Skip to main content
Top
Published in: Brain Structure and Function 7/2017

01-09-2017 | Original Article

Interhemispheric gene expression differences in the cerebral cortex of humans and macaque monkeys

Authors: Gerard Muntané, Gabriel Santpere, Andrey Verendeev, William W. Seeley, Bob Jacobs, William D. Hopkins, Arcadi Navarro, Chet C. Sherwood

Published in: Brain Structure and Function | Issue 7/2017

Login to get access

Abstract

Handedness and language are two well-studied examples of asymmetrical brain function in humans. Approximately 90% of humans exhibit a right-hand preference, and the vast majority shows left-hemisphere dominance for language function. Although genetic models of human handedness and language have been proposed, the actual gene expression differences between cerebral hemispheres in humans remain to be fully defined. In the present study, gene expression profiles were examined in both hemispheres of three cortical regions involved in handedness and language in humans and their homologues in rhesus macaques: ventrolateral prefrontal cortex, posterior superior temporal cortex (STC), and primary motor cortex. Although the overall pattern of gene expression was very similar between hemispheres in both humans and macaques, weighted gene correlation network analysis revealed gene co-expression modules associated with hemisphere, which are different among the three cortical regions examined. Notably, a receptor-enriched gene module in STC was particularly associated with hemisphere and showed different expression levels between hemispheres only in humans.
Appendix
Available only for authorised users
Literature
go back to reference Atabay MM, Oz ZS, Kurtman E (2014) The association between dopamine receptor (DRD4) gene polymorphisms and second language learning style and behavioral variability in undergraduate students in Turkey. Mol Biol Rep 41:5215–5220. doi:10.1007/s11033-014-3389-x CrossRef Atabay MM, Oz ZS, Kurtman E (2014) The association between dopamine receptor (DRD4) gene polymorphisms and second language learning style and behavioral variability in undergraduate students in Turkey. Mol Biol Rep 41:5215–5220. doi:10.​1007/​s11033-014-3389-x CrossRef
go back to reference Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264–278. doi:10.1523/JNEUROSCI.4178-07.2008 CrossRefPubMed Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264–278. doi:10.​1523/​JNEUROSCI.​4178-07.​2008 CrossRefPubMed
go back to reference Cashmore L, Uomini N, Chapelain A (2008) The evolution of handedness in humans and great apes: a review and current issues. J Anthropol Sci Riv Antropol JASS Ist Ital Antropol 86:7–35 Cashmore L, Uomini N, Chapelain A (2008) The evolution of handedness in humans and great apes: a review and current issues. J Anthropol Sci Riv Antropol JASS Ist Ital Antropol 86:7–35
go back to reference Corballis MC (2003) From mouth to hand: gesture, speech, and the evolution of right-handedness. Behav Brain Sci 26:199–208 (discussion 208–260) PubMed Corballis MC (2003) From mouth to hand: gesture, speech, and the evolution of right-handedness. Behav Brain Sci 26:199–208 (discussion 208–260) PubMed
go back to reference Dapretto M, Bookheimer SY (1999) Form and content: dissociating syntax and semantics in sentence comprehension. Neuron 24:427–432CrossRefPubMed Dapretto M, Bookheimer SY (1999) Form and content: dissociating syntax and semantics in sentence comprehension. Neuron 24:427–432CrossRefPubMed
go back to reference De la Fuente-Fernández R, Kishore A, Calne DB, Ruth TJ, Stoessl AJ (2000) Nigrostriatal dopamine system and motor lateralization. Behav Brain Res 112:63–68CrossRefPubMed De la Fuente-Fernández R, Kishore A, Calne DB, Ruth TJ, Stoessl AJ (2000) Nigrostriatal dopamine system and motor lateralization. Behav Brain Res 112:63–68CrossRefPubMed
go back to reference Eicher JD, Powers NR, Miller LL, Akshoomoff N, Amaral DG, Bloss CS, Libiger O, Schork NJ, Darst BF, Casey BJ et al (2013) Genome-wide association study of shared components of reading disability and language impairment. Genes Brain Behav 12:792–801. doi:10.1111/gbb.12085 CrossRefPubMedPubMedCentral Eicher JD, Powers NR, Miller LL, Akshoomoff N, Amaral DG, Bloss CS, Libiger O, Schork NJ, Darst BF, Casey BJ et al (2013) Genome-wide association study of shared components of reading disability and language impairment. Genes Brain Behav 12:792–801. doi:10.​1111/​gbb.​12085 CrossRefPubMedPubMedCentral
go back to reference Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5(10):R80 (Epub 2004 Sep 15) CrossRefPubMedPubMedCentral Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5(10):R80 (Epub 2004 Sep 15) CrossRefPubMedPubMedCentral
go back to reference Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S (eds) (2005) Bioinformatics and computational biology solutions using R and bioconductor, statistics for biology and health. Springer New York, New York Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S (eds) (2005) Bioinformatics and computational biology solutions using R and bioconductor, statistics for biology and health. Springer New York, New York
go back to reference Gilbert SL, Dobyns WB, Lanh BT (2005) Genetic links between brain development and brain evolution. Nat Rev Genet 6(7):581–590CrossRefPubMed Gilbert SL, Dobyns WB, Lanh BT (2005) Genetic links between brain development and brain evolution. Nat Rev Genet 6(7):581–590CrossRefPubMed
go back to reference Gil-da-Costa R, Martin A, Lopes M a, Muñoz M, Fritz JB, Braun AR (2006) Species-specific calls activate homologs of Broca’s and Wernicke’s areas in the macaque. Nat Neurosci 9:1064–1070CrossRefPubMed Gil-da-Costa R, Martin A, Lopes M a, Muñoz M, Fritz JB, Braun AR (2006) Species-specific calls activate homologs of Broca’s and Wernicke’s areas in the macaque. Nat Neurosci 9:1064–1070CrossRefPubMed
go back to reference Groen MA, Whitehouse AJO, Badcock NA, Bishop DVM (2012) Does cerebral lateralization develop? A study using functional transcranial Doppler ultrasound assessing lateralization for language production and visuospatial memory. Brain Behav 2:256–269. doi:10.1002/brb3.56 CrossRefPubMedPubMedCentral Groen MA, Whitehouse AJO, Badcock NA, Bishop DVM (2012) Does cerebral lateralization develop? A study using functional transcranial Doppler ultrasound assessing lateralization for language production and visuospatial memory. Brain Behav 2:256–269. doi:10.​1002/​brb3.​56 CrossRefPubMedPubMedCentral
go back to reference Hibar DP, Stein JL, Renteria ME, Arias-Vasquez A, Desrivières S, Jahanshad N, Toro R, Wittfeld K, Abramovic L, Andersson M, et al (2015) Common genetic variants influence human subcortical brain structures. Nature 520(7546):224–229. doi:10.1038/nature14101 CrossRefPubMedPubMedCentral Hibar DP, Stein JL, Renteria ME, Arias-Vasquez A, Desrivières S, Jahanshad N, Toro R, Wittfeld K, Abramovic L, Andersson M, et al (2015) Common genetic variants influence human subcortical brain structures. Nature 520(7546):224–229. doi:10.​1038/​nature14101 CrossRefPubMedPubMedCentral
go back to reference Hopkins WD, Leavens DA (1998) Hand use and gestural communication in chimpanzees (Pan troglodytes). J Comp Psychol Wash DC 1983 112:95–99. Hopkins WD, Leavens DA (1998) Hand use and gestural communication in chimpanzees (Pan troglodytes). J Comp Psychol Wash DC 1983 112:95–99.
go back to reference Hopkins WD, Russell JL, Cantalupo C, Freeman H, Schapiro SJ (2005). Factors influencing the prevalence and handedness for throwing in captive chimpanzees (Pan troglodytes). J Comp Psychol. Wash DC 1983 119:363–370. doi:10.1037/0735-7036.119.4.363 Hopkins WD, Russell JL, Cantalupo C, Freeman H, Schapiro SJ (2005). Factors influencing the prevalence and handedness for throwing in captive chimpanzees (Pan troglodytes). J Comp Psychol. Wash DC 1983 119:363–370. doi:10.​1037/​0735-7036.​119.​4.​363
go back to reference Hugdahl K, Westerhausen R (2012) The two halves of the brain, Ed: New. ed. The MIT Press Hugdahl K, Westerhausen R (2012) The two halves of the brain, Ed: New. ed. The MIT Press
go back to reference Karlebach G, Francks C (2015) Lateralization of gene expression in human language cortex. Cortex 67:30–36CrossRefPubMed Karlebach G, Francks C (2015) Lateralization of gene expression in human language cortex. Cortex 67:30–36CrossRefPubMed
go back to reference Medland SE, Duffy DL, Spurdle AB, Wright MJ, Geffen GM, Montgomery GW, Martin NG (2005) Opposite effects of androgen receptor CAG repeat length on increased risk of left-handedness in males and females. Behav Genet 35:735–744. doi:10.1007/s10519-005-6187-3 CrossRefPubMed Medland SE, Duffy DL, Spurdle AB, Wright MJ, Geffen GM, Montgomery GW, Martin NG (2005) Opposite effects of androgen receptor CAG repeat length on increased risk of left-handedness in males and females. Behav Genet 35:735–744. doi:10.​1007/​s10519-005-6187-3 CrossRefPubMed
go back to reference Nudel R, Simpson NH, Baird G, O’Hare A, Conti-Ramsden G, Bolton PF, Hennessy ER, SLI Consortium, Ring SM, Davey Smith G et al (2014) Genome-wide association analyses of child genotype effects and parent-of-origin effects in specific language impairment. Genes Brain Behav 13:418–429. doi:10.1111/gbb.12127 CrossRefPubMedPubMedCentral Nudel R, Simpson NH, Baird G, O’Hare A, Conti-Ramsden G, Bolton PF, Hennessy ER, SLI Consortium, Ring SM, Davey Smith G et al (2014) Genome-wide association analyses of child genotype effects and parent-of-origin effects in specific language impairment. Genes Brain Behav 13:418–429. doi:10.​1111/​gbb.​12127 CrossRefPubMedPubMedCentral
go back to reference Ocklenburg S, Ströckens F, Güntürkün O (2013a) Lateralisation of conspecific vocalisation in non-human vertebrates. Laterality 18:1–31CrossRefPubMed Ocklenburg S, Ströckens F, Güntürkün O (2013a) Lateralisation of conspecific vocalisation in non-human vertebrates. Laterality 18:1–31CrossRefPubMed
go back to reference Rudy J, Valafar F (2011) Empirical comparison of cross-platform normalization methods for gene expression data. BMC Bioinformatics Dec 7(12):467CrossRef Rudy J, Valafar F (2011) Empirical comparison of cross-platform normalization methods for gene expression data. BMC Bioinformatics Dec 7(12):467CrossRef
go back to reference Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3, Article3. doi:10.2202/1544-6115.1027 Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3, Article3. doi:10.​2202/​1544-6115.​1027
go back to reference Spinozzi G (2007) Factors Affecting Manual Laterality in Tufted Capuchins (Cebus Apella). In: Hopkins WD (ed), Special topics in primatology, the evolution of hemispheric specialization in primates. Elsevier, Amsterdam, pp 204–226CrossRef Spinozzi G (2007) Factors Affecting Manual Laterality in Tufted Capuchins (Cebus Apella). In: Hopkins WD (ed), Special topics in primatology, the evolution of hemispheric specialization in primates. Elsevier, Amsterdam, pp 204–226CrossRef
go back to reference Spocter MA, Hopkins WD, Garrison AR, Bauernfeind AL, Stimpson CD, Hof PR, Sherwood CC (2010) Wernicke’s area homologue in chimpanzees (Pan troglodytes) and its relation to the appearance of modern human language. Proc R Soc Lond B Biol Sci. doi:10.1098/rspb.2010.0011 Spocter MA, Hopkins WD, Garrison AR, Bauernfeind AL, Stimpson CD, Hof PR, Sherwood CC (2010) Wernicke’s area homologue in chimpanzees (Pan troglodytes) and its relation to the appearance of modern human language. Proc R Soc Lond B Biol Sci. doi:10.​1098/​rspb.​2010.​0011
go back to reference Vauclair J, Meguerditchian A (2007) Perceptual and Motor lateralization in two species of baboons. In: Hopkins WD (ed), Special topics in primatology, the evolution of hemispheric specialization in primates. Elsevier, Amsterdam, pp 182–202CrossRef Vauclair J, Meguerditchian A (2007) Perceptual and Motor lateralization in two species of baboons. In: Hopkins WD (ed), Special topics in primatology, the evolution of hemispheric specialization in primates. Elsevier, Amsterdam, pp 182–202CrossRef
go back to reference Wernicke C (1874) Der aphasische symptomencomplex: eine psychologische studie auf anatomischer basis. Cohn. Wernicke C (1874) Der aphasische symptomencomplex: eine psychologische studie auf anatomischer basis. Cohn.
go back to reference Wilson B, Kikuchi Y, Sun L, Hunter D, Dick F, Smith K, Thiele A, Griffiths TD, Marslen-Wilson WD, Petkov CI (2015) Auditory sequence processing reveals evolutionarily conserved regions of frontal cortex in macaques and humans. Nat Commun 6:8901CrossRefPubMedPubMedCentral Wilson B, Kikuchi Y, Sun L, Hunter D, Dick F, Smith K, Thiele A, Griffiths TD, Marslen-Wilson WD, Petkov CI (2015) Auditory sequence processing reveals evolutionarily conserved regions of frontal cortex in macaques and humans. Nat Commun 6:8901CrossRefPubMedPubMedCentral
go back to reference Xiao L, Jordan CL (2002) Sex differences, laterality, and hormonal regulation of androgen receptor immunoreactivity in rat hippocampus. Horm Behav 42:327–336CrossRefPubMed Xiao L, Jordan CL (2002) Sex differences, laterality, and hormonal regulation of androgen receptor immunoreactivity in rat hippocampus. Horm Behav 42:327–336CrossRefPubMed
Metadata
Title
Interhemispheric gene expression differences in the cerebral cortex of humans and macaque monkeys
Authors
Gerard Muntané
Gabriel Santpere
Andrey Verendeev
William W. Seeley
Bob Jacobs
William D. Hopkins
Arcadi Navarro
Chet C. Sherwood
Publication date
01-09-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 7/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1401-7

Other articles of this Issue 7/2017

Brain Structure and Function 7/2017 Go to the issue