Vocal learning beyond imitation: mechanisms of adaptive vocal development in songbirds and human infants

Studies of vocal learning in songbirds typically focus on the acquisition of sensory templates for song imitation and on the consequent process of matching song production to templates. However, functional vocal development also requires the capacity to adaptively diverge from sensory templates, and to flexibly assemble vocal units. Examples of adaptive divergence include the corrective imitation of abnormal songs, and the decreased tendency to copy over-abundant syllables. Such frequency-dependent effects might mirror tradeoffs between the assimilation of group identity (culture) while establishing individual and flexibly expressive songs. Intriguingly, although the requirements for vocal plasticity vary across songbirds, and more so between birdsong and language, the capacity to flexibly assemble vocal sounds develops in a similar, stepwise manner across species. Therefore, universal features of vocal learning go well beyond the capacity to imitate.

[1]  M. Fee,et al.  Changes in the neural control of a complex motor sequence during learning. , 2011, Journal of neurophysiology.

[2]  Manfred Gahr,et al.  Horizontal transmission of the father's song in the zebra finch (Taeniopygia guttata) , 2013, Biology Letters.

[3]  P. Mitra,et al.  How sleep affects the developmental learning of bird song , 2005, Nature.

[4]  Bence P. Ölveczky,et al.  Motor circuits are required to encode a sensory model for imitative learning , 2012, Nature Neuroscience.

[5]  W. Thorpe Learning and instinct in animals , 1956 .

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

[7]  M. Fee,et al.  Two Distinct Modes of Forebrain Circuit Dynamics Underlie Temporal Patterning in the Vocalizations of Young Songbirds , 2011, The Journal of Neuroscience.

[8]  M. Goldstein,et al.  Social Feedback to Infants' Babbling Facilitates Rapid Phonological Learning , 2008, Psychological science.

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

[10]  S F Volman,et al.  Convergence of untutored song in group-reared zebra finches (Taeniopygia guttata). , 1995, Journal of comparative psychology.

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

[12]  John A. Allen,et al.  Frequency dependent selection: homage to E. B. Poulton , 1984 .

[13]  R N Aslin,et al.  Statistical Learning by 8-Month-Old Infants , 1996, Science.

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

[15]  A. Leonardo,et al.  Ensemble Coding of Vocal Control in Birdsong , 2005, The Journal of Neuroscience.

[16]  D. Oller,et al.  Infant babbling and speech , 1976, Journal of Child Language.

[17]  P. Marler A comparative approach to vocal learning: Song development in white-crowned sparrows. , 1970 .

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

[19]  O Tchernichovski,et al.  Vocal imitation in zebra finches is inversely related to model abundance. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[20]  A. Arnold,et al.  Sexual dimorphism in vocal control areas of the songbird brain. , 1976, Science.

[21]  Todd W Troyer,et al.  Development of temporal structure in zebra finch song. , 2013, Journal of neurophysiology.

[22]  D Margoliash,et al.  Behavioral state modulation of auditory activity in a vocal motor system. , 1998, Science.

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

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

[25]  M. Brainard,et al.  Performance variability enables adaptive plasticity of ‘crystallized’ adult birdsong , 2007, Nature.

[26]  D. Oller The emergence of the speech capacity , 2000 .

[27]  Constance Scharff,et al.  Diminished FoxP2 Levels Affect Dopaminergic Modulation of Corticostriatal Signaling Important to Song Variability , 2013, Neuron.

[28]  Michale S Fee,et al.  The songbird as a model for the generation and learning of complex sequential behaviors. , 2010, ILAR journal.

[29]  S. Kirby,et al.  Language evolution in the laboratory , 2010, Trends in Cognitive Sciences.

[30]  P. Marler,et al.  Song "Dialects" in Three Populations of White-Crowned Sparrows , 1962 .

[31]  R. Mooney,et al.  The role of auditory feedback in vocal learning and maintenance , 2012, Current Opinion in Neurobiology.

[32]  Allison J. Doupe,et al.  Behavioral and Neural Signatures of Readiness to Initiate a Learned Motor Sequence , 2013, Current Biology.

[33]  E. Newport,et al.  When learners surpass their models: The acquisition of American Sign Language from inconsistent input , 2004, Cognitive Psychology.

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

[35]  J. Shonkoff,et al.  Development of infants with disabilities and their families: implications for theory and service delivery. , 1992, Monographs of the Society for Research in Child Development.

[36]  Gary F. Marcus,et al.  Stepwise acquisition of vocal combinatorial capacity in songbirds and human infants , 2013, Nature.

[37]  L. Parra,et al.  Vocal Exploration Is Locally Regulated during Song Learning , 2012, The Journal of Neuroscience.

[38]  Tara McAllister Byun,et al.  Bidirectional perception–production relations in phonological development: evidence from positional neutralization , 2012, Clinical linguistics & phonetics.

[39]  P. Mitra,et al.  De novo establishment of wild-type song culture in the zebra finch , 2009, Nature.

[40]  S. Peters,et al.  Calibration of song learning targets during vocal ontogeny in swamp sparrows, Melospiza georgiana , 2004, Animal Behaviour.

[41]  Partha Niyogi,et al.  Book Reviews: The Computational Nature of Language Learning and Evolution, by Partha Niyogi , 2007, CL.

[42]  O Tchernichovski,et al.  Social inhibition of song imitation among sibling male zebra finches. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Yoram Burak,et al.  The Basal Ganglia Is Necessary for Learning Spectral, but Not Temporal, Features of Birdsong , 2013, Neuron.

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

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

[46]  Partha P. Mitra,et al.  A Technique for Characterizing the Development of Rhythms in Bird Song , 2008, PLoS ONE.

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

[48]  C. ten Cate,et al.  Early experience and plasticity of song in adult male zebra finches (Taeniopygia guttata) , 1996 .

[49]  Steve Horvath,et al.  Molecular Microcircuitry Underlies Functional Specification in a Basal Ganglia Circuit Dedicated to Vocal Learning , 2012, Neuron.

[50]  S Pinker,et al.  Overregularization in language acquisition. , 1992, Monographs of the Society for Research in Child Development.