New insights into the auditory processing of communicative signals in the HVC of awake songbirds

In the present study, using a systematic recording method and a variety of stimuli, we determined the proportion of responsive sites and their response features in the vocal control nucleus HVC of awake-restrained starlings, a species with multiple song types. Responsive sites were classified into three groups, according to the number of stimuli to which they responded. Sites in the three groups showed responses to individual-specific songs, with sites in the group that showed responses to only one stimulus responding mostly to a bird's own song. In comparison, very few sites exhibited responses to universal species-specific songs and to artificial nonspecific sounds. By contrast, data obtained in the same birds under urethane anesthesia show that, although the total proportion of responsive sites was similar, numerous responses to a universal species-specific song and to an artificial nonspecific pure tone could be observed.

[1]  J. Edeline,et al.  Differences in auditory and physiological properties of HVc neurons between reproductively active male and female canaries (Serinus canaria) , 2001, The European journal of neuroscience.

[2]  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.

[3]  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.

[4]  Isabelle George,et al.  Auditory responses in the HVC of anesthetized starlings , 2005, Brain Research.

[5]  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.

[6]  Bradley C. Wheeler,et al.  Automatic Discrimination of Single Units , 1998 .

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

[8]  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.

[9]  J. Bolhuis,et al.  Localized neuronal activation in the zebra finch brain is related to the strength of song learning. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[11]  M. Gahr,et al.  The selectivity of sexual responses to song displays: effects of partial chemical lesion of the HVC in female canaries , 1998, Behavioural Brain Research.

[12]  F. Nottebohm,et al.  Neural lateralization of vocal control in a passerine bird. I. Song. , 1971, The Journal of experimental zoology.

[13]  D. Margoliash Evaluating theories of bird song learning: implications for future directions , 2002, Journal of Comparative Physiology A.

[14]  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.

[15]  P. F. Jenkins,et al.  Complex organization of the warbling song in the European starling Sturnus vulgaris , 1988 .

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

[17]  Masakazu Konishi,et al.  Gating of auditory responses in the vocal control system of awake songbirds , 1998, Nature Neuroscience.

[18]  R. Mooney,et al.  Auditory representation of the vocal repertoire in a songbird with multiple song types , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[21]  M. Lewicki Intracellular Characterization of Song-Specific Neurons in the Zebra Finch Auditory Forebrain , 1996, The Journal of Neuroscience.

[22]  H. Leppelsack,et al.  Responses of auditory neurons in the forebrain of a songbird to stimulation with species-specific sounds , 2004, Journal of comparative physiology.

[23]  K. Okanoya,et al.  Hearing in the starling (Sturnus vulgaris): absolute thresholds and critical ratios , 1986 .

[24]  Social influences on the whistled songs of starlings , 1982, Behavioral Ecology and Sociobiology.

[25]  D Margoliash,et al.  Global synchronous response to autogenous song in zebra finch HVc. , 1994, Journal of neurophysiology.

[26]  Peter L. Rauske,et al.  State and neuronal class-dependent reconfiguration in the avian song system. , 2003, Journal of neurophysiology.

[27]  Martine Hausberger,et al.  Neuronal bases of categorization in starling song , 2000, Behavioural Brain Research.

[28]  M. Kirsch,et al.  Unit recordings from a new auditory area in the frontal neostriatum of the awake starling (Sturnus vulgaris) , 2004, Experimental Brain Research.

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

[30]  Peter Marler,et al.  Song acquisition in European starlings, Sturnus vulgaris: a comparison of the songs of live-tutored, tape-tutored, untutored, and wild-caught males , 1993, Animal Behaviour.

[31]  L. C. Katz,et al.  Auditory responses in the zebra finch's motor system for song , 1981, Brain Research.

[32]  Björn Capsius,et al.  Response patterns and their relationship to frequency analysis in auditory forebrain centers of a songbird , 1999, Hearing Research.

[33]  Social influences on vocal development: Social influences on song acquisition and sharing in the European starling ( Sturnus vulgaris ) , 1997 .

[34]  M. Hausberger,et al.  A new extensive approach to single unit responses using multisite recording electrodes: application to the songbird brain , 2003, Journal of Neuroscience Methods.

[35]  Charles T. Snowdon,et al.  Social Influences on Vocal Development , 2005 .

[36]  M. Schmidt,et al.  Comparative approaches to avian song system function: insights into auditory and motor processing , 2002, Journal of Comparative Physiology A.

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

[38]  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.

[39]  J. S. McCasland,et al.  Neuronal control of bird song production , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  Martine Hausberger,et al.  Song sharing reflects the social organization in a captive group of European starlings (Sturnus vulgaris). , 1995 .

[41]  M. Hausberger Organization of Whistled Song Sequences in the European Starling , 1990 .

[42]  R. Mooney,et al.  Inhibitory and Excitatory Mechanisms Underlying Auditory Responses to Learned Vocalizations in the Songbird Nucleus HVC , 2003, Neuron.

[43]  C. Müller,et al.  Feature extraction and tonotopic organization in the avian auditory forebrain , 2004, Experimental Brain Research.

[44]  M S Lewicki,et al.  A review of methods for spike sorting: the detection and classification of neural action potentials. , 1998, Network.

[45]  D Margoliash,et al.  Gradual Emergence of Song Selectivity in Sensorimotor Structures of the Male Zebra Finch Song System , 1999, The Journal of Neuroscience.

[46]  M S Lewicki,et al.  Hierarchical Organization of Auditory Temporal Context Sensitivity , 1996, The Journal of Neuroscience.

[47]  L. Henry Captive and free living European starlings use differently their song repertoire , 1998 .

[48]  D. Margoliash Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  M Konishi,et al.  Dynamic control of auditory activity during sleep: Correlation between song response and EEG , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[51]  D. Perkel,et al.  Multiple cell types distinguished by physiological, pharmacological, and anatomic properties in nucleus HVc of the adult zebra finch. , 1998, Journal of neurophysiology.

[52]  P. Marler Birdsong and speech development: could there be parallels? , 1970, American scientist.

[53]  Jessica A. Cardin,et al.  Song system auditory responses are stable and highly tuned during sedation, rapidly modulated and unselective during wakefulness, and suppressed by arousal. , 2003, Journal of neurophysiology.

[54]  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.

[55]  Eliot A. Brenowitz Altered perception of species-specific song by female birds after lesions of a forebrain nucleus. , 1991, Science.

[56]  Miguel A. L. Nicolelis,et al.  Methods for Neural Ensemble Recordings , 1998 .

[57]  Gregory F Ball,et al.  Individual vocal recognition and the effect of partial lesions to HVc on discrimination, learning, and categorization of conspecific song in adult songbirds. , 2000, Journal of neurobiology.

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