High Levels of New Neuron Addition Persist When the Sensitive Period for Song Learning Is Experimentally Prolonged

Socially reared zebra finch males imitate a song they hear during posthatching days 30–65; during this time, many new neurons are added to the high vocal center (HVC), a forebrain nucleus necessary for the production of learned song. New neuron addition drops sharply after day 65, and no new songs are imitated. In contrast, male zebra finches reared in isolation from other males have more variable songs at day 65 and thereafter can still imitate new sounds (Eales, 1985). We show that, in isolate birds, a greater number of new neurons continues to be added to HVC during the next 85 d, and this number correlates with syllable variability. We suggest that new neuron addition and turnover facilitate song change and that this effect lingers when an expected learning event is delayed.

[1]  F. Nottebohm,et al.  Targeted Neuronal Death Affects Neuronal Replacement and Vocal Behavior in Adult Songbirds , 2000, Neuron.

[2]  H. Williams Models for song learning in the zebra finch: fathers or others? , 1990, Animal Behaviour.

[3]  Richard Hans Robert Hahnloser,et al.  Neural Mechanisms of Vocal Sequence Generation in the Songbird , 2004, Annals of the New York Academy of Sciences.

[4]  F. Nottebohm,et al.  Role of a telencephalic nucleus in the delayed song learning of socially isolated zebra finches. , 1993, Journal of neurobiology.

[5]  H. Williams,et al.  Auditory responses in avian vocal motor neurons: a motor theory for song perception in birds. , 1985, Science.

[6]  Philip H. Price Developmental determinants of structure in zebra finch song. , 1979 .

[7]  Stephanie A. White,et al.  Slow NMDA-EPSCs at synapses critical for song development are not required for song learning in zebra finches , 2000, Nature Neuroscience.

[8]  E. Nordeen,et al.  Early sensory and hormonal experience modulate age-related changes in NR2B mRNA within a forebrain region controlling avian vocal learning. , 2000, Journal of neurobiology.

[9]  K. D. Punta,et al.  An ultra-sparse code underlies the generation of neural sequences in a songbird , 2002 .

[10]  F. Nottebohm,et al.  Neurons generated in the adult brain are recruited into functional circuits. , 1984, Science.

[11]  F. Nottebohm,et al.  For Whom The Bird Sings Context-Dependent Gene Expression , 1998, Neuron.

[12]  L. A. Eales Song learning in zebra finches: some effects of song model availability on what is learnt and when , 1985, Animal Behaviour.

[13]  Fernando Nottebohm,et al.  Experience Affects Recruitment of New Neurons But Not Adult Neuron Number , 2002, The Journal of Neuroscience.

[14]  L. A. Eales Song learning in female-raised zebra finches: another look at the sensitive phase , 1987, Animal Behaviour.

[15]  Androgens and isolation from adult tutors differentially affect the development of songbird neurons critical to vocal plasticity. , 2001, Journal of neurophysiology.

[16]  F. Nottebohm,et al.  Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[17]  F. Nottebohm,et al.  Timing of brain-derived neurotrophic factor exposure affects life expectancy of new neurons. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[18]  R. Mooney,et al.  Androgens modulate NMDA receptor-mediated EPSCs in the zebra finch song system. , 1999, Journal of neurophysiology.

[19]  F. Nottebohm,et al.  Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[20]  F. Nottebohm,et al.  Central control of song in the canary, Serinus canarius , 1976, The Journal of comparative neurology.

[21]  C. Pytte,et al.  Vocal Control Neuron Incorporation Decreases with Age in the Adult Zebra Finch , 2002, The Journal of Neuroscience.

[22]  J. Hinds,et al.  Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. , 1977, Science.

[23]  Jörg Böhner,et al.  Early acquisition of song in the zebra finch, Taeniopygia guttata , 1990, Animal Behaviour.

[24]  F. Nottebohm,et al.  Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[25]  F. Nottebohm Neuronal Replacement in Adulthood , 1985, Annals of the New York Academy of Sciences.

[26]  A. C. Yu,et al.  Temporal Hierarchical Control of Singing in Birds , 1996, Science.

[27]  M S Brainard,et al.  Postlearning Consolidation of Birdsong: Stabilizing Effects of Age and Anterior Forebrain Lesions , 2001, The Journal of Neuroscience.

[28]  E.C.L. Vu,et al.  Identification of a forebrain motor programming network for the learned song of zebra finches , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  F. Nottebohm,et al.  A relationship between behavior, neurotrophin expression, and new neuron survival. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  F. Nottebohm,et al.  Dynamics of the Vocal Imitation Process: How a Zebra Finch Learns Its Song , 2001, Science.

[31]  Aaron S. Andalman,et al.  Vocal Experimentation in the Juvenile Songbird Requires a Basal Ganglia Circuit , 2005, PLoS biology.

[32]  F. Nottebohm,et al.  Social change affects the survival of new neurons in the forebrain of adult songbirds , 2002, Behavioural Brain Research.

[33]  Christopher Gregg,et al.  Pregnancy-Stimulated Neurogenesis in the Adult Female Forebrain Mediated by Prolactin , 2003, Science.

[34]  F. Nottebohm,et al.  Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[35]  J. Altman,et al.  Are New Neurons Formed in the Brains of Adult Mammals? , 1962, Science.

[36]  F. Nottebohm,et al.  Birth of projection neurons in the higher vocal center of the canary forebrain before, during, and after song learning. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[37]  F. Nottebohm,et al.  Production and survival of projection neurons in a forebrain vocal center of adult male canaries , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  F. Nottebohm,et al.  Gonads and Singing Play Separate, Additive Roles in New Neuron Recruitment in Adult Canary Brain , 2002, The Journal of Neuroscience.

[39]  E. Nordeen,et al.  NR2B downregulation in a forebrain region required for avian vocal learning is not sufficient to close the sensitive period for song learning , 2003, Neurobiology of Learning and Memory.

[40]  R W Guillery,et al.  Quantification without pontification: Choosing a method for counting objects in sectioned tissues , 1997, The Journal of comparative neurology.

[41]  S. Goldman,et al.  Hu protein as an early marker of neuronal phenotypic differentiation by subependymal zone cells of the adult songbird forebrain. , 1995, Journal of neurobiology.

[42]  F. Nottebohm,et al.  Fate of new neurons in adult canary high vocal center during the first 30 days after their formation , 1999, The Journal of comparative neurology.

[43]  Jessica A. Cardin,et al.  Sensorimotor nucleus NIf is necessary for auditory processing but not vocal motor output in the avian song system. , 2005, Journal of neurophysiology.

[44]  F. Nottebohm,et al.  Direct evidence for loss and replacement of projection neurons in adult canary brain , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  F. Nottebohm,et al.  A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  F. Gage,et al.  Functional neurogenesis in the adult hippocampus , 2002, Nature.

[47]  E. Nordeen,et al.  Projection neurons within a vocal motor pathway are born during song learning in zebra finches , 1988, Nature.

[48]  A. Doupe,et al.  Contributions of an avian basal ganglia–forebrain circuit to real-time modulation of song , 2005, Nature.

[49]  C. E. Ho,et al.  A procedure for an automated measurement of song similarity , 2000, Animal Behaviour.

[50]  K. Immelmann Song development in the zebra finch and other estrildid finches , 1969 .

[51]  E. Gould,et al.  Learning enhances adult neurogenesis in the hippocampal formation , 1999, Nature Neuroscience.