Transcriptomic insights into human brain evolution: acceleration, neutrality, heterochrony

Current Opinion in Genetics and Development

Volumn 29, Issue , 2014, Pages 110-119

  Somel, Mehmet ^a   Rohlfs, Rori ^b   Liu, Xiling ^c  

^a MIDDLE EAST TECHNICAL UNIVERSITY   (Turkey)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAX PLANCK INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

BRAIN; BRAIN DEVELOPMENT; COGNITION; DEVELOPMENTAL GENE; EVOLUTION; GENE EXPRESSION; GENETIC VARIABILITY; HUMAN; HUMAN GENETICS; HUMAN VERSUS ANIMAL COMPARISON; METABOLOME; MOLECULAR EVOLUTION; NEUROANATOMY; NONHUMAN; PHENOTYPE; PREFRONTAL CORTEX; REVIEW; SYNAPTOGENESIS; TRANSCRIPTOMICS; ADULT; ANATOMY AND HISTOLOGY; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PAN TROGLODYTES; SPECIES DIFFERENCE;

ADULT; ANIMALS; BIOLOGICAL EVOLUTION; BRAIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, DEVELOPMENTAL; HUMANS; PAN TROGLODYTES; SPECIES SPECIFICITY; TRANSCRIPTOME;

EID: 84908459919     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2014.09.001     Document Type: Review

References (126)

1. Hill K., Barton M., Hurtado A.M. The emergence of human uniqueness: characters underlying behavioral modernity. Evol Anthropol 2009, 18:187-200.
2. Laland K.N., Odling-Smee J., Myles S. How culture shaped the human genome: bringing genetics and the human sciences together. Nat Rev Genet 2010, 11:137-148.
3. Herrmann E., Call J., Hernàndez-Lloreda M.V., Hare B., Tomasello M. Humans have evolved specialized skills of social cognition: the cultural intelligence hypothesis. Science 2007, 317:1360-1366.
4. Inoue S., Matsuzawa T. Working memory of numerals in chimpanzees. Curr Biol 2007, 17:R1004-R1005.
5. Cook P., Wilson M. Do young chimpanzees have extraordinary working memory?. Psychon Bull Rev 2010, 17:599-600.
6. Tennie C., Call J., Tomasello M. Ratcheting up the ratchet: on the evolution of cumulative culture. Philos Trans R Soc Lond B Biol Sci 2009, 364:2405-2415.
7. Sherwood C.C., Bauernfeind A.L., Bianchi S., Raghanti M.A., Hof P.R. Human brain evolution writ large and small. Prog Brain Res 2012, 195:237-254.
8. Rilling J.K. Human and nonhuman primate brains: are they allometrically scaled versions of the same design?. Evol Anthropol 2006, 15:65-77.
9. Geschwind D.H., Rakic P. Cortical evolution: judge the brain by its cover. Neuron 2013, 80:633-647.
10. Prufer K., Racimo F., Patterson N., Jay F., Sankararaman S., Sawyer S., Heinze A., Renaud G., Sudmant P., de Filippo C., et al. The complete genome sequence of a Neanderthal from the Altai mountains. Nature 2013, 505:43-49.
11. Green R.E., Krause J., Briggs A.W., Maricic T., Stenzel U., Kircher M., Patterson N., Li H., Zhai W., Fritz M.H.-Y., et al. A draft sequence of the Neandertal genome. Science 2010, 328:710-722.
12. Reich D., Green R.E., Kircher M., Krause J., Patterson N., Durand E.Y., Viola B., Briggs A.W., Stenzel U., Johnson P.L.F., et al. Genetic history of an archaic hominin group from Denisova cave in Siberia. Nature 2010, 468:1053-1060.
13. Mikkelsen T., Hillier L., Eichler E., Zody M., Jaffe D., Yang S.-P., Enard W., Hellmann I., Lindblad-Toh K., Altheide T., et al. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 2005, 437:69-87.
14. Li C.-Y., Zhang Y., Wang Z., Zhang Y., Cao C., Zhang P.-W., Lu S.-J., Li X.-M., Yu Q., Zheng X., et al. A human-specific de novo protein-coding gene associated with human brain functions. PLoS Comput Biol 2010, 6:e1000734.
15. Knowles D.G., McLysaght A. Recent de novo origin of human protein-coding genes. Genome Res 2009, 19:1752-1759.
16. Wilson M.D., Odom D.T. Evolution of transcriptional control in mammals. Curr Opin Genet Dev 2009, 19:579-585.
17. Carroll S.B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 2008, 134:25-36.
18. Moss E.G. Heterochronic genes and the nature of developmental time. Curr Biol 2007, 17:R425-R434.
19. King M., Wilson A. Evolution at two levels in humans and chimpanzees. Science 1975, 188:107-116.
20. Cáceres M., Lachuer J., Zapala M.A., Redmond J.C., Kudo L., Geschwind D.H., Lockhart D.J., Preuss T.M., Barlow C. Elevated gene expression levels distinguish human from non-human primate brains. Proc Natl Acad Sci U S A 2003, 100:13030-13035.
21. Enard W., Khaitovich P., Klose J., Zollner S., Heissig F., Giavalisco P., Nieselt-Struwe K., Muchmore E., Varki A., Ravid R., et al. Intra- and interspecific variation in primate gene expression patterns. Science 2002, 296:340-343.
22. Uddin M., Wildman D., Liu G., Xu W., Johnson R., Hof P., Kapatos G., Grossman L., Goodman M. Sister grouping of chimpanzees and humans as revealed by genome-wide phylogenetic analysis of brain gene expression profiles. Proc Natl Acad Sci U S A 2004, 101:2957-2962.
23. Khaitovich P., Muetzel B., She X., Lachmann M., Hellmann I., Dietzsch J., Steigele S., Do H.-H., Weiss G., Enard W., et al. Regional patterns of gene expression in human and chimpanzee brains. Genome Res 2004, 14:1462-1473.
24. Khaitovich P., Enard W., Lachmann M., Paabo S. Evolution of primate gene expression. Nat Rev Genet 2006, 7:693-702.
25. Khaitovich P., Hellmann I., Enard W., Nowick K., Leinweber M., Franz H., Weiss G., Lachmann M., Paabo S. Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 2005, 309:1850-1854.
26. Brawand D., Soumillon M., Necsulea A., Julien P., Csárdi G., Harrigan P., Weier M., Liechti A., Aximu-Petri A., Kircher M., et al. The evolution of gene expression levels in mammalian organs. Nature 2011, 478:343-348.
27. Wood J.N. Social cognition and the prefrontal cortex. Behav Cogn Neurosci Rev 2003, 2:97-114.
28. Babbitt C., Fedrigo O., Pfefferle A., Boyle A., Horvath J., Furey T., Wray G. Both noncoding and protein-coding RNAs contribute to gene expression evolution in the primate brain. Genome Biol Evol 2010, 2010:67.
29. Fu X., Giavalisco P., Liu X., Catchpole G., Fu N., Ning Z.-B., Guo S., Yan Z., Somel M., Pääbo S., et al. Rapid metabolic evolution in human prefrontal cortex. Proc Natl Acad Sci U S A 2011, 108:6181-6186.
30. Bozek K., Wei Y., Yan Z., Liu X., Xiong J., Sugimoto M., Tomita M., Pääbo S., Pieszek R., Sherwood C., et al. Exceptional evolutionary divergence of human muscle and brain metabolomes parallels human cognitive and physical uniqueness. PLoS Biol 2014, 12:e1001871EP.
31. Nowick K., Gernat T., Almaas E., Stubbs L. Differences in human and chimpanzee gene expression patterns define an evolving network of transcription factors in brain. Proc Natl Acad Sci U S A 2009, 106:22358-22363.
32. 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, 0605938103.
33. Konopka G., Friedrich T., Davis-Turak J., Winden K., Oldham M.C., Gao F., Chen L., Wang G.-Z., Luo R., Preuss T.M., et al. Human-specific transcriptional networks in the brain. Neuron 2012, 75:601-617.
34. Somel M., Liu X., Tang L., Yan Z., Hu H., Guo S., Jiang X., Zhang X., Xu G., Xie G., et al. MicroRNA-driven developmental remodeling in the brain distinguishes humans from other primates. PLoS Biol 2011, 9:e1001214.
35. Rilling J.K., Insel T.R. Differential expansion of neural projection systems in primate brain evolution. Neuroreport 1999, 10:1453-1460.
36. Miller D.J., Duka T., Stimpson C.D., Schapiro S.J., Baze W.B., McArthur M.J., Fobbs A.J., Sousa A.M.M., Sestan N., Wildman D.E., et al. Prolonged myelination in human neocortical evolution. Proc Natl Acad Sci U S A 2012, 109:16480-16485.
37. Tung J., Barreiro L.B., Johnson Z.P., Hansen K.D., Michopoulos V., Toufexis D., Michelini K., Wilson M.E., Gilad Y. Social environment is associated with gene regulatory variation in the rhesus macaque immune system. Proc Natl Acad Sci U S A 2012, 109:6490-6495.
38. Sherwood C., Stimpson C., Raghanti M., Wildman D., Uddin M., Grossman L., Goodman M., Redmond J., Bonar C., Erwin J., et al. Evolution of increased glia-neuron ratios in the human frontal cortex. Proc Natl Acad Sci U S A 2006, 0605843103.
39. Khaitovich P., Weiss G., Lachmann M., Hellmann I., Enard W., Muetzel B., Wirkner U., Ansorge W., Pääbo S. A neutral model of transcriptome evolution. PLoS Biol 2004, 2:E132.
40. Kimura M. Evolutionary rate at the molecular level. Nature 1968, 217:624-626.
41. Bedford T., Hartl D.L. Optimization of gene expression by natural selection. Proc Natl Acad Sci U S A 2009, 106:1133-1138.
42. Oleksiak M., Churchill G., Crawford D. Variation in gene expression within and among natural populations. Nat Genet 2002, 32:261.
43. Gilad Y., Oshlack A., Smyth G.K., Speed T.P., White K.P. Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature 2006, 440:242-245.
44. Lynch M. The Origins of Genome Architecture 2007, Sinauer Associates.
45. Albert F.W., Somel M., Carneiro M., Aximu-Petri A., Halbwax M., Thalmann O., Blanco-Aguiar J.A., Plyusnina I.Z., Trut L., Villafuerte R., et al. A comparison of brain gene expression levels in domesticated and wild animals. PLoS Genet 2012, 8:e1002962.
46. Lin L., Shen S., Jiang P., Sato S., Davidson B.L., Xing Y. Evolution of alternative splicing in primate brain transcriptomes. Hum Mol Genet 2010, 19:2958-2960.
47. Merkin J., Russell C., Chen P., Burge C.B. Evolutionary dynamics of gene and isoform regulation in mammalian tissues. Science 2012, 338:1593-1600.
48. Li Z., Bammann H., Li M., Liang H., Yan Z., Phoebe Chen Y.-P., Zhao M., Khaitovich P. Evolutionary and ontogenetic changes in RNA editing in human, chimpanzee, and macaque brains. RNA 2013, 19:1693-1702.
49. Shulha H.P., Crisci J.L., Reshetov D., Tushir J.S., Cheung I., Bharadwaj R., Chou H.-J., Houston I.B., Peter C.J., Mitchell A.C., et al. Human-specific histone methylation signatures at transcription start sites in prefrontal neurons. PLoS Biol 2012, 10:e1001427.
50. Khaitovich P., Paabo S., Weiss G. Toward a neutral evolutionary model of gene expression. Genetics 2005, 170:929-939.
51. Chaix R., Somel M., Kreil D.P., Khaitovich P., Lunter G.A. Evolution of primate gene expression: drift and corrective sweeps?. Genetics 2008, 180:1379-1389.
52. Khan Z., Ford M.J., Cusanovich D.A., Mitrano A., Pritchard J.K., Gilad Y. Primate transcript and protein expression levels evolve under compensatory selection pressures. Science 2013, 342:1100-1104.
53. Fraser H.B., Moses A.M., Schadt E.E. Evidence for widespread adaptive evolution of gene expression in budding yeast. Proc Natl Acad Sci U S A 2010, 107:2977-2982.
54. Fraser H.B., Levy S., Chavan A., Shah H.B., Perez J.C., Zhou Y., Siegal M.L., Sinha H. Polygenic cis-regulatory adaptation in the evolution of yeast pathogenicity. Genome Res 2012, 22:1930-1939.
55. Perry G.H., Melsted P., Marioni J.C., Wang Y., Bainer R., Pickrell J.K., Michelini K., Zehr S., Yoder A.D., Stephens M., et al. Comparative RNA sequencing reveals substantial genetic variation in endangered primates. Genome Res 2012, 22:602-610.
56. Konopka G., Geschwind D.H. Human brain evolution: harnessing the genomics (r)evolution to link genes, cognition, and behavior. Neuron 2010, 68:231-244.
57. Somel M., Franz H., Yan Z., Lorenc A., Guo S., Giger T., Kelso J., Nickel B., Dannemann M., Bahn S., et al. Transcriptional neoteny in the human brain. Proc Natl Acad Sci U S A 2009, 106:5743-5748.
58. Somel M., Guo S., Fu N., Yan Z., Hu H.Y., Xu Y., Yuan Y., Ning Z., Hu Y., Menzel C., et al. Microrna, mRNA, and protein expression link development and aging in human and macaque brain. Genome Res 2010, 20:1207-1218.
59. Fraser H., Khaitovich P., Plotkin J., bo S., Eisen M. Aging and gene expression in the primate brain. PLoS Biol 2005, 3.
60. Smith B.H., Crummett T.L., Brandt K.L. Ages of eruption of primate teeth: a compendium for aging individuals and comparing life histories. Am J Phys Anthropol 1994, 37:177-231.
61. Walker R., Hill K., Burger O., Hurtado A.M. Life in the slow lane revisited: ontogenetic separation between chimpanzees and humans. Am J Phys Anthropol 2006, 129:577-583.
62. Gould S. Ontogeny and Phylogeny 1977, Harvard University Press.
63. Shea B. Heterochrony in human evolution: the case for neoteny reconsidered. Am J Phys Anthropol 1989, 32:69-101.
64. Liu X., Somel M., Tang L., Yan Z., Jiang X., Guo S., Yuan Y., He L., Oleksiak A., Zhang Y., et al. Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques. Genome Res 2012, 22:611-622.
65. McLean C.Y., Reno P.L., Pollen A.A., Bassan A.I., Capellini T.D., Guenther C., Indjeian V.B., Lim X., Menke D.B., Schaar B.T., et al. Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 2011, 471:216-219.
66. Charrier C., Joshi K., Coutinho-Budd J., Kim J.-E., Lambert N., de Marchena J., Jin W.-L., Vanderhaeghen P., Ghosh A., Sassa T., et al. Inhibition of srgap2 function by its human-specific paralogs induces neoteny during spine maturation. Cell 2012, 149:923-935.
67. Prabhakar S., Noonan J., Paabo S., Rubin E. Accelerated evolution of conserved noncoding sequences in humans. Science 2006, 314:786-790.
68. Pollard K., Salama S., King B., Kern A., Dreszer T., Katzman S., Siepel A., Pedersen J., Bejerano G., Baertsch R., et al. Forces shaping the fastest evolving regions in the human genome. PLoS Genet 2006, 2:e168.
69. Nowick K., Hamilton A.T., Zhang H., Stubbs L. Rapid sequence and expression divergence suggest selection for novel function in primate-specific KRAB-ZNF genes. Mol Biol Evol 2010, 27:2606-2610.
70. Zhang Y.E., Landback P., Vibranovski M.D., Long M. Accelerated recruitment of new brain development genes into the human genome. PLoS Biol 2011, 9:e1001179.
71. Hu H.Y., He L., Fominykh K., Yan Z., Guo S., Zhang X., Taylor M.S., Tang L., Li J., Liu J., et al. Evolution of the human-specific microRNA miR-941. Nat Commun 2012, 3:1145.
72. Haygood R., Fedrigo O., Hanson B., Yokoyama K.-D., Wray G.A. Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nat Genet 2007, 39:1140-1144.
73. Giger T., Khaitovich P., Somel M., Lorenc A., Lizano E., Harris L., Ryan M., Lan M., Wayland M., Bahn S., et al. Evolution of neuronal and endothelial transcriptomes in primates. Genome Biol Evol 2010, evq018:v011.
74. Pollard K., Salama S., Lambert N., Lambot M.-A., Coppens S., Pedersen J., Katzman S., King B., Onodera C., Siepel A., et al. An RNA gene expressed during cortical development evolved rapidly in humans. Nature 2006, 443:167-172.
75. Prabhakar S., Visel A., Akiyama J., Shoukry M., Lewis K., Holt A., Plajzer-Frick I., Morrison H., FitzPatrick D., Afzal V., et al. Human-specific gain of function in a developmental enhancer. Science 2008, 321:1346-1350.
76. Zeder M.A. Pathways to animal domestication. Biodiversity in Agriculture: Domestication, Evolution, and Sustainability 2012, Cambridge University Press. P. Gepts, T.R. Famula, R.L. Bettinger (Eds.).
77. Seid M., Wehner R. Delayed axonal pruning in the ant brain: a study of developmental trajectories. Dev Neurobiol 2009, 69:350-364.
78. Hsieh W.-P., Chu T.-M., Wolfinger R., Gibson G. Mixed-model reanalysis of primate data suggests tissue and species biases in oligonucleotide-based gene expression profiles. Genetics 2003, 165:747-757.
79. Nuzhdin S.V., Wayne M.L., Harmon K.L., McIntyre L.M. Common pattern of evolution of gene expression level and protein sequence in Drosophila. Mol Biol Evol 2004, 21:1308-1317.
80. Yanai I., Graur D., Ophir R. Incongruent expression profiles between human and mouse orthologous genes suggest widespread neutral evolution of transcription control. OMICS: J Integr Biol 2004, 8:15-24.
81. Lemos B., Meiklejohn C., Caceres M., Hartl D. Rates of divergence in gene expression profiles of primates, mice, and flies: stabilizing selection and variability among functional categories. Evolution 2005, 59:126-137.
82. Khaitovich P., Kelso J., Franz H., Visagie J., Giger T., Joerchel S., Petzold E., Green R., Lachmann M., bo S. Functionality of intergenic transcription: an evolutionary comparison. PLoS Genet 2006, 2:e171.
83. Whitehead A., Crawford D. Variation within and among species in gene expression: raw material for evolution. Mol Ecol 2006, 15:1197-1211.
84. Felsenstein J. Phylogenies and the comparative method. Am Nat 1985, 1-15.
85. Hansen T.F. Stabilizing selection and the comparative analysis of adaptation. Evolution 1997, 51:1341-1351.
86. Butler M.A., King A.A. Phylogenetic comparative analysis: a modeling approach for adaptive evolution. Am Nat 2004, 164:683-695.
87. Hansen T.F., Pienaar J., Orzack S.H. A comparative method for studying adaptation to a randomly evolving environment. Evolution 2008, 62:1965-1977.
88. O'Meara B.C., Beaulieu J.M. Modelling stabilizing selection: the attraction of Ornstein-Uhlenbeck models. Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology 2014, Springer-Verlag. L.Z. Garamszegi (Ed.).
89. Rohlfs R.V., Harrigan P., Nielsen R. Modeling gene expression evolution with an extended Ornstein-Uhlenbeck process accounting for within-species variation. Mol Biol Evol 2014, 31:201-211.
90. Kalinka A.T., Varga K.M., Gerrard D.T., Preibisch S., Corcoran D.L., Jarrells J., Ohler U., Bergman C.M., Tomancak P. Gene expression divergence recapitulates the developmental hourglass model. Nature 2010, 468:811-814.
91. Rohlfs R., Nielsen R. Identifying adaptive and plastic gene expression levels using a unified model for expression variance between and within species. bioRxiv 2014.
92. Gruber J.D., Vogel K., Kalay G., Wittkopp P.J. Contrasting properties of gene-specific regulatory, coding, and copy number mutations in saccharomyces cerevisiae: frequency, effects, and dominance. PLoS Genet 2012, 8:e1002497.
93. Huttenlocher P.R., Dabholkar A.S. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 1997, 387:167-178.
94. Huttenlocher P.R., de Courten C., Garey L.J., Van der Loos H. Synaptogenesis in human visual cortex-evidence for synapse elimination during normal development. Neurosci Lett 1982, 33:247-252.
95. Bianchi S., Stimpson C.D., Duka T., Larsen M.D., Janssen W.G.M., Collins Z., Bauernfeind A.L., Schapiro S.J., Baze W.B., McArthur M.J., et al. Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans. Proc Natl Acad Sci U S A 2013, 110(Suppl2):10395-10401.
96. Goyal M.S., Hawrylycz M., Miller J.A., Snyder A.Z., Raichle M.E. Aerobic glycolysis in the human brain is associated with development and neotenous gene expression. Cell Metab 2014, 19:49-57.
97. Bogin B. Evolutionary hypotheses for human childhood. Yearb Phys Anthropol 1997, 40:63-89.
98. Johnson M. Functional brain development in humans. Nat Rev Neurosci 2001, 2:475-483.
99. de Graaf-Peters V.B., Hadders-Algra M. Ontogeny of the human central nervous system: what is happening when?. Early Hum Dev 2006, 82:257-266.
100. Bufill E., Agustí J., Blesa R. Human neoteny revisited: the case of synaptic plasticity. Am J Hum Biol 2011, 23:729-739.
101. Shalizi A., Gaudillière B., Yuan Z., Stegmüller J., Shirogane T., Ge Q., Tan Y., Schulman B., Harper J.W., Bonni A. A calcium-regulated mef2 sumoylation switch controls postsynaptic differentiation. Science 2006, 311:1012-1017.
102. Flavell S.W., Cowan C.W., Kim T.-K., Greer P.L., Lin Y., Paradis S., Griffith E.C., Hu L.S., Chen C., Greenberg M.E. Activity-dependent regulation of mef2 transcription factors suppresses excitatory synapse number. Science 2006, 311:1008-1012.
103. Somel M., Liu X., Khaitovich P. Human brain evolution: transcripts, metabolites and their regulators. Nat Rev Neurosci 2013, 14:112-127.
104. Fisher S.E., Ridley M. Evolution. Culture, genes, and the human revolution. Science 2013, 340:929-930.
105. Herculano-Houzel S. The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost. Proc Natl Acad Sci U S A 2012, 109(Suppl1):10661-10668.
106. Rilling J.K., Insel T.R. The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 1999, 37:191-223.
107. Rilling J.K., Seligman R.A. A quantitative morphometric comparative analysis of the primate temporal lobe. J Hum Evol 2002, 42:505-533.
108. Schenker N.M., Hopkins W.D., Spocter M.A., Garrison A.R., Stimpson C.D., Erwin J.M., Hof P.R., Sherwood C.C. Broca's area homologue in chimpanzees (pan troglodytes): probabilistic mapping, asymmetry, and comparison to humans. Cereb Cortex 2010, 20:730-742.
109. Rilling J.K., Glasser M.F., Preuss T.M., Ma X., Zhao T., Hu X., Behrens T.E.J. The evolution of the arcuate fasciculus revealed with comparative dti. Nat Neurosci 2008, 11:426-428.
110. Li L., Hu X., Preuss T.M., Glasser M.F., Damen F.W., Qiu Y., Rilling J. Mapping putative hubs in human, chimpanzee and rhesus macaque connectomes via diffusion tractography. Neuroimage 2013, 80:462-474.
111. Nimchinsky E.A., Gilissen E., Allman J.M., Perl D.P., Erwin J.M., Hof P.R. A neuronal morphologic type unique to humans and great apes. Proc Natl Acad Sci U S A 1999, 96:5268-5273.
112. Semendeferi K., Teffer K., Buxhoeveden D.P., Park M.S., Bludau S., Amunts K., Travis K., Buckwalter J. Spatial organization of neurons in the frontal pole sets humans apart from great apes. Cereb Cortex 2010, 21:1485-1497.
113. Spocter M.A., Hopkins W.D., Barks S.K., Bianchi S., Hehmeyer A.E., Anderson S.M., Stimpson C.D., Fobbs A.J., Hof P.R., Sherwood C.C. Neuropil distribution in the cerebral cortex differs between humans and chimpanzees. J Comp Neurol 2012, 520:2917-2929.
114. Teffer K., Buxhoeveden D.P., Stimpson C.D., Fobbs A.J., Schapiro S.J., Baze W.B., McArthur M.J., Hopkins W.D., Hof P.R., Sherwood C.C., et al. Developmental changes in the spatial organization of neurons in the neocortex of humans and common chimpanzees. J Comp Neurol 2013, 521:4249-4259.
115. Schenker N.M., Buxhoeveden D.P., Blackmon W.L., Amunts K., Zilles K., Semendeferi K. A comparative quantitative analysis of cytoarchitecture and minicolumnar organization in broca's area in humans and great apes. J Comp Neurol 2008, 510:117-128.
116. Buxhoeveden D.P., Switala A.E., Litaker M., Roy E., Casanova M.F. Lateralization of minicolumns in human planum temporale is absent in nonhuman primate cortex. Brain Behav Evol 2001, 57:349-358.
117. Bianchi S., Stimpson C.D., Bauernfeind A.L., Schapiro S.J., Baze W.B., McArthur M.J., Bronson E., Hopkins W.D., Semendeferi K., Jacobs B., et al. Dendritic morphology of pyramidal neurons in the chimpanzee neocortex: regional specializations and comparison to humans. Cereb Cortex 2013, 23:2429-2436.
118. Allman J.M., Tetreault N.A., Hakeem A.Y., Manaye K.F., Semendeferi K., Erwin J.M., Park S., Goubert V., Hof P.R. The von economo neurons in the frontoinsular and anterior cingulate cortex. Ann N Y Acad Sci 2011, 1225:59-71.
119. Sakai T., Hirata S., Fuwa K., Sugama K., Kusunoki K., Makishima H., Eguchi T., Yamada S., Ogihara N., Takeshita H. Fetal brain development in chimpanzees versus humans. Curr Biol 2012, 22:R791-R792.
120. Leigh S.R. Brain growth, life history, and cognition in primate and human evolution. Am J Primatol 2004, 62:139-164.
121. Sakai T., Mikami A., Tomonaga M., Matsui M., Suzuki J., Hamada Y., Tanaka M., Miyabe-Nishiwaki T., Makishima H., Nakatsukasa M., et al. Differential prefrontal white matter development in chimpanzees and humans. Curr Biol 2011, 21:1397-1402.
122. Chen X., Errangi B., Li L., Glasser M.F., Westlye L.T., Fjell A.M., Walhovd K.B., Hu X., Herndon J.G., Preuss T.M., et al. Brain aging in humans, chimpanzees (Pan troglodytes), and rhesus macaques (Macaca mulatta): magnetic resonance imaging studies of macro- and microstructural changes. Neurobiol Aging 2013, 34:2248-2260.
123. Sherwood C.C., Gordon A.D., Allen J.S., Phillips K.A., Erwin J.M., Hof P.R., Hopkins W.D. Aging of the cerebral cortex differs between humans and chimpanzees. Proc Natl Acad Sci U S A 2011, 108:13029-13034.
124. Rilling J.K., Barks S.K., Parr L.A., Preuss T.M., Faber T.L., Pagnoni G., Bremner J.D., Votaw J.R. A comparison of resting-state brain activity in humans and chimpanzees. Proc Natl Acad Sci U S A 2007, 104:17146-17151.
125. Duka T., Anderson S.M., Collins Z., Raghanti M.A., Ely J.J., Hof P.R., Wildman D.E., Goodman M., Grossman L.I., Sherwood C.C. Synaptosomal lactate dehydrogenase isoenzyme composition is shifted toward aerobic forms in primate brain evolution. Brain Behav Evol 2014, 83:216-230.
126. Fedrigo O., Pfefferle A.D., Babbitt C.C., Haygood R., Wall C.E., Wray G.A. A potential role for glucose transporters in the evolution of human brain size. Brain Behav Evol 2011, 78:315-326.