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Proc Natl Acad Sci U S A. Aug 1, 1992; 89(15): 6818–6822.
PMCID: PMC49595

Song presentation induces gene expression in the songbird forebrain.

Abstract

We investigated the participation of genomic regulatory events in the response of the songbird brain to a natural auditory stimulus of known physiological and behavioral relevance, birdsong. Using in situ hybridization, we detected a rapid increase in forebrain mRNA levels of an immediate-early gene encoding a transcriptional regulator (ZENK; also known as zif-268, egr-1, NGFI-A, or Krox-24) following presentation of tape-recorded songs to canaries (Serinus canaria) and zebra finches (Taeniopygia guttata). ZENK induction is most marked in a forebrain region believed to participate in auditory processing and is greatest when birds hear the song of their own species. A significantly lower level of induction occurs when birds hear the song of a different species and no induction is seen after exposure to tone bursts. Cellular analysis indicates that the level of induction reflects the proportion of neurons recruited to express the gene. These results suggest a role for genomic responses in neural processes linked to song pattern recognition, discrimination, or the formation of auditory associations.

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  • Kroodsma DE. Reproductive development in a female songbird: differential stimulation by quality of male song. Science. 1976 May 7;192(4239):574–575. [PubMed]
  • Marler P, Peters S. Selective vocal learning in a sparrow. Science. 1977 Nov 4;198(4316):519–521. [PubMed]
  • Nottebohm F, Stokes TM, Leonard CM. Central control of song in the canary, Serinus canarius. J Comp Neurol. 1976 Feb 15;165(4):457–486. [PubMed]
  • Nottebohm F, Kelley DB, Paton JA. Connections of vocal control nuclei in the canary telencephalon. J Comp Neurol. 1982 Jun 1;207(4):344–357. [PubMed]
  • Konishi M. Birdsong for neurobiologists. Neuron. 1989 Nov;3(5):541–549. [PubMed]
  • Karten HJ. The ascending auditory pathway in the pigeon (Columba livia). II. Telencephalic projections of the nucleus ovoidalis thalami. Brain Res. 1968 Oct;11(1):134–153. [PubMed]
  • Kelley DB, Nottebohm F. Projections of a telencephalic auditory nucleus-field L-in the canary. J Comp Neurol. 1979 Feb 1;183(3):455–469. [PubMed]
  • Müller CM, Leppelsack HJ. Feature extraction and tonotopic organization in the avian auditory forebrain. Exp Brain Res. 1985;59(3):587–599. [PubMed]
  • Margoliash D. Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. J Neurosci. 1983 May;3(5):1039–1057. [PubMed]
  • Williams H, Nottebohm F. Auditory responses in avian vocal motor neurons: a motor theory for song perception in birds. Science. 1985 Jul 19;229(4710):279–282. [PubMed]
  • Margoliash D. Preference for autogenous song by auditory neurons in a song system nucleus of the white-crowned sparrow. J Neurosci. 1986 Jun;6(6):1643–1661. [PubMed]
  • Hunt SP, Pini A, Evan G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature. 1987 Aug 13;328(6131):632–634. [PubMed]
  • Dragunow M, Robertson HA. Kindling stimulation induces c-fos protein(s) in granule cells of the rat dentate gyrus. Nature. 1987 Oct 1;329(6138):441–442. [PubMed]
  • Sagar SM, Sharp FR, Curran T. Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science. 1988 Jun 3;240(4857):1328–1331. [PubMed]
  • Bartel DP, Sheng M, Lau LF, Greenberg ME. Growth factors and membrane depolarization activate distinct programs of early response gene expression: dissociation of fos and jun induction. Genes Dev. 1989 Mar;3(3):304–313. [PubMed]
  • Sheng M, Greenberg ME. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron. 1990 Apr;4(4):477–485. [PubMed]
  • Goelet P, Castellucci VF, Schacher S, Kandel ER. The long and the short of long-term memory--a molecular framework. Nature. 322(6078):419–422. [PubMed]
  • Christy BA, Lau LF, Nathans D. A gene activated in mouse 3T3 cells by serum growth factors encodes a protein with "zinc finger" sequences. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7857–7861. [PMC free article] [PubMed]
  • Sukhatme VP, Cao XM, Chang LC, Tsai-Morris CH, Stamenkovich D, Ferreira PC, Cohen DR, Edwards SA, Shows TB, Curran T, et al. A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization. Cell. 1988 Apr 8;53(1):37–43. [PubMed]
  • Milbrandt J. A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science. 1987 Nov 6;238(4828):797–799. [PubMed]
  • Lemaire P, Revelant O, Bravo R, Charnay P. Two mouse genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cells. Proc Natl Acad Sci U S A. 1988 Jul;85(13):4691–4695. [PMC free article] [PubMed]
  • Clayton DF, Huecas ME, Sinclair-Thompson EY, Nastiuk KL, Nottebohm F. Probes for rare mRNAs reveal distributed cell subsets in canary brain. Neuron. 1988 May;1(3):249–261. [PubMed]
  • Saini KD, Leppelsack HJ. Cell types of the auditory caudomedial neostriatum of the starling (Sturnus vulgaris). J Comp Neurol. 1981 May 10;198(2):209–229. [PubMed]
  • Northcutt RG. Evolution of the telencephalon in nonmammals. Annu Rev Neurosci. 1981;4:301–350. [PubMed]
  • Reiner A, Davis BM, Brecha NC, Karten HJ. The distribution of enkephalinlike immunoreactivity in the telencephalon of the adult and developing domestic chicken. J Comp Neurol. 1984 Sep 10;228(2):245–262. [PubMed]
  • Müller CM. Differential effects of acetylcholine in the chicken auditory neostriatum and hyperstriatum ventrale--studies in vivo and in vitro. J Comp Physiol A. 1987 Nov;161(6):857–866. [PubMed]
  • Christy B, Nathans D. DNA binding site of the growth factor-inducible protein Zif268. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8737–8741. [PMC free article] [PubMed]
  • Wisden W, Errington ML, Williams S, Dunnett SB, Waters C, Hitchcock D, Evan G, Bliss TV, Hunt SP. Differential expression of immediate early genes in the hippocampus and spinal cord. Neuron. 1990 Apr;4(4):603–614. [PubMed]
  • Cole AJ, Saffen DW, Baraban JM, Worley PF. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature. 1989 Aug 10;340(6233):474–476. [PubMed]
  • Rusak B, Robertson HA, Wisden W, Hunt SP. Light pulses that shift rhythms induce gene expression in the suprachiasmatic nucleus. Science. 1990 Jun 8;248(4960):1237–1240. [PubMed]
  • Konishi M, Akutagawa E. Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain. Nature. 1985 May 9;315(6015):145–147. [PubMed]
  • Nordeen KW, Nordeen EJ. Projection neurons within a vocal motor pathway are born during song learning in zebra finches. Nature. 1988 Jul 14;334(6178):149–151. [PubMed]
  • Nottebohm F. A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science. 1981 Dec 18;214(4527):1368–1370. [PubMed]
  • Nottebohm F. From bird song to neurogenesis. Sci Am. 1989 Feb;260(2):74–79. [PubMed]
  • Alvarez-Buylla A, Kirn JR, Nottebohm F. Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science. 1990 Sep 21;249(4975):1444–1446. [PubMed]

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