Toward a Song Code Evidence for a Syllabic Representation in the Canary Brain

We show that presentation of individual canary song syllables results in distinct expression patterns of the immediate-early gene ZENK in the caudomedial neostriatum (NCM) of adult canaries. Information on the spatial distribution and labeling of stained cells provides for a classification of ZENK patterns that (1) accords to the organization of stimuli into families, (2) preserves the stimuli intrafamily relationships, and (3) confers salience to natural over artificial stimuli, resulting in a nonclassical tonotopic map. Moreover, complex syllable maps cannot be reduced to any linear combinations of simple syllable maps. These properties arise from the collective response of NCM neurons to auditory stimuli, rather than from the behavior of single neurons. The syllabic representation described here may constitute an important step toward deciphering the rules of birdsong auditory representation.

[1]  A. Chaudhuri,et al.  Neural activity mapping with inducible transcription factors. , 1997, Neuroreport.

[2]  G. Langner,et al.  Topographic representation of periodicities in the forebrain of the mynah bird: one map for pitch and rhythm? , 1987, Brain Research.

[3]  B J Richmond,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. II. Quantification of response waveform. , 1987, Journal of neurophysiology.

[4]  D. Kroodsma,et al.  Ecology and evolution of acoustic communication in birds , 1997 .

[5]  G D Lewen,et al.  Reproducibility and Variability in Neural Spike Trains , 1997, Science.

[6]  H. Scheich,et al.  Functional organization of the avian auditory cortex analogue. I. Topographic representation of isointensity bandwidth , 1991, Brain Research.

[7]  R. Godard.  Long-term memory of individual neighbours in a migratory songbird , 1991, Nature.

[8]  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.

[9]  Fernando Nottebohm,et al.  The Origins of Vocal Learning , 1972, The American Naturalist.

[10]  Sidarta Ribeiro,et al.  ZENK protein regulation by song in the brain of songbirds , 1998, The Journal of comparative neurology.

[11]  D Margoliash,et al.  Functional organization of forebrain pathways for song production and perception. , 1997, Journal of neurobiology.

[12]  Henning Scheich,et al.  Auditory cortex: comparative aspects of maps and plasticity , 1991, Current Opinion in Neurobiology.

[13]  D. Margoliash,et al.  Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  C. Mello,et al.  Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  Björn Capsius,et al.  Influence of urethane anesthesia on neural processing in the auditory cortex analogue of a songbird , 1996, Hearing Research.

[16]  Eileen D. Adamson,et al.  A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization , 1988, Cell.

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

[18]  L. Optican,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. III. Information theoretic analysis. , 1987, Journal of neurophysiology.

[19]  M. Kreutzer,et al.  SYLLABLE PHONOLOGY AND SONG SEGMENTATION: TESTING THEIR SALIENCE IN FEMALE CANARIES , 1992 .

[20]  J. Milbrandt,et al.  A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. , 1987, Science.

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

[22]  F. Ackerman,et al.  The significance of a wish. , 1991, The Hastings Center report.

[23]  P. Lemaire,et al.  Two mouse genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cells. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[24]  R. Hartley,et al.  Expiratory muscle activity during song production in the canary. , 1990, Respiration physiology.

[25]  S J Chew,et al.  A large-capacity memory system that recognizes the calls and songs of individual birds. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[26]  D. Vicario,et al.  Song presentation induces gene expression in the songbird forebrain. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[27]  M. Nicolelis,et al.  Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. , 1995, Science.

[28]  F. Nottebohm,et al.  Motor-driven gene expression. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Andrew J. Cole,et al.  Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation , 1989, Nature.

[30]  R. F. Thompson,et al.  The search for the engram. , 1976, The American psychologist.

[31]  H. Güttinger,et al.  Consequences of domestication on the song structures in the canary , 1985 .

[32]  A. Goldsmith,et al.  Inverse changes in plasma prolactin and LH concentrations in female canaries after disruption and reinitiation of incubation. , 1984, The Journal of endocrinology.

[33]  P. Mundinger.  Behaviour-genetic analysis of canary song: inter-strain differences in sensory learning, and epigenetic rules , 1995, Animal Behaviour.

[34]  R. Menzel,et al.  Representations of odours and odour mixtures visualized in the honeybee brain , 1997, Nature.

[35]  P. Marler,et al.  Sparrows Learn Adult Song and More from Memory , 1981, Science.

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

[37]  G. Wang,et al.  Induction of the , 1996 .

[38]  R. Reale,et al.  Tonotopic organization in auditory cortex of the cat , 1980, The Journal of comparative neurology.

[39]  C. Gross,et al.  Representation of visual stimuli in inferior temporal cortex. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  A. Treves,et al.  The representational capacity of the distributed encoding of information provided by populations of neurons in primate temporal visual cortex , 1997, Experimental Brain Research.

[41]  Claude E. Shannon,et al.  The mathematical theory of communication , 1950 .

[42]  Roy Stripling,et al.  Response Modulation in the Zebra Finch Neostriatum: Relationship to Nuclear Gene Regulation , 1997, The Journal of Neuroscience.

[43]  H. Scheich,et al.  2-deoxyglucose accumulation parallels extracellularly recorded spike activity in the avian auditory neostriatum , 1984, Brain Research.

[44]  F. Nottebohm,et al.  Repeated exposure to one song leads to a rapid and persistent decline in an immediate early gene's response to that song in zebra finch telencephalon , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  M. Magnasco,et al.  An automated system for the mapping and quantitative analysis of immunocytochemistry of an inducible nuclear protein , 1999, Journal of Neuroscience Methods.

[46]  J. Wingfield,et al.  Plasma levels of prolactin and gonadal steroids in relation to multiple-brooding and renesting in free-living populations of the song sparrow, Melospiza melodia , 1990, Hormones and Behavior.

[47]  M. Dragunow.  A role for immediate-early transcription factors in learning and memory , 1996, Behavior genetics.

[48]  L. Brillouin.  Life, thermodynamics, and cybernetics. , 1949, American scientist.

[49]  F. Nottebohm,et al.  Quantal Duration of Auditory Memories , 1996, Science.

[50]  M. Kreutzer,et al.  Female canaries are sexually responsive to special song phrases , 1995, Animal Behaviour.

[51]  R. Hampson,et al.  The significance of neural ensemble codes during behavior and cognition. , 1997, Annual review of neuroscience.

[52]  Gregory F Ball,et al.  Induction of the Zenk protein after sexual interactions in male Japanese quail , 1997, Neuroreport.

[53]  Atsuyuki Okabe,et al.  Spatial Tessellations: Concepts and Applications of Voronoi Diagrams , 1992, Wiley Series in Probability and Mathematical Statistics.

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

[55]  Shihab A. Shamma,et al.  Auditory cortex , 1998 .

[56]  I. Weiler,et al.  Correspondence between sites of NGFI-A induction and sites of morphological plasticity following exposure to environmental complexity. , 1995, Brain research. Molecular brain research.

[57]  M. Stryker,et al.  Development of Orientation Preference Maps in Ferret Primary Visual Cortex , 1996, The Journal of Neuroscience.

[58]  L. Lau,et al.  A gene activated in mouse 3T3 cells by serum growth factors encodes a protein with "zinc finger" sequences. , 1988, Proceedings of the National Academy of Sciences of the United States of America.