A Bird's Eye View of Neural Circuit Formation This Review Comes from a Themed Issue on Developmental Neuroscience Edited Quick Tour of the Song Circuit and Its Development Behavioral Outline of Song Development

Neural circuits underlying complex learned behaviors, such as speech in humans, develop under genetic constraints and in response to environmental influences. Little is known about the rules and mechanisms through which such circuits form. We argue that songbirds, with their discrete and well studied neural pathways underlying a complex and naturally learned behavior, provide a powerful model for addressing these questions. We briefly review current knowledge of how the song circuit develops during learning and discuss new possibilities for advancing the field given recent technological advances.

[1]  Masakazu Konishi,et al.  New brain pathways found in the vocal control system of a songbird , 2010, The Journal of comparative neurology.

[2]  Richard Mooney,et al.  Neural mechanisms for learned birdsong. , 2009, Learning & memory.

[3]  Frank Johnson,et al.  Neurotrophins Suppress Apoptosis Induced by Deafferentation of an Avian Motor-Cortical Region , 1997, The Journal of Neuroscience.

[4]  Lei Liu,et al.  The Songbird Neurogenomics (SoNG) Initiative: Community-based tools and strategies for study of brain gene function and evolution , 2008, BMC Genomics.

[5]  F. Nottebohm,et al.  Transgenic songbirds offer an opportunity to develop a genetic model for vocal learning , 2009, Proceedings of the National Academy of Sciences.

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

[7]  A. Arnold,et al.  Neural, not gonadal, origin of brain sex differences in a gynandromorphic finch , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  S. Goldman,et al.  Brain-Derived Neurotrophic Factor Signaling in the HVC Is Required for Testosterone-Induced Song of Female Canaries , 2009, The Journal of Neuroscience.

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

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

[11]  S. Bottjer.  Developmental Regulation of Basal Ganglia Circuitry during the Sensitive Period for Vocal Learning in Songbirds , 2004, Annals of the New York Academy of Sciences.

[12]  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.

[13]  Richard Mooney,et al.  Acute injections of brain-derived neurotrophic factor in a vocal premotor nucleus reversibly disrupt adult birdsong stability and trigger syllable deletion. , 2005, Journal of neurobiology.

[14]  David R. Ladle,et al.  Assembly of Motor Circuits in the Spinal Cord: Driven to Function by Genetic and Experience-Dependent Mechanisms , 2007, Neuron.

[15]  Richard Hans Robert Hahnloser,et al.  An ultra-sparse code underliesthe generation of neural sequences in a songbird , 2002, Nature.

[16]  S. Bottjer,et al.  Afferent influences on cell death and birth during development of a cortical nucleus necessary for learned vocal behavior in zebra finches. , 1994, Development.

[17]  Christoph Schmitz,et al.  The Developmental Neurobiology of Autism Spectrum Disorder , 2006, The Journal of Neuroscience.

[18]  A. Arnold,et al.  Ontogeny of brain nuclei controlling song learning and behavior in zebra finches , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  Allison J. Doupe,et al.  Neurons in a Forebrain Nucleus Required for Vocal Plasticity Rapidly Switch between Precise Firing and Variable Bursting Depending on Social Context , 2008, The Journal of Neuroscience.

[20]  David A Lewis,et al.  Schizophrenia as a disorder of neurodevelopment. , 2002, Annual review of neuroscience.

[21]  H. Seung,et al.  Model of birdsong learning based on gradient estimation by dynamic perturbation of neural conductances. , 2007, Journal of neurophysiology.

[22]  A. Arnold,et al.  The development of afferent projections to the robust archistriatal nucleus in male zebra finches: a quantitative electron microscopic study , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[24]  F. Nottebohm,et al.  Site-Specific Retinoic Acid Production in the Brain of Adult Songbirds , 2000, Neuron.

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

[26]  R. Mooney,et al.  Lesions of an Avian Forebrain Nucleus That Disrupt Song Development Alter Synaptic Connectivity and Transmission in the Vocal Premotor Pathway , 1999, The Journal of Neuroscience.

[27]  T. Hensch,et al.  Early GABA function regulates sensory critical period during birdsong learning , 2007, Neuroscience Research.

[28]  Marcelo O Magnasco,et al.  Sparse time-frequency representations , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[29]  A. Sinclair,et al.  Robust and ubiquitous GFP expression in a single generation of chicken embryos using the avian retroviral vector, RCASBP. , 2009, Differentiation; research in biological diversity.

[30]  Masakazu Konishi,et al.  Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain , 1985, Nature.

[31]  C. Scharff,et al.  Knockdown of FoxP2 alters spine density in Area X of the zebra finch , 2010, Genes, brain, and behavior.

[32]  E. Nordeen,et al.  Neuron loss and addition in developing zebra finch song nuclei are independent of auditory experience during song learning. , 1991, Journal of neurobiology.

[33]  T. Hensch.  Critical period regulation. , 2004, Annual review of neuroscience.

[34]  Richard Mooney,et al.  Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning , 2010, Nature.

[35]  Richard H. R. Hahnloser,et al.  erratum: An ultra-sparse code underlies the generation of neural sequences in a songbird , 2003, Nature.

[36]  R. Mooney,et al.  Waiting periods versus early innervation: the development of axonal connections in the zebra finch song system , 1994, Journal of Neuroscience.

[37]  Ila R Fiete,et al.  Gradient learning in spiking neural networks by dynamic perturbation of conductances. , 2006, Physical review letters.

[38]  P. Kuhl,et al.  Birdsong and human speech: common themes and mechanisms. , 1999, Annual review of neuroscience.

[39]  S. Bottjer,et al.  The Role of Auditory Experience in the Formation of Neural Circuits Underlying Vocal Learning in Zebra Finches , 2002, The Journal of Neuroscience.

[40]  A. Monaco,et al.  A forkhead-domain gene is mutated in a severe speech and language disorder , 2001, Nature.

[41]  B. Southey,et al.  Discrete molecular states in the brain accompany changing responses to a vocal signal , 2009, Proceedings of the National Academy of Sciences.

[42]  Stephen J. Smith,et al.  Neural activity and the dynamics of central nervous system development , 2004, Nature Neuroscience.

[43]  S. Bottjer,et al.  Development of Topography within Song Control Circuitry of Zebra Finches during the Sensitive Period for Song Learning , 1999, The Journal of Neuroscience.

[44]  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.

[45]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[46]  Joseph K Jun,et al.  Development of Neural Circuitry for Precise Temporal Sequences through Spontaneous Activity, Axon Remodeling, and Synaptic Plasticity , 2007, PloS one.

[47]  Andreas Kotowicz,et al.  Auditory representations and memory in birdsong learning , 2010, Current Opinion in Neurobiology.

[48]  Felix Naef,et al.  Freedom and Rules: The Acquisition and Reprogramming of a Bird's Learned Song , 2005, Science.

[49]  F. Johnson,et al.  Reorganization of a telencephalic motor region during sexual differentiation and vocal learning in zebra finches. , 2000, Brain research. Developmental brain research.

[50]  Michale S Fee,et al.  A basal ganglia-forebrain circuit in the songbird biases motor output to avoid vocal errors , 2009, Proceedings of the National Academy of Sciences.

[51]  Richard Hans Robert Hahnloser,et al.  Spike-Time-Dependent Plasticity and Heterosynaptic Competition Organize Networks to Produce Long Scale-Free Sequences of Neural Activity , 2010, Neuron.

[52]  E. Nordeen,et al.  Song tutoring triggers CaMKII phosphorylation within a specialized portion of the avian basal ganglia. , 2005, Journal of neurobiology.

[53]  Michale S Fee,et al.  A Specialized Forebrain Circuit for Vocal Babbling in the Juvenile Songbird , 2008, Science.

[54]  A. Doupe.  Song- and Order-Selective Neurons in the Songbird Anterior Forebrain and their Emergence during Vocal Development , 1997, The Journal of Neuroscience.

[55]  C. Mello,et al.  Dietary retinoic acid affects song maturation and gene expression in the song system of the zebra finch , 2008, Developmental neurobiology.

[56]  O. Kiehn.  Development and functional organization of spinal locomotor circuits , 2011, Current Opinion in Neurobiology.

[57]  JR Kirn,et al.  Genesis and death of vocal control neurons during sexual differentiation in the zebra finch , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  Sarah E. London,et al.  Integrating Genomes, Brain and Behavior in the Study of Songbirds , 2009, Current Biology.

[59]  Ning Tian,et al.  Synaptic activity, visual experience and the maturation of retinal synaptic circuitry , 2008, The Journal of physiology.

[60]  Daniel Margoliash,et al.  Sleep and sensorimotor integration during early vocal learning in a songbird , 2008, Nature.

[61]  Mriganka Sur,et al.  Motility of dendritic spines in visual cortex in vivo: Changes during the critical period and effects of visual deprivation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[62]  E. Nordeen,et al.  Sex-dependent loss of projection neurons involved in avian song learning. , 1992, Journal of neurobiology.

[63]  Claudio V. Mello,et al.  Birdsong “Transcriptomics”: Neurochemical Specializations of the Oscine Song System , 2008, PloS one.

[64]  Timothy Q Gentner,et al.  Brain stem feedback in a computational model of birdsong sequencing. , 2009, Journal of neurophysiology.

[65]  Albert J. Vilella,et al.  The genome of a songbird , 2010, Nature.

[66]  C. Scharff,et al.  Incomplete and Inaccurate Vocal Imitation after Knockdown of FoxP2 in Songbird Basal Ganglia Nucleus Area X , 2007, PLoS biology.

[67]  P. Marler,et al.  Neuroscience of Birdsong , 2012 .

[68]  J. Han,et al.  Generation of transgenic quail through germ cell‐mediated germline transmission , 2008, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.