Impact of Experience-dependent and -independent Factors on Gene Expression in Songbird Brain

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2012 Oct 10

PMID 23045667

Citations 35

Authors

Jenny Drnevich

Kirstin L Replogle

Peter Lovell

Thomas P Hahn

Frank Johnson

Thomas G Mast

Ernest Nordeen

Kathy Nordeen

Christy Strand

Sarah E London

Motoko Mukai

John C Wingfield

Arthur P Arnold

Gregory F Ball

Eliot A Brenowitz

Juli Wade

Claudio V Mello

David F Clayton

Affiliations

Soon will be listed here.

Abstract

Songbirds provide rich natural models for studying the relationships between brain anatomy, behavior, environmental signals, and gene expression. Under the Songbird Neurogenomics Initiative, investigators from 11 laboratories collected brain samples from six species of songbird under a range of experimental conditions, and 488 of these samples were analyzed systematically for gene expression by microarray. ANOVA was used to test 32 planned contrasts in the data, revealing the relative impact of different factors. The brain region from which tissue was taken had the greatest influence on gene expression profile, affecting the majority of signals measured by 18,848 cDNA spots on the microarray. Social and environmental manipulations had a highly variable impact, interpreted here as a manifestation of paradoxical "constitutive plasticity" (fewer inducible genes) during periods of enhanced behavioral responsiveness. Several specific genes were identified that may be important in the evolution of linkages between environmental signals and behavior. The data were also analyzed using weighted gene coexpression network analysis, followed by gene ontology analysis. This revealed modules of coexpressed genes that are also enriched for specific functional annotations, such as "ribosome" (expressed more highly in juvenile brain) and "dopamine metabolic process" (expressed more highly in striatal song control nucleus area X). These results underscore the complexity of influences on neural gene expression and provide a resource for studying how these influences are integrated during natural experience.

Citing Articles

Divergence in expression of a singing-related neuroplasticity gene in the brains of 2 Ficedula flycatchers and their hybrids.

Wheatcroft D, Backstrom N, Dutoit L, McFarlane S, Mugal C, Wang M G3 (Bethesda). 2024; 15(2).

PMID: 39670717 PMC: 11797017. DOI: 10.1093/g3journal/jkae293.

Gene co-expression analysis reveals conserved and distinct gene networks between resistant and susceptible Lens ervoides challenged by hemibiotrophic and necrotrophic pathogens.

Cao Z, Banniza S Sci Rep. 2024; 14(1):24967.

PMID: 39443543 PMC: 11499849. DOI: 10.1038/s41598-024-76316-x.

Sensogenomics of music and Alzheimer's disease: An interdisciplinary view from neuroscience, transcriptomics, and epigenomics.

Navarro L, Gomez-Carballa A, Pischedda S, Montoto-Louzao J, Viz-Lasheras S, Camino-Mera A Front Aging Neurosci. 2023; 15:1063536.

PMID: 36819725 PMC: 9935844. DOI: 10.3389/fnagi.2023.1063536.

Dynamic transcriptome landscape in the song nucleus HVC between juvenile and adult zebra finches.

Shi Z, Zhang Z, Schaffer L, Huang Z, Fu L, Head S Adv Genet (Hoboken). 2023; 2(1):e10035.

PMID: 36618441 PMC: 9744550. DOI: 10.1002/ggn2.10035.

Linking the genomic signatures of human beat synchronization and learned song in birds.

Gordon R, Ravignani A, Hyland Bruno J, Robinson C, Scartozzi A, Embalabala R Philos Trans R Soc Lond B Biol Sci. 2021; 376(1835):20200329.

PMID: 34420388 PMC: 8380983. DOI: 10.1098/rstb.2020.0329.

References

Nottebohm F, Stokes T, Leonard C . Central control of song in the canary, Serinus canarius. J Comp Neurol. 1976; 165(4):457-86. DOI: 10.1002/cne.901650405. View

Zapala M, Hovatta I, Ellison J, Wodicka L, Del Rio J, Tennant R . Adult mouse brain gene expression patterns bear an embryologic imprint. Proc Natl Acad Sci U S A. 2005; 102(29):10357-62. PMC: 1173363. DOI: 10.1073/pnas.0503357102. View

Oldham M, Horvath S, Geschwind D . Conservation and evolution of gene coexpression networks in human and chimpanzee brains. Proc Natl Acad Sci U S A. 2006; 103(47):17973-8. PMC: 1693857. DOI: 10.1073/pnas.0605938103. View

Robinson G, Fernald R, Clayton D . Genes and social behavior. Science. 2008; 322(5903):896-900. PMC: 3052688. DOI: 10.1126/science.1159277. View

Cummings M, Larkins-Ford J, Reilly C, Wong R, Ramsey M, Hofmann H . Sexual and social stimuli elicit rapid and contrasting genomic responses. Proc Biol Sci. 2007; 275(1633):393-402. PMC: 2212751. DOI: 10.1098/rspb.2007.1454. View

Replogle K, Arnold A, Ball G, Band M, Bensch S, Brenowitz E . The Songbird Neurogenomics (SoNG) Initiative: community-based tools and strategies for study of brain gene function and evolution. BMC Genomics. 2008; 9:131. PMC: 2329646. DOI: 10.1186/1471-2164-9-131. View

Jarvis E . Learned birdsong and the neurobiology of human language. Ann N Y Acad Sci. 2004; 1016:749-77. PMC: 2485240. DOI: 10.1196/annals.1298.038. View

Crabbe J, Wahlsten D, Dudek B . Genetics of mouse behavior: interactions with laboratory environment. Science. 1999; 284(5420):1670-2. DOI: 10.1126/science.284.5420.1670. View

Zhang B, Horvath S . A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol. 2006; 4:Article17. DOI: 10.2202/1544-6115.1128. View

10.

Whitfield C, Ben-Shahar Y, Brillet C, Leoncini I, Crauser D, Leconte Y . Genomic dissection of behavioral maturation in the honey bee. Proc Natl Acad Sci U S A. 2006; 103(44):16068-75. PMC: 1622924. DOI: 10.1073/pnas.0606909103. View

11.

Clayton D, Balakrishnan C, London S . Integrating genomes, brain and behavior in the study of songbirds. Curr Biol. 2009; 19(18):R865-73. PMC: 2890260. DOI: 10.1016/j.cub.2009.07.006. View

12.

Doupe A, Kuhl P . Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci. 1999; 22:567-631. DOI: 10.1146/annurev.neuro.22.1.567. View

13.

Rashotte M, Sedunova E, Johnson F, Pastukhov I . Influence of food and water availability on undirected singing and energetic status in adult male zebra finches (Taeniopygia guttata). Physiol Behav. 2002; 74(4-5):533-41. DOI: 10.1016/s0031-9384(01)00600-x. View

14.

London S, Dong S, Replogle K, Clayton D . Developmental shifts in gene expression in the auditory forebrain during the sensitive period for song learning. Dev Neurobiol. 2009; 69(7):437-50. PMC: 2765821. DOI: 10.1002/dneu.20719. View

15.

Lein E, Hawrylycz M, Ao N, Ayres M, Bensinger A, Bernard A . Genome-wide atlas of gene expression in the adult mouse brain. Nature. 2006; 445(7124):168-76. DOI: 10.1038/nature05453. View

16.

Warren W, Clayton D, Ellegren H, Arnold A, Hillier L, Kunstner A . The genome of a songbird. Nature. 2010; 464(7289):757-62. PMC: 3187626. DOI: 10.1038/nature08819. View

17.

Oldham M, Konopka G, Iwamoto K, Langfelder P, Kato T, Horvath S . Functional organization of the transcriptome in human brain. Nat Neurosci. 2008; 11(11):1271-82. PMC: 2756411. DOI: 10.1038/nn.2207. View

18.

Johnson F, Rashotte M . Food availability but not cold ambient temperature affects undirected singing in adult male zebra finches. Physiol Behav. 2002; 76(1):9-20. DOI: 10.1016/s0031-9384(02)00685-6. View

19.

Su A, Wiltshire T, Batalov S, Lapp H, Ching K, Block D . A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A. 2004; 101(16):6062-7. PMC: 395923. DOI: 10.1073/pnas.0400782101. View

20.

Brenowitz E . Comparative approaches to the avian song system. J Neurobiol. 1997; 33(5):517-31. DOI: 10.1002/(sici)1097-4695(19971105)33:5<517::aid-neu3>3.0.co;2-7. View