Song‐Induced Gene Expression: A Window on Song Auditory Processing and Perception

Abstract: We review here evidence that a large portion of the caudomedial telencephalon of songbirds, distinct from the song control circuit, is involved in the perceptual processing of birdsong. When songbirds hear song, a number of caudomedial pallial areas are activated, as revealed by expression of the activity‐dependent gene zenk. These areas, which include field L subfields L1 and L3, as well as the adjacent caudomedial nidopallium (NCM) and caudomedial mesopallium (CMM), are part of the central auditory pathway and constitute a lobule in the caudomedial aspect of the telencephalon. Several lines of evidence indicate that the neural circuits integrating this lobule are capable of performing the auditory processing of song based on fine acoustic features. Thus, this lobule is well positioned to mediate song perceptual processing and discrimination, which are required for vocal communication and vocal learning. Importantly, the zenk gene encodes a transcription factor linked to synaptic plasticity, and it regulates the expression of target genes associated with specific neuronal cell functions. The induction of zenk likely represents a key regulatory event in a gene cascade triggered by song and leading to neuronal plasticity. Thus, zenk may be linked to molecular and cellular mechanisms underlying experience‐dependent modification of song‐responsive circuits. In summary, songbirds possess an elaborate system for song perceptual processing and discrimination that potentially also subserves song‐induced neuronal plasticity and song memory formation. The continued use of a multidisciplinary approach that integrates molecular, anatomical, physiological and behavioral methodologies has the potential to provide further significant insights into the underlying neurobiology of the perceptual aspects of vocal communication and learning.

[1]  T. Bliss,et al.  Differential expression of immediate early genes in the hippocampus and spinal cord , 1990, Neuron.

[2]  Amy A. Kruse,et al.  Development of song responses in the zebra finch caudomedial neostriatum: role of genomic and electrophysiological activities. , 2001, Journal of neurobiology.

[3]  C. Mello,et al.  Immediate-early gene responses in the avian song control system: cloning and expression analysis of the canary c-jun cDNA. , 1994, Brain research. Molecular brain research.

[4]  S. Volman,et al.  Quantitative assessment of song-selectivity in the zebra finch “high vocal center” , 1996, Journal of Comparative Physiology A.

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

[6]  H. Karten,et al.  Connections of the auditory forebrain in the pigeon (columba livia) , 1993, The Journal of comparative neurology.

[7]  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.

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

[10]  G D Pollak,et al.  GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. , 1992, Journal of neurophysiology.

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

[12]  P. Marler,et al.  Selective Vocal Learning in a Sparrow , 1977, Science.

[13]  Sidarta Ribeiro,et al.  Behaviourally driven gene expression reveals song nuclei in hummingbird brain , 2000, Nature.

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

[15]  W. K. Wong,et al.  Activation of Human Monoamine Oxidase B Gene Expression by a Protein Kinase C MAPK Signal Transduction Pathway Involves c-Jun and Egr-1* , 2002, The Journal of Biological Chemistry.

[16]  T. Curran,et al.  Expression of c-fos protein in brain: metabolic mapping at the cellular level. , 1988, Science.

[17]  L. Kaczmarek,et al.  Immediate early genes and inducible transcription factors in mapping of the central nervous system function and dysfunction , 2002 .

[18]  J. Bolhuis,et al.  Bird brains and songs: neural mechanisms of birdsong perception and memory , 2003 .

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

[20]  T. Herdegen,et al.  Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins , 1998, Brain Research Reviews.

[21]  James I. Morgan,et al.  Stimulus-transcription coupling in neurons: role of cellular immediate-early genes , 1989, Trends in Neurosciences.

[22]  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.

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

[24]  N. Pavletich,et al.  Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A , 1991, Science.

[25]  Masakazu Konishi,et al.  Decrystallization of adult birdsong by perturbation of auditory feedback , 1999, Nature.

[26]  D. Margoliash,et al.  Cytoarchitectonic organization and morphology of cells of the field L complex in male zebra finches (taenopygia guttata) , 1992, The Journal of comparative neurology.

[27]  C. Mello,et al.  Mapping vocal communication pathways in birds with inducible gene expression , 2002, Journal of Comparative Physiology A.

[28]  Rhea R. Kimpo,et al.  FOS Is Induced by Singing in Distinct Neuronal Populations in a Motor Network , 1997, Neuron.

[29]  H. Karten,et al.  The organization of the ascending auditory pathway in the pigeon (Columba livia). I. Diencephalic projections of the inferior colliculus (nucleus mesencephali lateralis, pars dorsalis). , 1967, Brain research.

[30]  C. Vianna,et al.  Analysis of Immediate-Early Gene Expression in the Songbird Brain Following Song Presentation , 1993 .

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

[32]  Johan J. Bolhuis,et al.  Localized immediate early gene expression related to the strength of song learning in socially reared zebra finches , 2001, The European journal of neuroscience.

[33]  P. Slater,et al.  Bird Song: Biological Themes and Variations , 1995 .

[34]  M. Criado,et al.  Phorbol ester activation of the neuronal nicotinic acetylcholine receptor alpha7 subunit gene: involvement of transcription factor Egr-1. , 2000, Journal of neurochemistry.

[35]  M. Greenberg,et al.  The regulation and function of c-fos and other immediate early genes in the nervous system , 1990, Neuron.

[36]  C. Catchpole,et al.  Female canaries that respond and discriminate more between male songs of different quality have a larger song control nucleus (HVC) in the brain. , 2002, Journal of neurobiology.

[37]  P. Marler,et al.  Singing in the brain. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[38]  W. Tischmeyer,et al.  Activation of immediate early genes and memory formation , 1999, Cellular and Molecular Life Sciences CMLS.

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

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

[41]  T. Devoogd,et al.  Interactions between Endocrinology and Learning in the Avian Song System , 1994, Annals of the New York Academy of Sciences.

[42]  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.

[43]  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.

[44]  K. Sen,et al.  Feature analysis of natural sounds in the songbird auditory forebrain. , 2001, Journal of neurophysiology.

[45]  R. Currie,et al.  Complexity of sensory environment drives the expression of candidate-plasticity gene, nerve growth factor induced-A , 2002, Neuroscience.

[46]  Timothy Q Gentner,et al.  Recent experience modulates forebrain gene–expression in response to mate–choice cues in European starlings , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[48]  R. Mooney,et al.  Intrinsic and Extrinsic Contributions to Auditory Selectivity in a Song Nucleus Critical for Vocal Plasticity , 2000, The Journal of Neuroscience.

[49]  T. Bliss,et al.  A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories , 2001, Nature Neuroscience.

[50]  Liisa A. Tremere,et al.  Expansion of receptive fields in raccoon somatosensory cortex in vivo by GABAA receptor antagonism: implications for cortical reorganization , 2001, Experimental Brain Research.

[51]  V. Sukhatme,et al.  A novel repression module, an extensive activation domain, and a bipartite nuclear localization signal defined in the immediate-early transcription factor Egr-1 , 1993, Molecular and cellular biology.

[52]  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.

[53]  H. Karten,et al.  Homology and evolutionary origins of the 'neocortex'. , 1991, Brain, behavior and evolution.

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

[55]  G. Thiel,et al.  Role of zinc-finger proteins Sp1 and zif268/egr-1 in transcriptional regulation of the human synaptobrevin II gene. , 1996, European journal of biochemistry.

[56]  M E Greenberg,et al.  Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. , 1993, Science.

[57]  H. Scheich,et al.  Functional organization of the avian auditory cortex analogue. II. Topographic distribution of latency , 1991, Brain Research.

[58]  A. Sillito The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. , 1975, The Journal of physiology.

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

[60]  J. Julien,et al.  AP-1 and Krox-24 transcription factors activate the neurofilament light gene promoter in P19 embryonal carcinoma cells. , 1994, Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research.

[61]  M. Konishi,et al.  Effects of deafening on song development in American robins and black-headed grosbeaks. , 1965, Zeitschrift fur Tierpsychologie.

[62]  F. Nottebohm,et al.  For Whom The Bird Sings Context-Dependent Gene Expression , 1998, Neuron.

[63]  S. H. Hulse,et al.  Female European starling preference and choice for variation in conspecific male song , 2000, Animal Behaviour.

[64]  R. Dykes,et al.  Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. , 1984, Journal of neurophysiology.

[65]  R. Dooling,et al.  Auditory pathways in the budgerigar. I. Thalamo-telencephalic projections. , 1987, Brain, behavior and evolution.

[66]  Eliot A. Brenowitz,et al.  Sexual dimorphisms in the neural vocal control system in song birds: ontogeny and phylogeny. , 1986, Brain, behavior and evolution.

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

[68]  Bruce L. McNaughton,et al.  Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles , 1999, Nature Neuroscience.

[69]  Gregory F Ball,et al.  Neural bases of song preferences in female zebra finches (Taeniopygia guttata) , 1998, Neuroreport.

[70]  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.

[71]  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.

[72]  J. Leah,et al.  The Egr transcription factors and their utility in mapping brain functioning , 2002 .

[73]  Anil Kumar,et al.  Acoustic communication in birds , 2003 .

[74]  D. Clayton,et al.  The Genomic Action Potential , 2000, Neurobiology of Learning and Memory.

[75]  C. Ang Emerging Auditory Selectivity in the Caudomedial Neostriatum of the Zebra Finch Songbird , 2001 .

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

[77]  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.

[78]  Carol A Barnes,et al.  Imaging neural activity with temporal and cellular resolution using FISH , 2001, Current Opinion in Neurobiology.

[79]  H. Scheich,et al.  Responsiveness of units in the auditory neostriatum of the guinea fowl (Numida meleagris) to species-specific calls and synthetic stimuli , 1979, Journal of comparative physiology.

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

[81]  R. Dooling,et al.  Auditory Pathways in the Budgerigar (Part 1 of 2) , 1987 .

[82]  G. Manley,et al.  Auditory processing in birds , 2000, Current Opinion in Neurobiology.

[83]  Khashayar Farsad,et al.  Comparative Vertebrate Neuroanatomy: Evolution and Adaptation , 1996, The Yale Journal of Biology and Medicine.

[84]  Gregory F Ball,et al.  Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. , 2001, Journal of neurobiology.

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

[86]  D. Margoliash,et al.  Neuronal populations and single cells representing learned auditory objects , 2003, Nature.

[87]  E. Nordeen,et al.  Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. , 1992, Behavioral and neural biology.

[88]  N Suga,et al.  Sharpening of frequency tuning by inhibition in the thalamic auditory nucleus of the mustached bat. , 1997, Journal of neurophysiology.

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

[90]  Richard J. Salvi,et al.  GABA-A antagonist causes dramatic expansion of tuning in primary auditory cortex. , 2000, Neuroreport.

[91]  F. Nottebohm,et al.  Conspecific and heterospecific song discrimination in male zebra finches with lesions in the anterior forebrain pathway. , 1998, Journal of neurobiology.

[92]  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.

[93]  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.

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

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

[96]  F. Nottebohm,et al.  Projections of a telencephalic auditory nucleus– field L–in the canary , 1979, The Journal of comparative neurology.

[97]  S Schoch,et al.  Regulation of synapsin I gene expression by the zinc finger transcription factor zif268/egr-1. , 1994, The Journal of biological chemistry.

[98]  M. Konishi The role of auditory feedback in the control of vocalization in the white-crowned sparrow. , 1965, Zeitschrift fur Tierpsychologie.

[99]  S. Brauth,et al.  Auditory Pathways in the Budgerigar , 1987 .

[100]  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.

[101]  D. Clayton,et al.  Localized Changes in Immediate-Early Gene Regulation during Sensory and Motor Learning in Zebra Finches , 1997, Neuron.

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

[103]  D. Nathans,et al.  DNA binding site of the growth factor-inducible protein Zif268. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[104]  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.

[105]  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.

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

[107]  H. Karten,et al.  The ascending auditory pathway in the pigeon (Columba livia). II. Telencephalic projections of the nucleus ovoidalis thalami. , 1968, Brain research.

[108]  H. Williams,et al.  Sexual dimorphism of auditory activity in the zebra finch song system. , 1985, Behavioral and neural biology.

[109]  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.

[110]  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.

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

[112]  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.

[113]  Sarah M. N. Woolley,et al.  Vocal Memory and Learning in Adult Bengalese Finches with Regenerated Hair Cells , 2002, The Journal of Neuroscience.

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

[115]  B. Ziółkowska,et al.  Chapter I Methods used in inducible transcription factor studies: focus on mRNA , 2002 .

[116]  D. Margoliash,et al.  Parallel pathways and convergence onto HVc and adjacent neostriatum of adult zebra finches (Taeniopygia guttata) , 1995, The Journal of comparative neurology.

[117]  J. Baraban,et al.  A Dominant Negative Egr Inhibitor Blocks Nerve Growth Factor-Induced Neurite Outgrowth by Suppressing c-Jun Activation: Role of an Egr/c-Jun Complex , 2002, The Journal of Neuroscience.

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

[119]  Philip Goelet,et al.  The long and the short of long–term memory—a molecular framework , 1986, Nature.

[120]  J. Salbaum,et al.  Evolutionary conservation of the immediate-early gene ZENK. , 1998, Molecular biology and evolution.

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

[122]  C. Mello Chapter IV Immediate-early gene (IEG) expression mapping of vocal communication areas in the avian brain , 2002 .

[123]  Sidarta Ribeiro,et al.  Toward a Song Code Evidence for a Syllabic Representation in the Canary Brain , 1998, Neuron.

[124]  S Schoch,et al.  The Human Synapsin II Gene Promoter , 1995, The Journal of Biological Chemistry.

[125]  E. Jarvis,et al.  Molecular mapping of brain areas involved in parrot vocal communication , 2000, The Journal of comparative neurology.