The prefrontal cortex is commonly associated with cognitive capacities related to human uniqueness: purposeful actions towards higher-level goals, complex social information processing, introspection, and language. Comparative investigations of the prefrontal cortex may thus shed more light on the neural underpinnings of what makes us human. Using histological data from 19 anthropoid primate species (6 apes including humans and 13 monkeys), we investigate cross-species relative size changes along the anterior (prefrontal) and posterior (motor) axes of the cytoarchitectonically defined frontal lobe in both hemispheres. Results reveal different scaling coefficients in the left versus right prefrontal hemisphere, suggest that the primary factor underlying the evolution of primate brain architecture is left hemispheric prefrontal hyperscaling, and indicate that humans are the extreme of a left prefrontal ape specialization in relative white to grey matter volume. These results demonstrate a neural adaptive shift distinguishing the ape from the monkey radiation possibly related to a cognitive grade shift between (great) apes and other primates.

1.
Adolphs R (2009): The social brain: neural basis of social knowledge. Annu Rev Psychol 60:693–716.
[PubMed]
2.
Amunts K, Jancke L, Mohlberg H, Steinmetz H, Zilles K (1998): Interhemispheric asymmetry in the human motor cortex and handedness. Eur J Neurosci 10:15402.
3.
Amunts K, Jancke L, Mohlberg H, Steinmetz H, Zilles K (2000): Interhemispheric asymmetry of the human motor cortex related to handedness and gender. Neuropsychologia 38:304–312.
[PubMed]
4.
Amunts K, Schleicher A, Burgel U, Mohlberg H, Uylings HBM, Zilles K (1999): Broca’s region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 412:319–341.
[PubMed]
5.
Asplund CL, Todd JJ, Snyder AP, Marois R (2010): A central role for the lateral prefrontal cortex in goal-direct and stimulus-driven attention. Nat Neurosci 13:507–514.
[PubMed]
6.
Berkman ET, Lieberman MD (2010): Approaching the bad and avoiding the good: lateral prefrontal cortical asymmetry distinguishes between action and valence. J Cogn Neurosci 22:1970–1979.
[PubMed]
7.
Blinkov SM, Glezer II (1968): Das Zentralnervensystem in Zahlen und Tabellen. Jena, Fischer.
8.
Brodmann K (1912): Neue Ergebnisse über die vergleichende histologische Lokalisation der Grosshirnrinde mit besonderer Berücksichtigung des Stirnhirns. Anat Anz 41:157–216.
9.
Bush EC, Allman JM (2004): The scaling of frontal cortex in primates and carnivores. Proc Natl Acad Sci USA 101:3962–3966.
[PubMed]
10.
Carreiras M, Seghier ML, Baquero S, Estevez A, Lozano A, Devlin JT, Price JC (2009): An anatomical signature for literacy. Nature 461:983–986.
[PubMed]
11.
Catani M, Forkel S, Thiebaut de Schotten M (2010): Asymmetry of the white matter pathways in the brain; in Hugdahl K, Westerhausen R (eds): The Two Halves of the Brain: Information Processing in the Cerebral Hemispheres. Cambridge, MIT Press.
12.
Corbetta M, Shulman GL (2002): Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215.
[PubMed]
13.
Dadda M, Cantalupo C, Hopkins WD (2008): An association between handedness and neuroanatomical asymmetries in chimpanzees (Pan troglodytes): evidence from the primary motor cortex. Folia Primatol 79:141–142.
14.
Deacon TW (1997): The Symbolic Species. New York, Norton.
15.
DeVoogd T, Krebs JR, Healy SD, Purvis A (1993): Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses among oscine birds. Proc R Soc B Biol Sci 254:75–82.
[PubMed]
16.
Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A (2004): Changes in grey matter induced by training. Nature 427:311–312.
[PubMed]
17.
Dunbar RIM (1996): Grooming, Gossip and the Evolution of Language. London, Faber & Faber.
18.
Dunbar RIM, Shultz S (2007): Understanding primate brain evolution. Philos Trans R Soc B Biol Sci 362:649–658.
[PubMed]
19.
Falk D, Hildebolt C, Cheverud J, Vannier M, Helmkamp RC, Konigsberg L (1990): Cortical asymmetries in frontal lobes of rhesus monkeys (Macaca mulatta). Brain Res 512:40–45.
[PubMed]
20.
Fleming SM, Weil RS, Nagy Z, Dolan RJ, Rees G (2010): Relating introspective accuracy to individual differences in brain structure. Science 329:1541–1543.
[PubMed]
21.
Freckleton RP, Harvey PH, Pagel M (2002): Phylogenetic analysis and comparative data: a test and review of evidence. Am Naturalist 160:712–726.
[PubMed]
22.
Gage MJG, Freckleton RP (2003): Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proc R Soc Lond Ser B Biol Sci 270:625–632.
[PubMed]
23.
Geyer S, Schleicher A, Zilles K (1999): Areas 3a, 3b, and 1 of human primary somatosensory cortex 1. Microstructural organization and interindividual variability. Neuroimage 10:63–83.
[PubMed]
24.
Gray JR, Thompson PM (2004): Neurobiology of intelligence: science and ethics. Nat Rev Neurosci 5:471–482.
[PubMed]
25.
Harvey PH, Pagel MD (1991): The Comparative Method in Evolutionary Biology. Oxford, Oxford University Press.
26.
Heilbroner PL, Holloway RL (1989): Anatomical brain asymmetry in monkeys: frontal, temporoparietal, and limbic cortex in Macaca. Am J Phys Anthropol 80:203–211.
[PubMed]
27.
Holloway RL (2002): How much larger is the relative volume of area 10 of the prefrontal cortex in humans? Am J Phys Anthropol 118:399–401.
[PubMed]
28.
Hopkins WD (ed) (2007): Evolution of Hemispheric Specialization in Primates. London, Academic Press.
29.
Hopkins WD, Cantalupo C, Taglialatela J (2007a): Handedness is associated with asymmetries in gyrification of the cerebral cortex of chimpanzees. Cereb Cortex 17:1750–1756.
[PubMed]
30.
Hopkins WD, Dunham L, Cantalupo C, Taglialatela JT (2007b): The relationship between handedness, brain asymmetries and corpus callosum size in chimpanzees (Pan troglodytes). Cereb Cortex 17:1757–1765.
[PubMed]
31.
Hopkins WD, Taglialatela JP, Dunham L, Pierre P (2007c): Behavioral and neuroanatomical correlates of white matter asymmetries in chimpanzees (Pan troglodytes). Eur J Neurosci 25:2565–2570.
[PubMed]
32.
Hopkins WD, Taglialatela JP, Megeurditchian A, Nir T, Schenker NM, Sherwood CC (2008): Gray matter asymmetries in chimpanzees as revealed by voxel-based morphology. Neuroimage 42:491–497.
[PubMed]
33.
Huber R, van Staaden MJ, Kaufman LS, Liem KF (1997): Microhabitat use, trophic patterns, and the evolution of brain structure in African cichlids. Brain Behav Evol 50:167–182.
[PubMed]
34.
Hugdahl K, Westerhausen R (eds) (2010): The Two Halves of the Brain: Information Processing in the Cerebral Hemispheres. Cambridge, MIT Press.
35.
Iwaniuk AN, Wylie DRW (2007): Neural specialization for hovering in hummingbirds: hypertrophy of the pretectal nucleus lentiformis mesencephali. J Comp Neurol 500:211–221.
[PubMed]
36.
Jerison HJ (1997): Evolution of prefrontal cortex; in Krasnegor NA, Lyon R, Goldman-Rakic PS (eds): Development of the Prefrontal Cortex: Evolution, Neurobiology, and Behavior. Baltimore, Paul H. Brookes, pp 9–26.
37.
Jerison HJ (2007): Evolution of the frontal lobes; in Miller BL, Cummings JL (eds): The Human Frontal Lobes: Functions and Disorders. New York, The Guilford Press.
38.
Johnson-Frey SH (2004): The neural bases of complex tool use in humans. Trends Cogn Sci 8:71–78.
[PubMed]
39.
Kaas JH (2006): Evolution of the neocortex. Curr Biol 16:R910–R914.
[PubMed]
40.
Lindenfors P (2005): Neocortex evolution in primates: the ‘social brain’ is for females. Biol Lett 1:407–410.
[PubMed]
41.
Lindenfors P, Nunn CL, Barton RA (2007): Primate brain architecture and selection in relation to sex. BMC Biol 5:20.
[PubMed]
42.
Marchant LF, McGrew WC, Eibl-Eibesfeldt I (1995): Is human handedness universal? Ethological analyses from three traditional cultures. Ethology 101:239–258.
43.
Martins EP, Hansen TF (1997): Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Naturalist 149:646–667.
44.
Matelli M, Luppino G, Geyer S, Zilles K (2004): Motor cortex; in Paxinos G, Mai JK (eds): The Human Nervous System. Amsterdam, Elsevier Academic Press, pp 975–996.
45.
McBride T, Arnold SE, Gur RC (1999): A comparative volumetric analysis of the prefrontal cortex in human and baboon MRI. Brain Behav Evol 54:159–166.
[PubMed]
46.
Miller EK, Cohen JD (2001): An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202.
[PubMed]
47.
Pagel M (1999): Inferring the historical patterns of biological evolution. Nature 401:877–884.
[PubMed]
48.
Paradis E, Claude J, Strimmer K (2004): APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290.
[PubMed]
49.
Passingham RE (1973): Anatomical differences between the neocortex of man and other primates. Brain Behav Evol 7:337–359.
[PubMed]
50.
Passingham RE (2002): The frontal cortex: does size matter? Nat Neurosci 5:190–192.
[PubMed]
51.
Petrides M (2005): Lateral prefrontal cortex: architectonic and functional organization. Philos Trans R Soc B Biol Sci 360:781–795.
[PubMed]
52.
Petrides M, Cadoret GV, Mackey S (2005): Orofacial somatomotor responses in the macaque monkey homologue of Broca’s area. Nature 435:1235–1238.
[PubMed]
53.
Preuss TM (2009): What is it like to be a human?; in Gazzaniga MS (ed): The Cognitive Neurosciences. Cambridge, MIT Press, pp 49–64.
54.
R Development Core Team (2010): R: A Language and Environment for Statistical Computing, Vienna.
55.
Rilling JK, Barks SK, Parr LA, Preuss TM, Faber TL, Pagnoni G, Bremner JD, Votaw JR (2008): A comparison of resting-state brain activity in humans and chimpanzees. Proc Natl Acad Sci USA 104:17146–17151.
56.
Sakai T, Hirai D, Mikami A, Suzuki J, Hamada Y, Tomonaga M, Tanaka M, Miyabe-Nishiwaki T, Makishima H, Makatsukasa M, Matsuzawa T: Prolonged maturation of prefrontal white matter in chimpanzees. Nat Neurosci, in press.
57.
Schenker NM, Buxhoeveden DP, Blackmon WL, Amunts K, Zilles K, Semendeferi K (2008): A comparative quantitative analysis of cytoarchitecture and minicolumnar organization in Broca’s area in humans and great apes. J Comp Neurol 510:117–128.
[PubMed]
58.
Schenker NM, Desgouttes A-M, Semendeferi K (2005): Neural connectivity and cortical substrates of cognition in hominoids. J Hum Evol 49:547–569.
[PubMed]
59.
Schenker NM, Hopkins WD, Spocter MA, Garrison AR, Stimpson CD, Erwin JM, Hof PR, Sherwood CC (2010): Broca’s area homologue in chimpanzees (Pan trogolodytes): probabilistic mapping, asymmetry, and comparison to humans. Cereb Cortex 20:730–742.
[PubMed]
60.
Schoenemann PT, Sheehan MJ, Glotzer LD (2005): Prefrontal white matter volume is disproportionately larger in humans than in other primates. Nat Neurosci 8:242–252.
[PubMed]
61.
Scholz J, Klein MC, Behrens TEJ, Johansen-Berg H (2009): Training induces changes in white-matter architecture. Nat Neurosci 12:1370–1371.
[PubMed]
62.
Semendeferi K, Armstrong E, Schleicher A, Zilles K, Van Hoesen GW (2001): Prefrontal cortex in humans and apes: a comparative study of area 10. Am J Phys Anthropol 114:224–241.
[PubMed]
63.
Semendeferi K, Lu A, Schenker N, Damasio H (2002): Humans and great apes share a large frontal cortex. Nat Neurosci 5:272–276.
[PubMed]
64.
Sherwood CC, Broadfield DC, Holloway RL, Gannon PL, Hof PR (2003): Variability of Broca’s area homologue in African great apes: implications for language evolution. Anat Rec A Discov Mol Cell Evol Biol 271:276–285.
[PubMed]
65.
Sherwood CC, Holloway RL, Erwin JM, Schleicher A, Zilles K, Hof PR (2004): Cortical orofacial motor representation in old world monkeys, great apes, and humans. I. Quantitative analysis of cytoarchitecture. Brain Behav Evol 63:61–81.
[PubMed]
66.
Sherwood CC, Holloway RL, Semendeferi K, Hof PR (2005): Is prefrontal white matter enlargement a human evolutionary specialization? Nat Neurosci 8:537–538.
[PubMed]
67.
Smaers JB, Schleicher A, Zilles K, Vinicius L (2010): Frontal white matter volume is associated with brain enlargement and higher structural connectivity in haplorrhine primates. PLoS One 5:e9123.
[PubMed]
68.
Smith AR, Seid MA, Jimenez LC, Wcislo WT (2010): Socially induced brain development in a facultatively eusocial sweat bee Megalopta genalis (Halictidae). Proc R Soc B Biol Sci 277:2157–2163.
[PubMed]
69.
Smith RJ, Cheverud JM (2002): Scaling of sexual dimorphism in body mass: a phylogenetic analysis of Rensch’s rule in primates. Int J Primatol 23:1095-1135.
70.
Taglialatela JP, Cantalupo C, Hopkins WD (2006): Gesture handedness predicts asymmetry in the chimpanzee inferior frontal gyrus. Neuroreport 7:923–927.
71.
Taglialatela JP, Russell J, Schaeffer JA, Hopkins WD (2008): Communicative signal activates ‘Broca’s’ homologue in chimpanzees. Curr Biol 18:343–348.
[PubMed]
72.
Uylings HBM, Van Eden CG (1990): Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. Prog Brain Res 85:31–62.
[PubMed]
73.
Uylings HBM, Jacobsen AM, Zilles K, Amunts K (2006): Left-right asymmetry in volume and number of neurons in adult Broca’s area. Cortex 42:652–658.
[PubMed]
74.
Zhang K, Sejnowski TJ (2000): A universal scaling law between gray matter and white matter of cerebral cortex. Proc Natl Acad Sci USA 97:5621–5626.
[PubMed]
75.
Zilles K, Dabringhaus A, Geyer S, Amunts K, Qu M, Schleicher A, Gilissen E, Schlaug G, Steinmetz H (1996): Structural asymmetries in the human forebrain and the forebrain of non-human primates and rats. Neurosci Biobehav Rev 20:593–605.
[PubMed]
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