Abstract
The discovery of neurogenesis in adult canaries came as a surprise because it was found in a context where it had not been contemplated, the study of vocal learning. To everybody’s disbelief, the new, spontaneously produced neurons replaced numerically others that had died, a process of spontaneous brain self-repair or rejuvenation. I will describe how these discoveries came about and how they have helped us understand the natural history of neurogenesis and neuronal replacement in adult brain. Adult neurogenesis may also shed light on a basic issue of brain function: what limits learning?
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adar, E., Nottebohm, F., Barnea, A. 2008. The relationship between nature of social change, age and position of new neurons and their survival in adult zebra finch brain. J. Neurosci. 28:5394–5400.
Agate, R.J., Grisham, W., Wade, J., Mann, S., Wingfield, J., Schanen, C., Palotie, A., Arnold, A.P. 2003. A neural, not gonadal, origin of brain sex differences in a gynandromorphic finch. Proc. Natl. Acad. Sci. USA 100:4873–4878.
Agate, R.J., Choe, M., Arnold, A.P. 2004. Sex differences in structure and expression of the sex chromosome genes CHD1Z and CHD1W in zebra finches. Mol. Biol. Evol. 21:384–396.
Airey, D.C., Kroodsma, D.E., DeVoogd, T.J. 2000. Differences in the complexity of song tutoring cause differences in the amount learned and in dendritic spine density in a songbird telencephalic song control nucleus. Neurobiol. Learn. Mem. 73:274–281.
Altman, J. 1962. Are new neurons formed in the brains of adult mammals? Science 135:1127–1128.
Altman, J. 1963. Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat. Rec. 145:573–591.
Altman, J. 1967. Postnatal growth and differentiation of the mammalian brain, with implications for a morphological theory of memory. In “The Neurosciences, a Study Program”, G.C. Quarton, T. Melnechuck, F.O. Schmidt, eds., pp. 723–743. The Rockefeller University Press, New York.
Altman, J. 1969. DNA metabolism and cell proliferation. In “Structural Neurochemistry”, A. Lajtha, ed. Plenum Press, New York/London, Handbook of Neurochemistry, vol II, pp. 137–182.
Altman, J. 1970. Postnatal neurogenesis and the problem of neural plasticity. In “Developmental Neurobiology”, pp.197–237.
Altman, J., Bulut, F.G. 1976. Organic maturation and the development of learning capacity. In “Neural Mechanisms of Learning and Memory”, M.R. Rosenzweig, E.L. Bennett, eds., pp. 236–240. MIT Press.
Altman, J., Das, G.D. 1965. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–335.
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.
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. USA 101:3957–3961.
Alvarez-Buylla, A., Lim, D.A. 2004. For the long run: maintaining germinal niches in the adult brain. Neuron 41:683–686.
Alvarez-Buylla, A., Nottebohm, F. 1988. Migration of young neurons in adult avian brain. Nature 335:353–354.
Alvarez-Buylla, A., Buskirk, D.R., Nottebohm, F. 1987. Monoclonal antibody reveals radial glia in adult avian brain. J. Comp. Neurol. 264:159–170.
Alvarez-Buylla, A., Theelen, M., Nottebohm, F. 1988a. Birth of projection neurons in the higher vocal center of the canary forebrain before, during and after song learning. Proc. Natl. Acad. Sci. USA. 85:8722–8726.
Alvarez-Buylla, A., Theelen, M., Nottebohm, F. 1988b. Mapping of radial glia and of a new cell type in adult canary brain. J. Neurosci. 8:2707–2712.
Alvarez-Buylla, A., Kirn, J.R., Nottebohm, F. 1990a. Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science 249:1444–1446.
Alvarez-Buylla, A., Theelen, M., Nottebohm, F. 1990b. Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division. Neuron 5:101–109.
Alvarez-Buylla, A., Ling, C-Y., Nottebohm, F. 1992. High vocal center growth and its relation to neurogenesis, neuronal replacement and song acquisition in juvenile canaries. J. Neurobiol. 23:396–406.
Alvarez-Buylla, A., Garcia-Verdugo, J.M., Mateo, A.S., Merchant-Larios, H. 1998. Primary neural precursors and intermitotic nuclear migration in the ventricular zone of adult canaries. J. Neurosci. 18:1020–1037.
Alvarez-Buylla, A., Seri, B., Doetsch, F. 2002. Identification of neural stem cells in the adult vertebrate brain. Brain Res. Bull. 57:751–758.
Andalman, A.S., Fee, M.S. 2009. A basal ganglia-forebrain circuit in the songbird biases motor output to avoid vocal errors. Proc. Natl. Acad. Sci. USA 106:12518–12523.
Anderson, M.J., Waxman, S.G. 1985. Neurogenesis in adult vertebrate spinal cord in situ and in vitro: a new model system. In “Hope for a New Neurology”, F. Nottebohm, ed., Ann. N.Y. Acad. Sci., vol 457, pp. 213–233.
Angevine, J.B. 1965. Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp. Neurol. Suppl. 2:1–70.
Arnold, A.P., Nottebohm, F., Pfaff, D.W. 1976. Hormone concentrating cells in vocal control and other areas of the brain of the zebra finch. J. Comp. Neurol. 165:487–512.
Aronov, D., Andalman, A.S., Fee, M.S. 2008. A specialized forebrain circuit for vocal babbling in the juvenile songbird. Science 320:630–634.
Barnea, A., Nottebohm, F. 1994. Seasonal recruitment of new neurons in the hippocampus of adult, free-ranging black-capped chickadees. Proc. Natl. Acad. Sci. USA 91:11217–11221.
Barnea, A., Nottebohm, F. 1996. Recruitment and replacement of hippocampal neurons in young and adult chickadees: an addition to the theory of hippocampal learning. Proc. Natl. Acad. Sci. USA 93:714–718.
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.
Bayer, S.A. 1985. Neuron production in the hippocampus and olfactory bulb of the adult rat brain: addition or replacement? In “Hope for a New Neurology”, F. Nottebohm, ed., Ann. N.Y. Acad. Sci., vol 457, pp. 163–172.
Bayer, S.A., Yackel, J.W., Puri, P.S. 1982. Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216:890–892.
Birse, S.C., Leonard, R.B., Coggeshall, R.E. 1980. Neuronal increase in various areas of the nervous system of the guppy, Lebistes. J. Comp. Neurol. 194:291–301.
Boehner, J. 1990. Early acquisition of song in the zebra finch, Taeniopygia guttata. Anim. Behav. 39:369–374.
Bottjer, S.W., Miesner, E.A., Arnold, A.P. 1984. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224:901–903.
Bottjer, S.W., Halsema, K.A., Brown, S.A., Miesner, E.A. 1989. Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches. J. Comp. Neurol. 279:312–326.
Brainard, M.S., Doupe, A.J. 2000. Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404:762–766.
Brainard, M.S., Doupe, A.J. 2001. Postlearning consolidation of birdsong: stabilizing effects of age and anterior forebrain lesions. J. Neurosci. 21:2501–2517.
Breunig, J.J et al. 2007. Everything that glitters isn’t gold: a critical review of postnatal neural precursor analyses. Stem Cell Res. 1:612–627.
Bryans, W.A. 1959. Mitotic activity in the brain of the adult rat. Anat. Rec. 133:65–71.
Bullock, T.H. 1961. The origins of patterned nervous discharge. Behaviour 17:48–59.
Burd, G.D., 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.
Burek, M.J., Nordeen, K.W., Nordeen, E.J. 1991. Neuron loss and addition in developing zebra finch song nuclei are independent of auditory experience during song learning. J. Neurobiol. 22:215–223.
Cajal, S.R. 1894. The Croonian Lecture. La fine structure des centres nerveux. Proc. R. soc. Lond. B 55:444–467.
Cajal, S.R. 1911. Histologie du Systeme Nerveux, vol. 2, pp. 80–119. Maloire, Paris.
Canady, R.A., Kroodsma, D.E., Nottebohm, F. 1984. Population differences in complexity of a learned skill are correlated with brain space involved. Proc. Natl. Acad. Sci. USA 81:6232–6234.
Canady R.A., Burd, G.B., DeVoogd, T.J., Nottebohm, F. 1988. Effect of testosterone on input received by an identified neuron type of the canary song system: a Golgi/EM/Degeneration study. J. Neurosci. 8:3770–3784.
Cardin, J.A., Schmidt, M.F. 2004. Auditory responses in multiple sensorimotor song system nuclei are co-modulated by behavioral state. J. Neurophysiol. 91:2148–2163.
Dave, A.S., Yu, A.C., Margoliash, D. 1998. Behavioral state modulation of auditory activity in a vocal motor system. Science 282:2250–2254.
Dayer, A.G., Cleaver K.M., Abouantoun, T., Cameron, H.A. 2005. New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J. Cell Biol. 168:415–427.
DeVoogd, T.J., Nottebohm, F. 1981. Gonadal hormones induce dendritic growth in the adult brain. Science 214:202–204.
DeVoogd, T.J., Nixdorf, B., Nottebohm, F. 1985. Synaptogenesis and changes in synaptic morphology related to acquisition of a new behavior. Brain Res. 329:304–308.
DeVoogd, T.J., Pyskaty, D.J., Nottebohm, F. 1991. Lateral asymmetries and testosterone-induced changes in the gross morphology of the hypoglossal nucleus in adult canaries. J. Comp. Neurol. 307:65–76.
DeVoogd, T.J., Krebs, J.R., Healy, S.D., Purvis, A. 1993. Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses amongst oscine birds. Proc. R. Soc. Lond. B 254:75–82.
Doetsch, F., Caille, I., Lim, D.A., Garcia-Verdugo, J.M., Alvarez-Buylla, A. 1999. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703–716.
Eales, L.A. 1985. Song learning in zebra finches: some effects of song model availability on what is learnt and when. Anim. Behav. 33:1293–1300.
Easter, S.S., Jr. 1983. Postnatal neurogenesis and changing connections. Trends Neurosci. 6:53–56.
Goldman, S.A., 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.
Gould, E., Reeves, A.J., Graziano M.S.A., Gross, C.G. 1999. Neurogenesis in the neocortex of adult primates. Science 286:548–552.
Graziadei, P.P.C., DeHan, R.S. 1973. Neuronal regeneration in frog olfactory system. J. Cell Biol. 59:525–530.
Graziadei, P.P.C., Monti Graziadei, G.A. 1978. Continuous cell renewal in the olfactory system. In “Handbook of Sensory Physiology”, M. Jacobson, ed., vol IX, pp. 55–83. Springer Verlag, Berlin.
Graziadei, P.P.C., Monti Graziadei, G.A. 1985. Neurogenesis and plasticity of the olfactory sensory neurons. In “Hope for a New Neurology”, F. Nottebohm, ed., Ann. N.Y. Acad. Sci., vol 457, pp. 143–161.
Gurney, M.E. 1981. Hormonal control of cell form and number in the zebra finch song system. J. Neurosci. 1:658–673.
Gurney, M.E., Konishi, M. 1980. Hormone induced sexual differentiation of brain and behavior in zebra finches. Science 208:1380–1383.
Hahnloser, R.H., Kozhevnikov, A.A., Fee, M.S. 2002. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419:65–70.
Hebb, D.O. 1949. The organization of behavior. John Wiley & Sons, New York.
Huber, F. 1960. Untersuchungen ueber die Funktion des Zentralnervensystems und insbesondere des Gehirns bei der Fortbewegung und der Lauterzeugung der Grillen. Z. vergl. Physiol. 44:60–132.
Immelmann, K. 1969. Song development in the zebra finch and other estrildid finches. In “Bird Vocalizations”, R.A. Hinde, ed., pp. 61–74. Cambridge Univ. Press, London & New York.
Janata, P., Margoliash, D. 1999. Gradual emergence of song selectivity in sensorimotor structures of the male zebra finch song system. J. Neurosci. 19:5108–5118.
Johns, P.R. 1982. Formation of photoreceptors in larval and adult goldfish. J. Neurosci. 2:178–198.
Kandel, E.R. 2006. In search of memory. W.W. Norton & Co., New York and London.
Kao, M.H., Doupe, A.J., Brainard, M.S. 2005. Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 433:638–643.
Kaplan, M.S. 1985. Formation and turnover of neurons in young and senescent animals: an electron microscopic and morphometric analysis. In “Hope for a New Neurology”, F. Nottebohm, ed., Ann. N.Y. Acad. Sci., vol 457, pp. 173–192.
Kaplan, M.S., Hinds, J.W. 1977. Neurogenesis in the adult rat: electron microscopic analysis of light autoradiographs. Science 197:1092–1094.
Karten, H.J., Hodos, W. 1967. A stereotaxic atlas of the brain of the pigeon (Columba livia). The Johns Hopkins Press, Baltimore.
Katz, L.C., Gurney, M.E. 1981. Auditory responses in the zebra finch’s motor system for song. Brain Res. 221:192–197.
Kirn, J.R., Nottebohm, F. 1993. Direct evidence for loss and replacement of projection neurons in adult canary brain. J. Neurosci. 13:1654–1663.
Kirn, J.R., Alvarez-Buylla, A., Nottebohm, F. 1991. Production and survival of projection neurons in the forebrain vocal center of adult male canaries. J. Neurosci. 11:1756–1762.
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. USA 91:7844–7848.
Kirn, J.R., Fishman, K., Sasportas, A., Alvarez-Buylla, F., 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.
Kittelberger, J.M., Mooney, R. 2004. Acute injections of brain-derived neurotrophic factor in a vocal premotor nucleus reversibly disrupt adult birdsong stability and trigger syllable deletion. J. Neurobiol. 62:406–424.
Koketsu, D., Mikami, A., Miyamoto, Y., Hisatsune, T. 2003. Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys. J. Neurosci. 23:937–942.
Konishi, M. 1963. The role of auditory feedback in the vocal behavior of the domestic fowl. Z. Tierpsychol. 20:349–367.
Konishi, M. 1965. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z. Tierpsychol. 22:770–783.
Konorski, J. 1948. Conditioned reflexes and neuron organization. Cambridge Univ. Press, London.
Kornack, D.R., Rakic, P. 2001. Cell proliferation without neurogenesis in adult primate neocortex. Science 294:2127–2130.
Korr, H. 1980. Proliferation of different cell types in the brain. Adv. Anat. Embryol. Cell Biol. 61:1–69.
Kriegstein, A., Alvarez-Buylla, A. 2009. The glial nature of embryonic and adult neural stem cells. Ann. Rev. Neurosci. 32:149–184.
Lahousse, E. 1888. Recherches sur l’ontogenese du cervelet. Arch. de Biol. 8:43–110.
Lashley, K.S. 1950. In search of the engram. In “Physiological Mechanisms in Animal Behavior”. Symposia Soc. Exp. Biol., vol IV, Cambridge Univ. Press, pp. 454–482.
Leonard, R.B., Goggeshall, R.E., Willis, W.D. 1978. A documentation of an age related increase in neuronal and axonal numbers in the stingray. J. Comp. Neurol. 179:13–22.
Li, X-C., Jarvis, E.D., Alvarez-Borda, B., Lim, D.A., Nottebohm, F. 2000. A relationship between behavior, neurotrophin expression and new neuron survival. Proc. Natl. Acad. Sci. USA 97:8584–8589.
Lipkind, D., Nottebohm, F., Rado, R., Barnea, A. 2002. Social change affects the survival of new neurons in the forebrain of adult songbirds. Behav. Brain Res. 133:31–43.
Long, M.A., Fee, M.S. 2008. Using temperature to analyse temporal dynamics in the songbird motor pathway. Nature 456:189–194.
Magavi, S.S., Leavitt, B.R., Macklis, J.D. 2000. Induction of neurogenesis in the neocortex of adult mice. Nature 405:951–955.
Margoliash, D. 1986. Preference for autogenous song by auditory neurons in a song system nucleus of the white-crowned sparrow. J. Neurosci. 6:1643–1661.
Marler, P. 1970a. A comparative approach to vocal learning: song learning in white-crowned sparrows. J. Comp. Physiol. Psychol. 71 (monogr.):1–25.
Marler, P. 1970b. Birdsong and speech development: could there be parallels? Am. Sci. 58:669–673.
Marler, P., Tamura, M. 1964. Culturally transmitted patterns of vocal behavior in sparrows. Science 146:1483–1486.
Marler, P., Waser, M.S. 1977. The role of auditory feedback in canary song development. J. Comp. Physiol. Psychol. 91:8–16.
Merkle, F.T., Tramontin, A.D., Garcia-Verdugo, J.M., Alvarez-Buylla, A. 2004. Proc. Natl. Acad. Sci. USA 101:17528–17532.
Messier, B., Leblond, C.P., Smart, I. 1958. Presence of DNA synthesis and mitosis in the brain of young adult mice. Exptl. Cell. Res. 14:224–226.
Miale, I.L., Sidman, R.L. 1961. An autoradiograpic analysis of histogenesis in the mouse cerebellum. Exp. Neurol. 4:277–296.
Mooney, R. 2009. Neural mechanisms for learned birdsong. Learn. Mem. 16:655–669.
Mundinger, P. 1970. Vocal imitation and individual recognition of finch calls. Science 168:480–482.
Nordeen, E.J., Nordeen, K.W. 1988. Sex and regional differences in the incorporation of neurons born during song learning in zebra finches. J. Neurosci. 8:2869–2874.
Nottebohm, F. 1971. Neural lateralization of vocal control in a passerine bird. I. Song. J. Exp. Zool. 177:229–261.
Nottebohm, F. 1972a. The origins of vocal learning. Am. Nat. 106:116–140.
Nottebohm, F. 1972b. Neural lateralization of vocal control in a passerine bird. II. Subsong, calls and a theory of vocal learning. J. Exp. Zool. 179:35–49.
Nottebohm, F. 1980a. Testosterone triggers growth of brain vocal control nuclei in adult female canaries. Brain Res. 189:429–436.
Nottebohm, F. 1980b. Brain pathways for vocal learning in birds: a review of the first 10 years. In “Progress in Psychobiology and Physiological Psychology”, J.M.S. Sprage, A.N.E. Epstein, eds., vol. 9, pp. 85–124. Academic Press, New York.
Nottebohm, F. 1981. A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science 214:1368–1370.
Nottebohm, F. 1984. Birdsong as a model in which to study brain processes related to learning. Condor 86:227–236.
Nottebohm, F. 1985. Neuronal replacement in adulthood. In “Hope for a New Neurology”,F. Nottebohm, ed., Ann. N.Y. Acad. Sci., vol 457, pp. 143–161.
Nottebohm, F. 1989. From birdsong to neurogenesis. Sci. Am. 260:74–79.
Nottebohm, F. 1993. The search for neural mechanisms that define the sensitive period for song learning in birds. Netherlands J. Zoology.
Nottebohm, F., Arnold, A.P. 1976. Sexual dimorphism in vocal control areas of the songbird brain, Science 194:211–213.
Nottebohm, F., Nottebohm, M.E. 1971. Vocalizations of breeding behavior of surgically deafened ring doves, Streptopelia risoria. Anim. Behav. 19:313–327.
Nottebohm, F., Nottebohm, M.E. 1978. Relationship between song repertoire and age in the canary, Serinus canarius. Z. Tierpsychol. 46:298–305.
Nottebohm, F., Stokes, T.M., Leonard, C.M. 1976. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165:457–486.
Nottebohm, F., Kasparian, S., Pandazis, C. 1981. Brain space for a learned task. Brain Res. 213:99–109.
Nottebohm, F., Kelley, D.B., Paton, J.A. 1982. Connections of vocal control nuclei in the canary telencephalon. J. Comp. Neurol. 207:344–357.
Nottebohm, F., Nottebohm, M.E., Crane, L.A. 1986. Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei. Behav. Neural. Biol. 46:445–471.
Nottebohm, F., Nottebohm, M.E., Crane, L.A., Wingfield, J.C. 1987. Seasonal changes in gonadal hormone levels of adult male canaries and their relation to song. Behav. Neural. Biol. 47:197–211.
Nottebohm, F. 1993. The search for neural mechanisms that define the sensitive period for song learning in birds. Netherlands J. Zoology.
Nottebohm, F., O’Loughlin, B., Gould, K., Yohay, C., Alvarez-Buylla, A. 1994. The life span of new neurons in a song control nucleus of the canary brain depends on time of year when these cells are born. Proc. Natl. Acad. Sci. USA 91:7849–7853.
Oelveczky, B.P., Andalman, A.S., Fee, M.S. 2005. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol. 3:902–908, e153.
Okuhata, S., Saito, N. 1987. Synaptic connections of thalamo-cerebral vocal nuclei of the canary. Brain Res. Bull. 18:35–44.
Paton, J.A., Nottebohm, F. 1984. Neurons generated in the adult brain are recruited into functional circuits. Science 225:1046–1048.
Raisman, G., Field, P.M. 1971. Sexual dimorphism in the preoptic area of the brain. Science 173:731–733.
Rakic, P. 1985a. Limits of neurogenesis in primates. Science 227:154–156.
Rakic, P. 1985b. DNA synthesis and cell division in the adult primate brain. In “Hope for a New Neurology”, F. Nottebohm, ed., Ann. N.Y. Acad. Sci., vol 457, pp. 193–211.
Rakic, P. 2002. Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat. Rev. Neurosci. 3:65–71.
Rasika, S., Nottebohm, F., Alvarez-Buylla, A. 1994. Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. Proc. Natl. Acad. Sci. USA 91:7854–7858.
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.
Raymond, P.A., Easter, S.S. 1983. Postembryonic growth of the optic tectum in goldfish.I. Location of germinal cells and numbers of neurons produced. J. Neurosci. 3:1077–1091.
Roberts, T.F., Tschida, K.A., Klein, M.E., Mooney, R. 2010. Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning. Nature 463:948–952.
Roeder, K.D. 1962. Neural mechanisms of animal behavior. Am. Zool. 2:105–115.
Schaper, A. 1894. Die morphologische und histologische Entwicklung des Kleinhirns. Morphol. Jahrb, 21:625–670.
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.
Scott, B.B., Lois, C. 2007. Developmental origin and identity of song system neurons born during vocal learning in songbirds. J. Comp. Neurol. 502:202–214.
Seri, B., Garcia-Verdugo, J.M., McEwen, B.S., Alvarez-Buylla, A. 2001. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21:7154–7160.
Simpson, H.B., Vicario, D.S. 1991. Early estrogen treatment of female zebra finches masculinizes the brain pathway for learned vocalizations. J. Neurobiol. 22:777–793.
Smart, I. 1961. The subependymal layer of mouse brain and its cell production as shown by radioautography after thymidine-H3 injection. J. Comp. Neurol. 116:325–348.
Stokes, T.C., Leonard, C.M., Nottebohm, F. 1974. The telencephalon, diencephalon and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J. Comp. Neurol. 156:337–374.
Sugita, N. 1918. Comparative studies on the growth of the cerebral cortex. V., pts. I and 11. J. Comp. Neur. 30:61–117.
Thorpe, W.H. 1954. The process of song learning in the chaffinch as studied by means of the sound spectrograph. Nature 173:465–469.
Thorpe, W.H. 1955. Comments on the “bird fancyer’s delight” together with notes on imitation in the subsong of the chaffinch. Ibis 97:247–251.
Thorpe, W.H. 1958. The learning of song patterns by birds, with especial reference to the song of the chaffinch, Fringilla coelebs. Ibis 100:535–570.
Thorpe, W.H., Pilcher, P.M. 1958. The nature and characteristics of sub-song. Br. Birds 51:509–514.
Uzman, L.L. 1960. The histogenesis of the mouse cerebellum as studied by its tritiated thymidine uptake. J. Comp. Neurol. 114:137–159.
Vates, G.E., Nottebohm, F. 1995. Feedback circuitry within a song learning pathway. Proc. Natl. Acad. Sci. USA 92:5139–5143.
Vates, G.E., Broome, B.M., Mello, C.V., Nottebohm, F. 1996. Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taeniopygia guttata). J. Comp. Neurol. 366:613–642.
Vates, G.E., Vicario, D.S., Nottebohm, F. 1997. Reafferent thalamo-“cortical” loops in the song system of oscine songbirds. J. Comp. Neurol. 380:275–290.
von Holst, E. 1935. Ueber den Prozess der zentralnervoesen Koordination. Pflueg. Arch. ges. Physiol. 236:149–158.
von Holst, E., von Saint Paul, U. 1960. Vom Wirkungsgefuege der Triebe. Naturwissenschaften 47:409–422.
Wade, J., Arnold, A.P. 1996. Functional testicular tissue does not masculinize development of the zebra finch song system. Proc. Natl. Acad. Sci. USA 93:5264–5268.
Waser, M.S., Marler, P. 1977. Song learning in canaries. J. Comp. Physiol. Psychol. 91:1–7.
Wiersma, C.A.G. 1962. The organization of the arthropod central nervous system. Am. Zool. 2:67–78.
Wilbrecht, L., Crionas, A., Nottebohm, F. 2002a. Experience affects recruitment of new neurons but not adult neuron number. J. Neurosci. 22:825–831.
Wilbrecht, L., Petersen, T., Nottebohm, 2002b. Bilateral LMAN lesions cancel differences in HVC neuronal recruitment induced by unilateral syringeal denervation. J. Comp. Physiol. A 188:909–915.
Wilbrecht, L., Williams, H., Gangadhar, N., Nottebohm, F. 2006. High levels of new neuron addition persist when the sensitive period for song learning is experimentally prolonged. J. Neurosci. 26:9135–9141.
Williams, H., Nottebohm, F. 1985. Auditory responses in avian vocal motor neurons: a motor theory for song perception in birds. Science 229:279–282.
Williams, H., Crane, L.A., Hale, T.K., Esposito, M.A., Nottebohm, F. 1992. Right side dominance for song control in the zebra finch. J. Neurobiol. 23:1006–1020.
Wilson, D.M. 1961. The central nervous control of flight in the locust. J. Exp. Biol. 38:471–490.
Yu, A.C., Margoliash, D. 1996. Temporal hierarchical control of singing in birds. Science 273:1871–1875.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer
About this chapter
Cite this chapter
Nottebohm, F. (2011). Song Learning in Birds Offers a Model for Neuronal Replacement in Adult Brain. In: Seki, T., Sawamoto, K., Parent, J.M., Alvarez-Buylla, A. (eds) Neurogenesis in the Adult Brain I. Springer, Tokyo. https://doi.org/10.1007/978-4-431-53933-9_2
Download citation
DOI: https://doi.org/10.1007/978-4-431-53933-9_2
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-53932-2
Online ISBN: 978-4-431-53933-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)