Molecular microcircuitry underlies functional specification in a basal ganglia circuit dedicated to vocal learning

Neuron

Volumn 73, Issue 3, 2012, Pages 537-552

  Hilliard, AustinT ^a   Miller, JulieE ^a   Fraley, Elizabeth R ^a   Horvath, Steve ^a   White, StephanieA ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BEHAVIOR CONTROL; CONTROLLED STUDY; FOXP2 GENE; GENE EXPRESSION PROFILING; LEARNING; MICROARRAY ANALYSIS; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; SINGING; SONGBIRD; VENTRAL STRIATOPALLIDUM; VOCALIZATION;

ANIMALS; BASAL GANGLIA; COMPUTATIONAL BIOLOGY; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; MALE; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHOPYRUVATE HYDRATASE; SONGBIRDS; VOCALIZATION, ANIMAL;

EID: 84863052622     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.01.005     Document Type: Article

References (51)

1. Balthazart J., Voigt C., Boseret G., Ball G.F. Expression of reelin, its receptors and its intracellular signaling protein, Disabled1 in the canary brain: relationships with the song control system. Neuroscience 2008, 153:944-962.
2. Benjamini Y., Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. Royal Stat. Soc. Series B (Methodological) 1995, 57:289-300.
3. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., Xing Y., Lubischer J.L., Krieg P.A., Krupenko S.A., et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J.Neurosci. 2008, 28:264-278.
4. Enard W., Gehre S., Hammerschmidt K., Hölter S.M., Blass T., Somel M., Brückner M.K., Schreiweis C., Winter C., Sohr R., et al. A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell 2009, 137:961-971.
5. Farries M.A., Perkel D.J. A telencephalic nucleus essential for song learning contains neurons with physiological characteristics of both striatum and globus pallidus. J.Neurosci. 2002, 22:3776-3787.
6. Feenders G., Liedvogel M., Rivas M., Zapka M., Horita H., Hara E., Wada K., Mouritsen H., Jarvis E.D. Molecular mapping of movement-associated areas in the avian brain: a motor theory for vocal learning origin. PLoS ONE 2008, 3:e1768.
7. Haesler S., Rochefort C., Georgi B., Licznerski P., Osten P., Scharff C. Incomplete and inaccurate vocal imitation after knockdown of FoxP2 insongbird basal ganglia nucleus Area X. PLoS Biol. 2007, 5:e321.
8. Hahnloser R.H.R., Kozhevnikov A.A., Fee M.S. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 2002, 419:65-70.
9. Halassa M.M., Haydon P.G. Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu. Rev. Physiol. 2010, 72:335-355.
10. Herz J., Chen Y. Reelin, lipoprotein receptors and synaptic plasticity. Nat. Rev. Neurosci. 2006, 7:850-859.
11. Hessler N.A., Doupe A.J. Singing-related neural activity in a dorsal forebrain-basal ganglia circuit of adult zebra finches. J.Neurosci. 1999, 19:10461-10481.
12. Hosono K., Noda S., Shimizu A., Nakanishi N., Ohtsubo M., Shimizu N., Minoshima S. YPEL5 protein of the YPEL gene family is involved in the cell cycle progression by interacting with two distinct proteins RanBPM and RanBP10. Genomics 2010, 96:102-111.
13. Hu Z., Mellor J., Wu J., DeLisi C. VisANT: an online visualization and analysis tool for biological interaction data. BMC Bioinformatics 2004, 5:17.
14. Huang W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
15. Jarvis E.D. Learned birdsong and the neurobiology of human language. Ann. N Y Acad. Sci. 2004, 1016:749-777.
16. Jarvis E.D., Nottebohm F. Motor-driven gene expression. Proc. Natl. Acad. Sci. USA 1997, 94:4097-4102.
17. Jarvis E.D., Scharff C., Grossman M.R., Ramos J.A., Nottebohm F. For whom the bird sings: context-dependent gene expression. Neuron 1998, 21:775-788.
18. Kaestner K.H., Knochel W., Martinez D.E. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 2000, 14:142-146.
19. Kim Y.H., Perlman W.R., Arnold A.P. Expression of androgen receptor mRNA in zebra finch song system: developmental regulation by estrogen. J.Comp. Neurol. 2004, 469:535-547.
20. Kimpo R.R., Doupe A.J. FOS is induced by singing in distinct neuronal populations in a motor network. Neuron 1997, 18:315-325.
21. Konopka G., Bomar J.M., Winden K., Coppola G., Jonsson Z.O., Gao F.Y., Peng S., Preuss T.M., Wohlschlegel J.A., Geschwind D.H. Human-specific transcriptional regulation of CNS development genes by FOXP2. Nature 2009, 462:213-217.
22. Langfelder P., Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 2008, 9:559.
23. Langfelder P., Zhang B., Horvath S. Defining clusters froma hierarchical cluster tree: the Dynamic Tree Cut package for R. Bioinformatics 2008, 24:719-720.
24. Langfelder P., Luo R., Oldham M.C., Horvath S. Is my network module preserved and reproducible?. PLoS Comput. Biol. 2011, 7:e1001057.
25. Li X., Wang X.J., Tannenhauser J., Podell S., Mukherjee P., Hertel M., Biane J., Masuda S., Nottebohm F., Gaasterland T. Genomic resources for songbird research and their use in characterizing gene expression during brain development. Proc. Natl. Acad. Sci. USA 2007, 104:6834-6839.
26. Lieberman P. Toward an Evolutionary Biology of Language 2006, Harvard University Press, Cambridge.
27. Maccarrone M., Rossi S., Bari M., De Chiara V., Fezza F., Musella A., Gasperi V., Prosperetti C., Bernardi G., Finazzi-Agrò A., et al. Anandamide inhibits metabolism and physiological actions of 2-arachidonoylglycerol in the striatum. Nat. Neurosci. 2008, 11:152-159.
28. Miller J.E., Spiteri E., Condro M.C., Dosumu-Johnson R.T., Geschwind D.H., White S.A. Birdsong decreases protein levels of FoxP2, a molecule required for human speech. J.Neurophysiol. 2008, 100:2015-2025.
29. Miller J.E., Hilliard A.T., White S.A. Song practice promotes acutevocal variability at a key stage of sensorimotor learning. PLoS ONE 2010, 5:e8592.
30. Musella A., De Chiara V., Rossi S., Prosperetti C., Bernardi G., Maccarrone M., Centonze D. TRPV1 channels facilitate glutamate transmission in the striatum. Mol. Cell. Neurosci. 2009, 40:89-97.
31. Nottebohm F. The road we travelled: discovery, choreography, and significance of brain replaceable neurons. Ann. N Y Acad. Sci. 2004, 1016:628-658.
32. Oldham M.C., Konopka G., Iwamoto K., Langfelder P., Kato T., Horvath S., Geschwind D.H. Functional organization of the transcriptome in human brain. Nat. Neurosci. 2008, 11:1271-1282.
33. Poopatanapong A., Teramitsu I., Byun J.S., Vician L.J., Herschman H.R., White S.A. Singing, but not seizure, induces synaptotagmin IV in zebra finch song circuit nuclei. J.Neurobiol. 2006, 66:1613-1629.
34. Reiner A., Perkel D.J., Bruce L.L., Butler A.B., Csillag A., Kuenzel W., Medina L., Paxinos G., Shimizu T., Striedter G., et al. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J.Comp. Neurol. 2004, 473:377-414. Avian Brain Nomenclature Forum.
35. Replogle K., Arnold A.P., Ball G.F., Band M., Bensch S., Brenowitz E.A., Dong S., Drnevich J., Ferris M., George J.M., et al. The Songbird Neurogenomics (SoNG) Initiative: community-based tools and strategies for study of brain gene function and evolution. BMC Genomics 2008, 9:131.
36. Soderstrom K., Luo B. Late-postnatal cannabinoid exposure persistently increases FoxP2 expression within zebra finch striatum. Dev. Neurobiol. 2010, 70:195-203.
37. Soderstrom K., Tian Q. Distinct periods of cannabinoid sensitivity during zebra finch vocal development. Brain Res. Dev. Brain Res. 2004, 153:225-232.
38. Spiteri E., Konopka G., Coppola G., Bomar J., Oldham M., Ou J., Vernes S.C., Fisher S.E., Ren B., Geschwind D.H. Identification of the transcriptional targets of FOXP2, a gene linked to speech and language, in developing human brain. Am. J. Hum. Genet. 2007, 81:1144-1157.
39. Tchernichovski O., Nottebohm F., Ho C.E., Pesaran B., Mitra P.P. A procedure for an automated measurement of song similarity. Anim. Behav. 2000, 59:1167-1176.
40. Teramitsu I., White S.A. FoxP2 regulation during undirected singing in adult songbirds. J.Neurosci. 2006, 26:7390-7394.
41. Teramitsu I., Kudo L.C., London S.E., Geschwind D.H., White S.A. Parallel FoxP1 and FoxP2 expression in songbird and human brain predicts functional interaction. J.Neurosci. 2004, 24:3152-3163.
42. Teramitsu I., Poopatanapong A., Torrisi S., White S.A. Striatal FoxP2 is actively regulated during songbird sensorimotor learning. PLoS ONE 2010, 5:e8548.
43. Thompson J.A., Perkel D.J. Endocannabinoids mediate synaptic plasticity at glutamatergic synapses on spiny neurons within a basal ganglia nucleus necessary for song learning. J.Neurophysiol. 2011, 105:1159-1169.
44. Vernes S.C., Spiteri E., Nicod J., Groszer M., Taylor J.M., Davies K.E., Geschwind D.H., Fisher S.E. High-throughput analysis of promoter occupancy reveals direct neural targets of FOXP2, a gene mutated in speech and language disorders. Am. J. Hum. Genet. 2007, 81:1232-1250.
45. Vernes S.C., Oliver P.L., Spiteri E., Lockstone H.E., Puliyadi R., Taylor J.M., Ho J., Mombereau C., Brewer A., Lowy E., et al. Foxp2 regulates gene networks implicated in neurite outgrowth in the developing brain. PLoS Genet. 2011, 7:e1002145.
46. Wada K., Howard J.T., McConnell P., Whitney O., Lints T., Rivas M.V., Horita H., Patterson M.A., White S.A., Scharff C., et al. A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. Proc. Natl. Acad. Sci. USA 2006, 103:15212-15217.
47. Warren W.C., Clayton D.F., Ellegren H., Arnold A.P., Hillier L.W., Künstner A., Searle S., White S., Vilella A.J., Fairley S., et al. The genome of a songbird. Nature 2010, 464:757-762.
48. White S.A. Genes and vocal learning. Brain Lang. 2010, 115:21-28.
49. Yip A.M., Horvath S. Gene network interconnectedness and thegeneralized topological overlap measure. BMC Bioinformatics 2007, 8:22.
50. Zhang B., Horvath S. A general framework for weighted gene co-expression network analysis. Stat. Appl. Genet. Mol. Biol. 2005, 4:e17.
51. Zhao W., Langfelder P., Fuller T., Dong J., Li A., Hovarth S. Weighted gene coexpression network analysis: state of the art. J.Biopharm. Stat. 2010, 20:281-300.