Conspecific and heterospecific song discrimination in male zebra finches with lesions in the anterior forebrain pathway.

Adult zebra finches can produce normal song in the absence of Area X, IMAN, or DLM, nuclei that constitute the anterior forebrain pathway of songbirds. Here, we address whether lesions involving Area X and IMAN affect adult male zebra finches' ability to discriminate between conspecific or heterospecific songs. Intact birds and lesioned birds were trained on an operant GO/NOGO conditioning paradigm to discriminate between hetero- or conspecific songs. Both lesioned and intact birds were able to learn all discriminations. Lesioned and intact birds performed equivalently on canary song discriminations. In contrast, discriminations involving bird's own song took significantly more trails to learn for lesioned birds than for intact birds. Discrimination between conspecific songs in general also took longer in the lesioned birds, but missed significance level. Birds with control lesions medial to Area X did not show any differences from intact animals. Our results suggest that an intact anterior forebrain pathway is not required to discriminate between heterospecific songs. In contrast, Area X and IMAN contribute to a male zebra finch's ability to discriminate between its own song and that of other zebra finches.

[1]  H. Williams,et al.  Auditory responses in avian vocal motor neurons: a motor theory for song perception in birds. , 1985, Science.

[2]  U. Heinemann,et al.  Electrophysiological and morphological evidence for a new projection of LMAN‐neurones towards area X , 1995, Neuroreport.

[3]  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.

[4]  A. Reiner,et al.  Neurotransmitter organization and connectivity of the basal ganglia in vertebrates: implications for the evolution of basal ganglia. , 1995, Brain, behavior and evolution.

[5]  G. E. Vates,et al.  Feedback circuitry within a song-learning pathway. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[6]  R. Sossinka,et al.  Song Types in the Zebra Finch Poephila guttata castanotis1 , 1980 .

[7]  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.

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

[9]  Sandra A. Brown,et al.  Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches , 1989, The Journal of comparative neurology.

[10]  E. Nordeen,et al.  Long-term maintenance of song in adult zebra finches is not affected by lesions of a forebrain region involved in song learning. , 1993, Behavioral and neural biology.

[11]  Andrew P. King,et al.  A Brain of Her Own: A Neural Correlate of Song Assessment in a Female Songbird , 1997, Neurobiology of Learning and Memory.

[12]  P. McArthur Similarity of playback songs to self song as a determinant of response strength in song sparrows (Melospiza melodia) , 1986, Animal Behaviour.

[13]  R. Dooling,et al.  Perception of conspecific faces by budgerigars (Melopsittacus undulatus): I. Natural faces. , 1992, Journal of comparative psychology.

[14]  O. Hikosaka Basal ganglia — possible role in motor coordination and learning , 1991, Current Opinion in Neurobiology.

[15]  S. Volman,et al.  Development of neural selectivity for birdsong during vocal learning , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  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.

[17]  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.

[18]  H. Williams,et al.  Hemispheric differences in avian song discrimination. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[19]  S. Bottjer,et al.  Circuits, hormones, and learning: vocal behavior in songbirds. , 1997, Journal of neurobiology.

[20]  A. Doupe,et al.  Song- and order-selective neurons develop in the songbird anterior forebrain during vocal learning. , 1997, Journal of neurobiology.

[21]  D. Vicario,et al.  Song-selective auditory input to a forebrain vocal control nucleus in the zebra finch. , 1993, Journal of neurobiology.

[22]  F. Nottebohm,et al.  Testosterone facilitates some conspecific song discriminations in castrated zebra finches (Taeniopygia guttata). , 1992, Proceedings of the National Academy of Sciences of the United States of America.

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

[24]  F. Nottebohm,et al.  A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  Arturo Alvarez-Buylla,et al.  Simple microcomputer system for mapping tissue sections with the light microscope , 1988, Journal of Neuroscience Methods.

[26]  K. Okanoya,et al.  Auditory perception of conspecific and heterospecific vocalizations in birds: evidence for special processes. , 1992 .

[27]  H. Williams,et al.  Timbre discrimination in zebra finch (Taeniopygia guttata) song syllables. , 1990, Journal of comparative psychology.

[28]  R. Hassler Striatal control of locomotion, intentional actions and of integrating and perceptive activity , 1978, Journal of the Neurological Sciences.

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

[30]  A. Horn,et al.  How western meadowlarks classify their songs: evidence from song matching , 1988, Animal Behaviour.

[31]  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.

[32]  J. G. Stevenson Reinforcing effects of chaffinch song. , 1967, Animal Behaviour.

[33]  A. Reiner,et al.  Avian homologues of mammalian intralaminar, mediodorsal and midline thalamic nuclei: immunohistochemical and hodological evidence. , 1997, Brain, behavior and evolution.

[34]  F. Nottebohm,et al.  Role of gender, season, and familiarity in discrimination of conspecific song by zebra finches (Taeniopygia guttata). , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[35]  H. Williams,et al.  Song learning in birds: the relation between perception and production. , 1990, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[36]  P. Marler,et al.  Anterior forebrain pathway is needed for stable song expression in adult male white-crowned sparrows (Zonotrichia leucophrys) , 1998, Behavioural Brain Research.

[37]  Fernando Nottebohm,et al.  Reafferent thalamo‐“cortical” loops in the song system of oscine songbirds , 1997, The Journal of comparative neurology.

[38]  S. H. Hulse,et al.  Absolute and relative pitch discrimination in serial pitch perception by birds , 1984 .

[39]  A. Graybiel Building action repertoires: memory and learning functions of the basal ganglia , 1995, Current Opinion in Neurobiology.

[40]  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.

[41]  A. Arnold,et al.  Forebrain lesions disrupt development but not maintenance of song in passerine birds. , 1984, Science.

[42]  F. Nottebohm,et al.  Connections of vocal control nuclei in the canary telencephalon , 1982, The Journal of comparative neurology.

[43]  S. Okuhata,et al.  Synaptic connections of thalamo-cerebral vocal nuclei of the canary , 1987, Brain Research Bulletin.

[44]  E. Nordeen,et al.  Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. , 1990, Behavioral and neural biology.