FOS Is Induced by Singing in Distinct Neuronal Populations in a Motor Network

Mechanisms underlying the learned vocal behavior of songbirds were studied by examining expression of the protein product of the immediate early gene c-fos (Fos) in zebra finches. Auditory stimuli including the bird's own song did not induce Fos in the song system. In contrast, the motor act of singing induced Fos in two song sensorimotor nuclei, HVc and RA. This induction was independent of auditory feedback, since it occurred in deafened birds that sang. Double-labeling studies demonstrated that only one of the two sets of projection neurons in HVc expressed singing-related Fos. The motor-driven induction of Fos identifies functionally distinct cell populations in a network for singing and may point to sites of cellular plasticity necessary for song maintenance.

[1]  Jonathan A. Cooper,et al.  Platelet-derived growth factor induces rapid but transient expression of the c-fos gene and protein , 1984, Nature.

[2]  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.

[3]  T. Curran,et al.  Superinduction of c-fos by nerve growth factor in the presence of peripherally active benzodiazepines. , 1985, Science.

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

[5]  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.

[6]  F. Nottebohm,et al.  High vocal center growth and its relation to neurogenesis, neuronal replacement and song acquisition in juvenile canaries. , 1992, Journal of neurobiology.

[7]  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.

[8]  H Scheich,et al.  Comparison of Frequency‐specific c‐Fos Expression and Fluoro‐2‐deoxyglucose Uptake in Auditory Cortex of Gerbils (Meriones unguiculatus) , 1995, The European journal of neuroscience.

[9]  Arousal enhances [14C]2-deoxyglucose uptake in four forebrain areas of the zebra finch , 1986, Behavioural Brain Research.

[10]  R. McCarley,et al.  Activation of Ventrolateral Preoptic Neurons During Sleep , 1996, Science.

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

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

[13]  U. Jürgens,et al.  C‐fos Expression During Vocal Mobbing in the New World Monkey Saguinus fuscicollis , 1996, The European journal of neuroscience.

[14]  F. Nottebohm,et al.  Direct evidence for loss and replacement of projection neurons in adult canary brain , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  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.

[16]  K. Herrmann,et al.  Isolation-dependent enhancement of 2-[14C]deoxyglucose uptake in the forebrain of zebra finch males. , 1988, Behavioral and neural biology.

[17]  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.

[18]  Philip H. Price Developmental determinants of structure in zebra finch song. , 1979 .

[19]  Frank Johnson,et al.  Topographic organization of a forebrain pathway involved with vocal learning in zebra finches , 1995, The Journal of comparative neurology.

[20]  L. Teesch,et al.  Intrinsic interactions between alkaline earth metal ions and peptides: a gas-phase study , 1990 .

[21]  T. Curran,et al.  Calcium as a modulator of the immediate-early gene cascade in neurons. , 1988, Cell calcium.

[22]  E.C.L. Vu,et al.  Identification of a forebrain motor programming network for the learned song of zebra finches , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  K. Chergui,et al.  Burst stimulation of the medial forebrain bundle selectively increases Fos-like immunoreactivity in the limbic forebrain of the rat , 1996, Neuroscience.

[24]  R. Mooney,et al.  Two distinct inputs to an avian song nucleus activate different glutamate receptor subtypes on individual neurons. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

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

[26]  F. Nottebohm,et al.  Birth of projection neurons in the higher vocal center of the canary forebrain before, during, and after song learning. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

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

[28]  I. Verma,et al.  Induction of the proto-oncogene fos by nerve growth factor. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

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

[30]  D. Hosford,et al.  Induction of c-fos mRNA by kindled seizures: complex relationship with neuronal burst firing , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  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.

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

[33]  奥畑 荘司 Synaptic connections of thalamo-cerebral vocal nuclei of the canary , 1987 .

[34]  F. Nottebohm,et al.  Role of a telencephalic nucleus in the delayed song learning of socially isolated zebra finches. , 1993, Journal of neurobiology.

[35]  M. Greenberg,et al.  Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. , 1986, Science.

[36]  J. Kleim,et al.  Synaptogenesis and FOS Expression in the Motor Cortex of the Adult Rat after Motor Skill Learning , 1996, The Journal of Neuroscience.

[37]  E. M. Rouiller,et al.  Mapping of the motor pathways in rats: c-fos induction by intracortical microstimulation of the motor cortex correlated with efferent connectivity of the site of cortical stimulation , 1992, Neuroscience.

[38]  W. Wisden,et al.  Light pulses that shift rhythms induce gene expression in the suprachiasmatic nucleus. , 1990, Science.

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

[40]  F. Sharp,et al.  Metabolic mapping with cellular resolution: c-fos vs. 2-deoxyglucose. , 1993, Critical reviews in neurobiology.

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

[42]  F. Sharp,et al.  Light induces a Fos-like nuclear antigen in retinal neurons. , 1990, Brain research. Molecular brain research.

[43]  T. Curran,et al.  Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. , 1991, Annual review of neuroscience.

[44]  E. Nordeen,et al.  Estrogen accumulation in zebra finch song control nuclei: implications for sexual differentiation and adult activation of song behavior. , 1987, Journal of neurobiology.

[45]  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.

[46]  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.

[47]  J. Kornhauser,et al.  Regulation of jun-B messenger RNA and AP-1 activity by light and a circadian clock. , 1992, Science.

[48]  A. C. Yu,et al.  Temporal Hierarchical Control of Singing in Birds , 1996, Science.

[49]  H. Williams,et al.  Temporal patterning of song production: participation of nucleus uvaeformis of the thalamus. , 1993, Journal of neurobiology.

[50]  E. Nordeen,et al.  Projections of androgen-accumulating neurons in a nucleus controlling avian song , 1989, Brain Research.

[51]  S. Rose,et al.  Effects of early experience on c-fos gene expression in the chick forebrain , 1991, Brain Research.

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

[53]  S. Hunt,et al.  Induction of c-fos-like protein in spinal cord neurons following sensory stimulation , 1987, Nature.

[54]  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.

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

[56]  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.

[57]  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.

[58]  James I. Morgan,et al.  Role of ion flux in the control of c-fos expression , 1986, Nature.

[59]  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.

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

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

[62]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[63]  J R McKibben,et al.  Changes in stereotyped central motor patterns controlling vocalization are induced by peripheral nerve injury. , 1992, Behavioral and neural biology.

[64]  Ann M Graybiel,et al.  Network-Level Changes in Expression of Inducible Fos–Jun Proteins in the Striatum during Chronic Cocaine Treatment and Withdrawal , 1996, Neuron.

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