Hormones Behav 55: 217–227.
98. Mirescu C, Gould E. 2006. Stress and adult neurogenesis. Hippocampus 16: 233–238.
99. Mooney R, Prather JF. 2005. The HVC microcircuit: The synaptic basis for interactions between song motor and vocal plasticity pathways. J Neurosci 25: 1952–1964.
100. Morris RG. 2006. Elements of a neurobiological theory of hippocampal function: The role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 23: 2829–2846.
101. Nordeen KW, Nordeen EJ. 1988. Projection neurons within a vocal motor pathway are born during song learning in zebra finches. Nature 334: 149–151.
102. 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.
103. Nordeen KW, Marler P, Nordeen EJ. 1989. Addition of song-related neurons in swamp sparrows coincides with mem-orization, not production, of learned songs. J Neurobiol 20: 651–661.
104. Nottebohm F. 1985. Neuronal replacement in adulthood. Ann NYAcad Sci 457: 143–161.
105. Nottebohm F. 1989. From bird song to neurogenesis. Sci Am 260: 74–79.
106. NottebohmF. 2002. Why are some neurons replacedin adult brain? J Neurosci 22: 624–628.
107. Nottebohm F. 2004. The road we travelled: Discovery, choreography, and significance of brain replaceable neurons. Ann NYAcad Sci 1016: 628–658.
108. Nottebohm F, Nottebohm ME. 1978. Relationship between song repertoire and age in the canary, Serinus canarius. Zeitschrift-fuer-Tierpsychologie 46: 298–305.
109. Nottebohm F, O’Loughlin B, Gould K, Yohay K, Alvarez-Buylla A. 1994. The life span of new neurons in a song control nucleus of the adult canary brain depends on time of year when these cells are born. Proc Natl Acad Sci 91: 7849–7853.
110. O’Loghlen AL, Beecher MD. 1999. Mate, neighbour and stranger songs: A female song sparrow perspective. Anim Behav 58: 13–20.
111. Patel SN, Clayton NS, Krebs JR. 1997. Spatial learning induces neurogenesis in the avian brain. Behav Brain Res 89: 115–128.
112. Paton JA, Nottebohm FN. 1984. Neurons generated in the adult brain are recruited into functional circuits. Science 225: 1046–1048.
113. Piersma T, Lindstrom A. 1997. Rapid reversible changes in organ size as a component of adaptive behavior. Trends Ecol Evol 12: 134–138.
114. Pytte CL, Parent C, Wildstein S, Varghese C, Oberlander S. 2010. Deafening decreases neuronal incorporation in the zebra finch caudomedial nidopallium (NCM). Behav Brain Res 211: 141–147.
115. Rakic P. 1985. Limits of neurogenesis in primates. Science 227: 1054–1056.
116. Rasika S, Nottebohm F,Alvarez-BuyllaA.1994. Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. Proc Natl Acad Sci 91: 7854–7888.
117. Rasika S, Alvarez-Buylla A, Nottebohm F. 1999. BDNF mediates the effects of testosterone on the survival of new neurons in an adult brain. Neuron 22: 53–62.
118. Rochefort C, Gheusi G, Vincent JD, Lledo PM. 2002. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 22: 2679–2689.
119. Sakata JT, Brainard MS. 2006. Real-time contributions of auditory feedback to avian vocal motor control. J Neuro-sci 26: 9619–9628.
120. Scharff C, Nottebohm F, Cynx J. 1998. Conspecific and het-erospecific song discrimination in male zebra finches with lesionsin the anterior forebrain pathway.J Neurobiol 36: 81–90.
121. Scharff C, Kirn JR, Grossman M, Macklis JD, Nottebohm F. 2000. Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds. Neuron 25: 481–492.
122. Scott BB, Lois C. 2007. Developmental origin and identity of song system neurons born during vocal learning in songbirds. J Comp Neurol 502: 202–214.
123. Scott BB, Gardner T, Ji N, Fee MS, Lois C. 2012. Wandering neuronal migration in the postnatal vertebrate forebrain. J Neurosci 32: 1436–1446.
124. Scotto-Lomassese S, Rochefort C, Nshdejan A, Scharff C. 2007. HVC interneurons are not renewed in adult male zebra finches. Eur J Neurosci 25: 1663–1668.
125. Shultz S, Dunbar R. 2010. Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality. Proc Natl Acad Sci 107: 21582–21586.
126. 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.
127. Singh TD, Heinrich JE, Wissman AM, Brenowitz EA, Nordeen EJ, Nordeen KW. 2003. Seasonal regulation of NMDA receptor NR2B mRNA in the adult canary song system. J Neurobiol 54: 593–603.
128. Smith GT, Brenowitz EA, Wingfield JC, Baptista LF. 1995. Seasonal changes in song nuclei and song behavior in Gambel’s white-crowned sparrows. J Neurobiol 28: 114–125.
129. Smith GT, Brenowitz EA, Beecher MD, Wingfield JC. 1997. Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure inwild songbirds. J Neurosci 17: 6001–6010.
130. Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Boström E, Westerlund I, Vial C, et al. 2013. Dynamics of hippocampal neurogenesis in adult humans. Cell 153: 1219–1227.
131. Stoddard PK, Beecher MD, Horning CL, Campbell SE. 1991. Recognition of individual neighbors by song in the song sparrow, a species with song repertoires. Behav Ecol Sociobiol 29: 211–215.
132. Sturdy CB, Wild JM, Mooney R. 2003. Respiratory and tel-encephalic modulation of vocal motor neurons in the zebra finch. J Neurosci 23: 1072–1086.
133. Suberbielle E, Sanchez PE, Kravitz AV, Wang X, Ho K, Ei-lertson K, Devidze N, Kreitzer AC, Mucke L. 2013. Physiologic brain activitycauses DNA double-strand breaks in neurons, with exacerbation by amyloid-b. Nat Neurosci 16: 613–621.
134. Tashiro A, Sandler VM, Toni N, Zhao C, Gage FH. 2006. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442: 929–933.
135. Thompson CK. 2011. Cell death and the song control system: A model for how sex steroid hormones regulate naturally occurring neurodegeneration. Dev Growth Differ 53: 213–224.
136. Thompson CK, Brenowitz EA. 2005. Seasonal change in neuron size and spacing but not neuronal recruitment in a basal ganglia nucleus in the avian song control system. J Comp Neurol 481: 276–283.
137. Thompson CK, Brenowitz EA. 2008. Caspase inhibitor infusion protects an avian song control circuit from seasonal-like neurodegeneration. J Neurosci 28: 7130–7136.
138. Thompson CK, Brenowitz EA. 2009. Neurogenesis in an adult avian song nucleus is reduced by decreasing cas-pase-mediated apoptosis. J Neurosci 29: 4586–4591.
139. Thompson CK, Brenowitz EA. 2010. Neuroprotective effects of testosterone in a naturally occurring model of neuro-degeneration in the adult avian song control system. J Comp Neurol 518: 4760–4770.
140. Thompson CK, Bentley GE, Brenowitz EA. 2007. Rapid seasonal-like regression of the adult avian song control system. Proc Natl Acad Sci 104: 15520–15525.
141. Thompson CK, Meitzen J, Replogle K, Drnevich J, Lent KL, Wissman AM, Farin FM, Bammler TK, Beyer RP, Clayton DF, et al. 2012. Seasonal changes in patterns of gene expression in avian song control brain regions. PLoS ONE 7: e35119.
142. Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE, Gage FH, Schinder AF. 2008. Neurons bornin the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 11: 901–907.
143. Tramontin AD, Brenowitz EA. 1999. A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning. J Neuro-biol 40: 316–326.
144. Tramontin AD, Brenowitz EA. 2000. Seasonal plasticity in the adult brain. Trends Neurosci 23: 251–258.
145. Tramontin AD, Hartman VN, Brenowitz EA. 2000. Breeding conditions induce rapid and sequential growth in adult avian song control circuits: A model of seasonal plasticity in the brain. J Neurosci 20: 854–861.
146. Tramontin AD, Perfito N, Wingfield JC, Brenowitz EA. 2001. Seasonal growth of song control nuclei precedes seasonal reproductive development in wild adult song sparrows. Gen Comp Endocrinol 122: 1–9.
147. Tumer EC, Brainard MS. 2007. Performance variability enables adaptive plasticity of “crystallized” adult birdsong. Nature 450: 1240–1244.
148. Vellema M, Van der Linden A, Gahr M. 2010. Area-specific migration and recruitment of new neurons in the adult songbird brain. J Comp Neurol 518: 1442–1459.
149. Wada K, Sakaguchi H, Jarvis ED, Hagiwara M. 2004. Differential expression of glutamate receptors in avian neural pathways for learned vocalization. J Comp Neurol 476: 44–64.
150. Walton C, Pariser E, Nottebohm F. 2012. The zebra finch paradox: Song is little changed, but number of neurons doubles. J Neurosci 32: 761–774.
151. Wang Y, Qin AH. 2010. Molecular and cellular mechanisms of excitotoxic neuronal death. Apoptosis 15: 1382–1402.
152. Wang N, Aviram R, Kirn JR. 1999. Deafening alters neuron turnover within the telencephalic motor pathway for song control in adult zebra finches. J Neurosci 19: 10554–10561.
153. Wang N, Hurley P, Pytte C, Kirn JR. 2002. Vocal control neuron incorporation decreases with age in the adult zebra finch. J Neurosci 22: 10864–10870.
154. Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW, Kunstner A, Searle S, White S, Vilella AJ, Fairley S,et al. 2010. The genome of a songbird. Nature 464: 757–762.
155. Wennstrom KL, Reeves BJ, Brenowitz EA. 2001. Testosterone treatment increases the metabolic capacity of adult avian song control nuclei. J Neurobiol 48: 256–264.
156. Westenbroek C, Den Boer JA, Veenhuis M, Ter Horst GJ. 2004. Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Res Bull 64: 303–308.
157. Wilbrecht L. 2003. “The recruitment of new neurons to the song system during the sensitive period for song learning in the zebra finch.” PhD thesis, Rockefeller University, New York.
158. Wilbrecht L, Kirn JR. 2004. Neuron addition and loss in the song system: Regulation and function. Ann NY Acad Sci 1016: 659–683.
159. Wilbrecht L, Nottebohm F. 2004. Age and experience affect the recruitment of new neurons to the song system of zebra finches during the sensitive period for song learn- ing: Ditto for vocal learning in humans? Ann NY Acad Sci 1021: 404–409.
160. Wilbrecht L, Crionas A, Nottebohm F. 2002. Experience affects recruitment of new neurons but not adult neuron number. J Neurosci 22: 825–831.
161. Wissman AM, Brenowitz EA. 2009. The role of neurotro-phins in the seasonal-like growth of the avian song control system. J Neurosci 29: 6461–6471.
162. Woolley SM, Rubel EW. 1997. Bengalese finches Lon-chura Striata domestica depend upon auditory feedback for the maintenance of adult song. J Neurosci 17: 6380–6390.
163. Yoshii A, Constantine-Paton M. 2007. BDNF induces transport ofPSD-95 todendrites through PI3K-AKTsignaling after NMDA receptor activation. Nat Neurosci 10: 702–711.
164. Zhang Y, Tounekti O, Akerman B, Goodyer CG, LeBlanc A. 2001. 17-b-estradiol induces an inhibitor of active cas-pases. J Neurosci 21: RC176.