From perception to action in songbird production: dynamics of a whole loop.

Birdsong emerges when a set of highly interconnected brain areas manage to generate a complex output. This consists of precise respiratory rhythms as well as motor instructions to control the vocal organ configuration. In this way, during birdsong production, dedicated cortical areas interact with life-supporting ones in the brainstem, such as the respiratory nuclei. We discuss an integrative view of this interaction together with a widely accepted "top-down" representation of the song system. We also show that a description of this neural network in terms of dynamical systems allows to explore songbird production and processing by generating testable predictions.

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

[2]  R. Suthers Contributions to birdsong from the left and right sides of the intact syrinx , 1990, Nature.

[3]  J. F. Prather,et al.  Precise auditory–vocal mirroring in neurons for learned vocal communication , 2008, Nature.

[4]  J Martin Wild,et al.  Functional Neuroanatomy of the Sensorimotor Control of Singing , 2004, Annals of the New York Academy of Sciences.

[5]  F. Goller,et al.  Role of syringeal muscles in gating airflow and sound production in singing brown thrashers. , 1996, Journal of neurophysiology.

[6]  Franz Goller,et al.  A circular model for song motor control in Serinus canaria , 2015, Front. Comput. Neurosci..

[7]  Robin C. Ashmore,et al.  Bottom-Up Activation of the Vocal Motor Forebrain by the Respiratory Brainstem , 2008, The Journal of Neuroscience.

[8]  Franz Goller,et al.  Nonlinear model predicts diverse respiratory patterns of birdsong. , 2006, Physical review letters.

[9]  D. Margoliash,et al.  Song replay during sleep and computational rules for sensorimotor vocal learning. , 2000, Science.

[10]  A. Doupe,et al.  Song-selective auditory circuits in the vocal control system of the zebra finch. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[11]  F Goller,et al.  Role of syringeal muscles in controlling the phonology of bird song. , 1996, Journal of neurophysiology.

[12]  R. Mooney Different Subthreshold Mechanisms Underlie Song Selectivity in Identified HVc Neurons of the Zebra Finch , 2000, The Journal of Neuroscience.

[13]  Franz Goller,et al.  Hormonal acceleration of song development illuminates motor control mechanism in canaries , 2010, Developmental neurobiology.

[14]  A. Doupe,et al.  Compromised Neural Selectivity for Song in Birds with Impaired Sensorimotor Learning , 2000, Neuron.

[15]  Yonatan Sanz Perl,et al.  Elemental gesture dynamics are encoded by song premotor cortical neurons , 2013, Nature.

[16]  Marc F. Schmidt,et al.  Pattern of interhemispheric synchronization in HVc during singing correlates with key transitions in the song pattern. , 2003, Journal of neurophysiology.

[17]  Yonatan Sanz Perl,et al.  Reconstruction of physiological instructions from Zebra finch song. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[18]  D Margoliash,et al.  Preference for autogenous song by auditory neurons in a song system nucleus of the white-crowned sparrow , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  E. Izhikevich,et al.  Weakly connected neural networks , 1997 .

[20]  H. Williams,et al.  Temporal patterning of song production: participation of nucleus uvaeformis of the thalamus. , 1993, Journal of neurobiology.

[21]  Richard Mooney,et al.  Auditory Plasticity in a Basal Ganglia–Forebrain Pathway during Decrystallization of Adult Birdsong , 2007, The Journal of Neuroscience.

[22]  M. Fee,et al.  Using temperature to analyze temporal dynamics in the songbird motor pathway , 2008, Nature.

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

[24]  Masakazu Konishi,et al.  Neural auditory selectivity develops in parallel with song. , 2005, Journal of neurobiology.

[25]  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.

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

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

[28]  A. Doupe,et al.  Contributions of Tutor and Bird’s Own Song Experience to Neural Selectivity in the Songbird Anterior Forebrain , 1999, The Journal of Neuroscience.

[29]  F Goller,et al.  Low-dimensional dynamical model for the diversity of pressure patterns used in canary song. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[30]  A. Doupe,et al.  Translating birdsong: songbirds as a model for basic and applied medical research. , 2013, Annual review of neuroscience.

[31]  Robin C. Ashmore,et al.  Brainstem and Forebrain Contributions to the Generation of Learned Motor Behaviors for Song , 2005, The Journal of Neuroscience.

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

[33]  Franz Goller,et al.  Implications for lateralization of bird song from unilateral gating of bilateral motor patterns , 1995, Nature.

[34]  Kosuke Hamaguchi,et al.  A Distributed Recurrent Network Contributes to Temporally Precise Vocalizations , 2016, Neuron.

[35]  J. S. McCasland,et al.  Interaction between auditory and motor activities in an avian song control nucleus. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Marc F. Schmidt,et al.  The respiratory-vocal system of songbirds: anatomy, physiology, and neural control. , 2014, Progress in brain research.

[37]  A. Doupe,et al.  Anterior Forebrain Neurons Develop Selectivity by an Intermediate Stage of Birdsong Learning , 1997, The Journal of Neuroscience.

[38]  Richard H R Hahnloser,et al.  Spikes and Bursts in Two Types of Thalamic Projection Neurons Differentially Shape Sleep Patterns and Auditory Responses in a Songbird , 2008, The Journal of Neuroscience.

[39]  Franz Goller,et al.  Temperature Induced Syllable Breaking Unveils Nonlinearly Interacting Timescales in Birdsong Motor Pathway , 2013, PloS one.

[40]  Franz Goller,et al.  Breathtaking Songs: Coordinating the Neural Circuits for Breathing and Singing. , 2016, Physiology.

[41]  Franz Goller,et al.  Peripheral Motor Dynamics of Song Production in the Zebra Finch , 2004, Annals of the New York Academy of Sciences.

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

[43]  G. Mindlin,et al.  An integrated model for motor control of song in Serinus canaria , 2016, Journal of Physiology-Paris.

[44]  R. Mooney Auditory–vocal mirroring in songbirds , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[45]  Gabriel B. Mindlin,et al.  Low dimensional dynamics in birdsong production , 2014 .

[46]  M. Coleman,et al.  Recovery of impaired songs following unilateral but not bilateral lesions of nucleus uvaeformis of adult zebra finches. , 2005, Journal of neurobiology.

[47]  Gabriel B Mindlin,et al.  Average activity of excitatory and inhibitory neural populations. , 2016, Chaos.

[48]  F Goller,et al.  The neuromuscular control of birdsong. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.