Doublecortin as a marker of adult neuroplasticity in the canary song control nucleus HVC

It is established that in songbirds the size of several brain song control nuclei varies seasonally, based on changes in cell size, dendritic branching and, in nucleus HVC, the incorporation of newborn neurons. In the developing and adult mammalian brain, the protein doublecortin (DCX) is expressed in postmitotic neurons and, as a part of the microtubule machinery, required for neuronal migration. We recently showed that in adult canaries, DCX‐immunoreactive (ir) cells are present throughout the telencephalon, but the link between DCX and the active neurogenesis observed in songbirds remained uncertain. We demonstrate here that DCX labels recently born cells in the canary telencephalon and that, in parallel with changes in HVC volume, the number of DCX‐ir cells is increased specifically in the HVC of testosterone‐treated males compared with castrates, and in castrated testosterone‐treated males paired with a female as compared with males paired with another male. The numbers of elongated DCX‐ir cells (presumptive migrating neurons) and round multipolar DCX‐ir cells (differentiating neurons) were also affected by the sex of the subjects and their photoperiodic condition (photosensitive vs photostimulated vs photorefractory). Thus, in canaries the endocrine state, as well as the social or photoperiodic condition independently of variation in steroid hormone action, affects the number of cells expressing a protein involved in neuronal migration specifically in brain areas that incorporate new neurons in the telencephalon. The DCX gene may be one of the targets by which testosterone and social stimuli induce seasonal changes in the volume of song nuclei.

[1]  M. Chopp,et al.  Neuroblast Division during Migration toward the Ischemic Striatum: A Study of Dynamic Migratory and Proliferative Characteristics of Neuroblasts from the Subventricular Zone , 2007, The Journal of Neuroscience.

[2]  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.

[3]  G. Ball,et al.  Testis-dependent and -independent effects of photoperiod on volumes of song control nuclei in American tree sparrows (Spizella arborea) , 1997, Brain Research.

[4]  Jacques Balthazart,et al.  Neuroendocrinology of Song Behavior and Avian Brain Plasticity: Multiple Sites of Action of Sex Steroid Hormones , 2002, Frontiers in Neuroendocrinology.

[5]  Gregory F Ball,et al.  Seasonal neuroplasticity in the songbird telencephalon: a role for melatonin. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Tobias Plümpe,et al.  Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation , 2006, BMC Neuroscience.

[7]  Gregory F Ball,et al.  Song activation by testosterone is associated with an increased catecholaminergic innervation of the song control system in female canaries , 2003, Neuroscience.

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

[9]  P. Deviche,et al.  Vocal control region sizes of an adult female songbird change seasonally in the absence of detectable circulating testosterone concentrations. , 2000, Journal of neurobiology.

[10]  G. Ball,et al.  The microtubule-associated protein doublecortin is broadly expressed in the telencephalon of adult canaries , 2007, Journal of Chemical Neuroanatomy.

[11]  A. Capes-Davis,et al.  Expression of doublecortin (DCX) and doublecortin‐like kinase (DCLK) within the developing chick brain , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[12]  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.

[13]  M. Gahr,et al.  Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds , 1999, The Journal of comparative neurology.

[14]  Jacques Balthazart,et al.  Seasonal Plasticity in the Song Control System: Multiple Brain Sites of Steroid Hormone Action and the Importance of Variation in Song Behavior , 2004, Annals of the New York Academy of Sciences.

[15]  A. Álvarez-Buylla,et al.  Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. , 1997, Journal of neurobiology.

[16]  G. Ball,et al.  Coordinated and dissociated effects of testosterone on singing behavior and song control nuclei in canaries (Serinus canaria) , 2005, Hormones and Behavior.

[17]  S. Bottjer,et al.  Connections of a motor cortical region in zebra finches: Relation to pathways for vocal learning , 2000, The Journal of comparative neurology.

[18]  J. Gleeson,et al.  Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain , 2006, Nature Neuroscience.

[19]  Jürgen Winkler,et al.  Transient expression of doublecortin during adult neurogenesis , 2003, The Journal of comparative neurology.

[20]  M. Frotscher,et al.  Balance between Neurogenesis and Gliogenesis in the Adult Hippocampus: Role for Reelin , 2006, Developmental Neuroscience.

[21]  J. Wingfield,et al.  Seasonal changes in gonadal hormone levels of adult male canaries and their relation to song. , 1987, Behavioral and neural biology.

[22]  P. Slater,et al.  Bird Song: Biological Themes and Variations , 1995 .

[23]  Jürgen Winkler,et al.  Doublecortin expression levels in adult brain reflect neurogenesis , 2005, The European journal of neuroscience.

[24]  G. E. Vates,et al.  Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taenopygia guttata) , 1996, The Journal of comparative neurology.

[25]  H. Karten,et al.  A stereotaxic atlas of the brain of the pigeon (Columba livia) , 1967 .

[26]  F. Nottebohm,et al.  Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. , 1990, Science.

[27]  Eliot A. Brenowitz,et al.  Contributions of Social Cues and Photoperiod to Seasonal Plasticity in the Adult Avian Song Control System , 1999, The Journal of Neuroscience.

[28]  S. Bottjer,et al.  Neurogenesis within the juvenile zebra finch telencephalic ventricular zone: A map of proliferative activity , 2005, The Journal of comparative neurology.

[29]  Eliot A. Brenowitz,et al.  Seasonal growth of song control nuclei precedes seasonal reproductive development in wild adult song sparrows. , 2001, General and comparative endocrinology.

[30]  Jacques Balthazart,et al.  Androgen Receptor, Estrogen Receptor α, and Estrogen Receptorβ Show Distinct Patterns of Expression in Forebrain Song Control Nuclei of European Starlings1. , 1999, Endocrinology.

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

[32]  C. Walsh,et al.  Doublecortin Is a Microtubule-Associated Protein and Is Expressed Widely by Migrating Neurons , 1999, Neuron.

[33]  Sandra A. Brown,et al.  Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches , 1989, The Journal of comparative neurology.

[34]  A. Arnold,et al.  Forebrain lesions disrupt development but not maintenance of song in passerine birds. , 1984, Science.

[35]  F. Nottebohm A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. , 1981, Science.

[36]  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.

[37]  A. Koulakoff,et al.  Doublecortin functions at the extremities of growing neuronal processes. , 2003, Cerebral cortex.

[38]  D Margoliash,et al.  An introduction to birdsong and the avian song system. , 1997, Journal of neurobiology.

[39]  S. Dloniak,et al.  Effects of Testosterone and Photoperiodic Condition on Song Production and Vocal Control Region Volumes in Adult Male Dark-Eyed Juncos (Junco hyemalis) , 2001, Hormones and Behavior.

[40]  M. Gahr,et al.  Estrogen receptors in the avian brain: Survey reveals general distribution and forebrain areas unique to songbirds , 1993, The Journal of comparative neurology.

[41]  T. Nicholls,et al.  The effect of duration of the daily photoperiod on recovery of photosensitivity in photorefractory canaries (Serinus canarius). , 1977, General and comparative endocrinology.

[42]  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.

[43]  A. Arnold,et al.  The distribution of expression of doublecortin (DCX) mRNA and protein in the zebra finch brain , 2006, Brain Research.

[44]  G. Leboucher,et al.  Copulation-solicitation Displays in Female Canaries (Serinus canaria): are Oestradiol Implants Necessary? , 2010 .

[45]  B. Echenne,et al.  doublecortin is the major gene causing X-linked subcortical laminar heterotopia (SCLH). , 1998, Human molecular genetics.

[46]  Yasuyoshi Watanabe,et al.  Multi‐directional differentiation of doublecortin‐ and NG2‐immunopositive progenitor cells in the adult rat neocortex in vivo , 2007, The European journal of neuroscience.

[47]  A. Shetty,et al.  Efficacy of doublecortin as a marker to analyse the absolute number anddendritic growth of newly generated neurons in the adult dentate gyrus , 2004, The European journal of neuroscience.

[48]  Gerald E. Hough,et al.  Revised nomenclature for avian telencephalon and some related brainstem nuclei , 2004, The Journal of comparative neurology.

[49]  Fernando Nottebohm,et al.  Descending auditory pathways in the adult male zebra finch (Taeniopygia Guttata) , 1998, The Journal of comparative neurology.

[50]  Erich D. Jarvis,et al.  Brains and birdsong , 2004 .

[51]  Eliot A. Brenowitz,et al.  Seasonal plasticity in the adult brain , 2000, Trends in Neurosciences.

[52]  F. Nottebohm,et al.  Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei. , 1986, Behavioral and neural biology.

[53]  C. Ribak,et al.  Spatiotemporal profile of dendritic outgrowth from newly born granule cells in the adult rat dentate gyrus , 2007, Brain Research.

[54]  Fernando Nottebohm,et al.  Testosterone triggers growth of brain vocal control nuclei in adult female canaries , 1980, Brain Research.

[55]  P. Marler,et al.  Nature's Music: The Science of Birdsong , 2004 .

[56]  G. Ball Neuroendocrine basis of seasonal changes in vocal behavior among songbirds , 2000 .

[57]  Michael S. Brainard,et al.  Auditory feedback in learning and maintenance of vocal behaviour , 2000, Nature Reviews Neuroscience.

[58]  R. Ramos,et al.  RNAi reveals doublecortin is required for radial migration in rat neocortex , 2003, Nature Neuroscience.

[59]  P. Deviche,et al.  Photoperiod and testosterone independently affect vocal control region volumes in adolescent male songbirds. , 1998, Journal of neurobiology.

[60]  B. McEwen,et al.  Doublecortin expression in the adult rat telencephalon , 2001, The European journal of neuroscience.

[61]  Eliot A. Brenowitz,et al.  Plasticity of the Adult Avian Song Control System , 2004, Annals of the New York Academy of Sciences.

[62]  Fernando Nottebohm,et al.  Migration of young neurons in adult avian brain , 1988, Nature.

[63]  F. Nottebohm,et al.  The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates , 1974, The Journal of comparative neurology.

[64]  A. Hannan,et al.  Expression of doublecortin correlates with neuronal migration and pattern formation in diverse regions of the developing chick brain , 1999, Journal of neuroscience research.

[65]  C. Mandyam,et al.  Determination of key aspects of precursor cell proliferation, cell cycle length and kinetics in the adult mouse subgranular zone , 2007, Neuroscience.

[66]  H. Williams Birdsong and Singing Behavior , 2004, Annals of the New York Academy of Sciences.

[67]  Gregory F Ball,et al.  Social context affects testosterone-induced singing and the volume of song control nuclei in male canaries (Serinus canaria). , 2006, Journal of neurobiology.

[68]  J. Balthazart,et al.  Simultaneous pituitary–gonadal recrudescence in two Corsican populations of male blue tits with asynchronous breeding dates , 2006, Hormones and Behavior.

[69]  Fernando Nottebohm,et al.  The Neural Basis of Birdsong , 2005, PLoS biology.

[70]  S. Watson,et al.  Estrogen receptor α and β mRNA expressions by proliferating and differentiating cells in the adult rat dentate gyrus and subventricular zone , 2005, Neuroscience.

[71]  S. Mcconnell,et al.  Doublecortin Is a Developmentally Regulated, Microtubule-Associated Protein Expressed in Migrating and Differentiating Neurons , 1999, Neuron.

[72]  F. Nottebohm From bird song to neurogenesis. , 1989, Scientific American.

[73]  Gregory F Ball,et al.  Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings. , 1999, Endocrinology.

[74]  Gregory F Ball,et al.  Immunocytochemical localization of androgen receptors in the male songbird and quail brain , 1992, The Journal of comparative neurology.