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Young, active and well-connected: adult-born neurons in the zebra finch are activated during singing

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Abstract

Neuronal replacement in the pallial song control nucleus HVC of adult zebra finches constitutes an interesting case of homeostatic plasticity; in spite of continuous addition and attrition of neurons in ensembles that code song elements, adult song remains remarkably invariant. New neurons migrate into HVC and later synapse with their target, arcopallial song nucleus RA (HVCRA). New HVCRA neurons respond to auditory stimuli (in anaesthetised animals), but whether and when they become functionally active during singing is unknown. We studied this, using 5-bromo-2′-deoxyuridine to birth-date neurons, combined with immunohistochemical detection of immediate-early gene (IEG) expression and retrograde tracer injections into RA to track connectivity. Interestingly, singing was followed by IEG expression in a substantial fraction of new neurons that were not retrogradely labelled from RA, suggesting a possible role in HVC-intrinsic network function. As new HVC neurons matured, the proportion of HVCRA neurons that expressed IEGs after singing increased significantly. Since it was previously shown that singing induces IEG expression in HVC also in deaf birds and that hearing song does not induce IEG expression in HVC, our data provide the first direct evidence that new HVC neurons are engaged in song motor behaviour.

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References

  • Aimone JB, Wiles J, Gage FH (2006) Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 9:723–727

    Article  CAS  PubMed  Google Scholar 

  • Alonso M, Lepousez G, Sebastien W, Bardy C, Gabellec MM, Torquet N, Lledo PM (2012) Activation of adult-born neurons facilitates learning and memory. Nat Neurosci 15:897–904

    Article  CAS  PubMed  Google Scholar 

  • Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. 3. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J Comp Neurol 136:269–293

    Article  CAS  PubMed  Google Scholar 

  • Altman J, Das GD (1965) Post-natal origin of microneurones in the rat brain. Nature 207:953–956

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Buylla A, Kirn JR (1997) Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J Neurobiol 33:585–601

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Buylla A, Lim DA (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41:683–686

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Buylla A, Nottebohm F (1988) Migration of young neurons in adult avian brain. Nature 335:353–354

    Article  CAS  PubMed  Google Scholar 

  • Amador A, Perl YS, Mindlin GB, Margoliash D (2013) Elemental gesture dynamics are encoded by song premotor cortical neurons. Nature 495:59–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barnea A, Nottebohm F (1994) Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci USA 91:11217–11221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berninger B, Marty S, Zafra F, da Penha Berzaghi M, Thoenen H, Lindholm D (1995) GABAergic stimulation switches from enhancing to repressing BDNF expression in rat hippocampal neurons during maturation in vitro. Development 121:2327–2335

    CAS  PubMed  Google Scholar 

  • Blättler F, Hahnloser RH (2011) An efficient coding hypothesis links sparsity and selectivity of neural responses. PLoS One 6:e25506

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Cardin JA, Schmidt MF (2004) Auditory responses in multiple sensorimotor song system nuclei are co-modulated by behavioral state. J Neurophysiol 91:2148–2163

    Article  PubMed  Google Scholar 

  • Carlen M, Cassidy RM, Brismar H, Smith GA, Enquist LW, Frisen J (2002) Functional integration of adult-born neurons. Curr Biol 12:606–608

    Article  CAS  PubMed  Google Scholar 

  • Cayre M, Malaterre J, Scotto-Lomassese S, Strambi C, Strambi A (2002) The common properties of neurogenesis in the adult brain: from invertebrates to vertebrates. Comp Biochem Physiol B Biochem Mol Biol 132:1–15

    Article  PubMed  Google Scholar 

  • Charvet CJ, Striedter GF (2011a) Causes and consequences of expanded subventricular zones. Eur J Neurosci 34:988–993

    Article  PubMed  Google Scholar 

  • Charvet CJ, Striedter GF (2011b) Developmental modes and developmental mechanisms can channel brain evolution. Front Neuroanat 5:4. doi:10.3389/fnana.2011.00004

  • Cole AJ, Saffen DW, Baraban JM, Worley PF (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340:474–476

    Article  CAS  PubMed  Google Scholar 

  • Curtis MA, Kam M, Faull RL (2011) Neurogenesis in humans. Eur J Neurosci 33:1170–1174

    Article  PubMed  Google Scholar 

  • Duque A, Rakic P (2011) Different effects of bromodeoxyuridine and [3H]thymidine incorporation into DNA on cell proliferation, position, and fate. J Neurosci 31:15205–15217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dutar P, Vu HM, Perkel DJ (1998) Multiple cell types distinguished by physiological, pharmacological, and anatomic properties in nucleus HVc of the adult zebra finch. J Neurophysiol 80:1828–1838

    CAS  PubMed  Google Scholar 

  • Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317

    Article  CAS  PubMed  Google Scholar 

  • Ernst A, Alkass K, Bernard S, Salehpour M, Perl S, Tisdale J, Possnert G, Druid H, Frisen J (2014) Neurogenesis in the striatum of the adult human brain. Cell 156:1072–1083

    Article  CAS  PubMed  Google Scholar 

  • Fee MS, Kozhevnikov AA, Hahnloser RH (2004) Neural mechanisms of vocal sequence generation in the songbird. Ann N Y Acad Sci 1016:153–170

    Article  PubMed  Google Scholar 

  • Feenders G, Liedvogel M, Rivas M, Zapka M, Horita H, Hara E, Wada K, Mouritsen H, Jarvis ED (2008) Molecular mapping of movement-associated areas in the avian brain: a motor theory for vocal learning origin. PLoS One 3:e1768

    Article  PubMed  PubMed Central  Google Scholar 

  • Fleischmann A, Hvalby O, Jensen V, Strekalova T, Zacher C, Layer LE, Kvello A, Reschke M, Spanagel R, Sprengel R, Wagner EF, Gass P (2003) Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J Neurosci 23:9116–9122

    CAS  PubMed  Google Scholar 

  • Font E, Desfilis E, Perez-Canellas MM, Garcia-Verdugo JM (2001) Neurogenesis and neuronal regeneration in the adult reptilian brain. Brain Behav Evol 58:276–295

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Foster EF, Bottjer SW (1998) Axonal connections of the high vocal center and surrounding cortical regions in juvenile and adult male zebra finches. J Comp Neurol 397:118–138

    Article  CAS  PubMed  Google Scholar 

  • Gahr M, Garcia-Segura LM (1996) Testosterone-dependent increase of gap-junctions in HVC neurons of adult female canaries. Brain Res 712:69–73

    Article  CAS  PubMed  Google Scholar 

  • Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589–593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ge S, Sailor KA, Ming GL, Song H (2008) Synaptic integration and plasticity of new neurons in the adult hippocampus. J Physiol 586:3759–3765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldberg JH, Fee MS (2012) A cortical motor nucleus drives the basal ganglia-recipient thalamus in singing birds. Nat Neurosci 15:620–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldman SA, Nedergaard M (1992) Newly generated neurons of the adult songbird brain become functionally active in long-term culture. Brain Res Dev Brain Res 68:217–223

    Article  CAS  PubMed  Google Scholar 

  • 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 USA 80:2390–2394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8:481–488

    Article  CAS  PubMed  Google Scholar 

  • Graber MH, Helmchen F, Hahnloser RH (2013) Activity in a premotor cortical nucleus of zebra finches is locally organized and exhibits auditory selectivity in neurons but not in glia. PLoS One 8:e81177

    Article  PubMed  PubMed Central  Google Scholar 

  • Guzowski JF, Setlow B, Wagner EK, McGaugh JL (2001) Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J Neurosci 21:5089–5098

    CAS  PubMed  Google Scholar 

  • Hahnloser RH, Kozhevnikov AA, Fee MS (2002) An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419:65–70

    Article  CAS  PubMed  Google Scholar 

  • Hessler NA, Doupe AJ (1999) Social context modulates singing-related neural activity in the songbird forebrain. Nat Neurosci 2:209–211

    Article  CAS  PubMed  Google Scholar 

  • Hughes PE, Young D, Preston KM, Yan Q, Dragunow M (1998) Differential regulation by MK801 of immediate-early genes, brain-derived neurotrophic factor and trk receptor mRNA induced by a kindling after-discharge. Brain Res Mol Brain Res 53:138–151

    Article  CAS  PubMed  Google Scholar 

  • Hurley P, Pytte C, Kirn JR (2008) Nest of origin predicts adult neuron addition rates in the vocal control system of the zebra finch. Brain Behav Evol 71:263–270

    Article  PubMed  PubMed Central  Google Scholar 

  • Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153–1161

    Article  CAS  PubMed  Google Scholar 

  • Jarvis ED, Nottebohm F (1997) Motor-driven gene expression. Proc Natl Acad Sci USA 94:4097–4102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jarvis ED, Scharff C, Grossman MR, Ramos JA, Nottebohm F (1998) For whom the bird sings: context-dependent gene expression. Neuron 21:775–788

    Article  CAS  PubMed  Google Scholar 

  • Jessberger S, Kempermann G (2003) Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur J Neurosci 18:2707–2712

    Article  PubMed  Google Scholar 

  • Jin DZ, Ramazanoglu FM, Seung HS (2007) Intrinsic bursting enhances the robustness of a neural network model of sequence generation by avian brain area HVC. J Comput Neurosci 23:283–299

    Article  PubMed  Google Scholar 

  • Jones MW, Errington ML, French PJ, Fine A, Bliss TV, Garel S, Charnay P, Bozon B, Laroche S, Davis S (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4:289–296

    Article  CAS  PubMed  Google Scholar 

  • Kee N, Teixeira CM, Wang AH, Frankland PW (2007) Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10:355–362

    Article  CAS  PubMed  Google Scholar 

  • Kempermann G (2014) Off the beaten track: new neurons in the adult human striatum. Cell 156:870–871

    Article  CAS  PubMed  Google Scholar 

  • Kempermann G, Wiskott L, Gage FH (2004) Functional significance of adult neurogenesis. Curr Opin Neurobiol 14:186–191

    Article  CAS  PubMed  Google Scholar 

  • Kimpo RR, Doupe AJ (1997) FOS is induced by singing in distinct neuronal populations in a motor network. Neuron 18:315–325

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kirn JR, 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 USA 91:7844–7848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirn JR, Fishman Y, Sasportas K, Alvarez-Buylla A, Nottebohm 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

    Article  CAS  PubMed  Google Scholar 

  • Kojima S, Doupe AJ (2009) Activity propagation in an avian basal ganglia-thalamocortical circuit essential for vocal learning. J Neurosci 29:4782–4793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kozhevnikov AA, Fee MS (2007) Singing-related activity of identified HVC neurons in the zebra finch. J Neurophysiol 97:4271–4283

    Article  PubMed  Google Scholar 

  • Kruse AA, Stripling R, Clayton DF (2000) Minimal experience required for immediate-early gene induction in zebra finch neostriatum. Neurobiol Learn Mem 74:179–184

    Article  CAS  PubMed  Google Scholar 

  • Kubikova L, Turner EA, Jarvis ED (2007) The pallial basal ganglia pathway modulates the behaviorally driven gene expression of the motor pathway. Eur J Neurosci 25:2145–2160

    Article  PubMed  PubMed Central  Google Scholar 

  • LaDage LD, Roth TC 2nd, Pravosudov VV (2011) Hippocampal neurogenesis is associated with migratory behaviour in adult but not juvenile sparrows (Zonotrichia leucophrys ssp.). Proc Biol Sci 278:138–143

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 USA 97:8584–8589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma DK, Kim WR, Ming GL, Song H (2009) Activity-dependent extrinsic regulation of adult olfactory bulb and hippocampal neurogenesis. Ann N Y Acad Sci 1170:664–673

    Article  PubMed  PubMed Central  Google Scholar 

  • MacGibbon GA, Lawlor PA, Hughes P, Young D, Dragunow M (1995) Differential expression of inducible transcription factors in basal ganglia neurons. Brain Res Mol Brain Res 34:294–302

    Article  CAS  PubMed  Google Scholar 

  • Magavi SS, Mitchell BD, Szentirmai O, Carter BS, Macklis JD (2005) Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo. J Neurosci 25:10729–10739

    Article  CAS  PubMed  Google Scholar 

  • Mileusnic R, Anokhin K, Rose SP (1996) Antisense oligodeoxynucleotides to c-fos are amnestic for passive avoidance in the chick. NeuroReport 7:1269–1272

    Article  CAS  PubMed  Google Scholar 

  • Mongiat LA, Esposito MS, Lombardi G, Schinder AF (2009) Reliable activation of immature neurons in the adult hippocampus. PLoS One 4:e5320

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Nissant A, Bardy C, Katagiri H, Murray K, Lledo PM (2009) Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat Neurosci 12:728–730

    Article  CAS  PubMed  Google Scholar 

  • Nixdorf BE, Davis SS, DeVoogd TJ (1989) Morphology of Golgi-impregnated neurons in hyperstriatum ventralis, pars caudalis in adult male and female canaries. J Comp Neurol 284:337–349

    Article  CAS  PubMed  Google Scholar 

  • Nottebohm F, Stokes TM, Leonard CM (1976) Central control of song in the canary, Serinus canarius. J Comp Neurol 165:457–486

    Article  CAS  PubMed  Google Scholar 

  • Nowakowski RS, Lewin SB, Miller MW (1989) Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 18:311–318

    Article  CAS  PubMed  Google Scholar 

  • Paton JA, Nottebohm FN (1984) Neurons generated in the adult brain are recruited into functional circuits. Science 225:1046–1048

    Article  CAS  PubMed  Google Scholar 

  • Prather JF, Peters S, Nowicki S, Mooney R (2008) Precise auditory-vocal mirroring in neurons for learned vocal communication. Nature 451:305–310

    Article  CAS  PubMed  Google Scholar 

  • Pytte CL, Gerson M, Miller J, Kirn JR (2007) Increasing stereotypy in adult zebra finch song correlates with a declining rate of adult neurogenesis. Dev Neurobiol 67:1699–1720

    Article  PubMed  Google Scholar 

  • Rakic P (2002) Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat Rev Neurosci 3:65–71

    Article  CAS  PubMed  Google Scholar 

  • Rauske PL, Shea SD, Margoliash D (2003) State and neuronal class-dependent reconfiguration in the avian song system. J Neurophysiol 89:1688–1701

    Article  PubMed  Google Scholar 

  • Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch DH, Alvarez-Buylla A (2011) Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478:382–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki A, Sotnikova TD, Gainetdinov RR, Jarvis ED (2006) Social context-dependent singing-regulated dopamine. J Neurosci 26:9010–9014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Schmidt-Hieber C, Jonas P, Bischofberger J (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184–187

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Scott BB, Gardner T, Ji N, Fee MS, Lois C (2012) Wandering neuronal migration in the postnatal vertebrate forebrain. J Neurosci 32:1436–1446

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Shea SD, Koch H, Baleckaitis DD, Ramirez JM, Margoliash D (2009) Neuron-specific cholinergic modulation of a forebrain song control nucleus. J Neurophysiol 103(2):733–745

    Article  PubMed  PubMed Central  Google Scholar 

  • Sossinka R, Böhner J (1980) Song types in the zebra finch (Poephila guttata castanotis). Z Tierpsychol 53:123–132

  • Stokes TM, Leonard CM, Nottebohm F (1974) The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J Comp Neurol 156:337–374

    Article  CAS  PubMed  Google Scholar 

  • Tashiro A, Makino H, Gage FH (2007) Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J Neurosci 27:3252–3259

    Article  CAS  PubMed  Google Scholar 

  • Tchernichovski O, Nottebohm F, Ho CE, Pesaran B, Mitra PP (2000) A procedure for an automated measurement of song similarity. Anim Behav 59:1167–1176

    Article  PubMed  Google Scholar 

  • Tokarev K, Tiunova A, Scharff C, Anokhin K (2011) Food for song: expression of C-Fos and ZENK in the Zebra Finch song nuclei during food aversion learning. PLoS One 6:e21157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47:803–815

    Article  CAS  PubMed  Google Scholar 

  • 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 Neurobiol 40:316–326

    Article  CAS  PubMed  Google Scholar 

  • Vates GE, Vicario DS, Nottebohm F (1997) Reafferent thalamo—“cortical” loops in the song system of oscine songbirds. J Comp Neurol 380:275–290

    Article  CAS  PubMed  Google Scholar 

  • Wada K, Howard JT, McConnell P, Whitney O, Lints T, Rivas MV, Horita H, Patterson MA, White SA, Scharff C, Haesler S, Zhao S, Sakaguchi H, Hagiwara M, Shiraki T, Hirozane-Kishikawa T, Skene P, Hayashizaki Y, Carninci P, Jarvis ED (2006) A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. Proc Natl Acad Sci USA 103:15212–15217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Woolley SC, Doupe AJ (2008) Social context-induced song variation affects female behavior and gene expression. PLoS Biol 6:e62

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu AC, Margoliash D (1996) Temporal hierarchical control of singing in birds. Science 273:1871–1875

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645–660

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Parts of this work were funded by SFB (Sonderforschungsbereich) 655. KT is grateful for generous support provided by a fellowship from the Boehringer Ingelheim Fonds. We appreciate Philip Rebensburg’s contribution to analysis of data on new neurons in Area X. We thank Volker Haucke and his group for technical support in microscopy. Jonathan Benichov provided useful commentary on the original manuscript.

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The authors declare that they have no conflict of interest.

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Correspondence to Constance Scharff.

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Tokarev, K., Boender, A.J., Claßen, G.A.E. et al. Young, active and well-connected: adult-born neurons in the zebra finch are activated during singing. Brain Struct Funct 221, 1833–1843 (2016). https://doi.org/10.1007/s00429-015-1006-y

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