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Cellular signatures in the primary visual cortex of phylogeny and placentation

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Abstract

The long-held view that brain size can be used as an index of general functional capacity across mammals is in conflict with increasing evidence for phyletic differences in cellular organization. Furthermore, it is poorly understood how the internal cellular organization of the brain covaries with overall brain size variation. Using design-based stereology, we quantified glial cell and neuronal densities in the primary visual cortex of 71 mammalian species (spanning 11 orders) to test how those cellular densities are influenced by phylogeny, behavior, environment, and anatomy. We further tested cellular densities against mode of placentation to determine whether a relationship may exist. We provide evidence for cellular signatures of phylogenetic divergence from the mammalian trend in primates and carnivores, as well as considerably divergent scaling patterns between the primate suborders, Strepsirrhini and Haplorrhini, that likely originated at the anthropoid stem. Finally, we show that cellular densities in the mammalian cortex relate to the variability of maternal resources to the fetus in a species.

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References

  • Ahima RS, Bjorbaek C, Osei S, Flier JS (1999) Regulation of neuronal and glial proteins by leptin: implications for brain development. Endocrinology 140(6):2755–2762

    Article  PubMed  CAS  Google Scholar 

  • Aiello LC, Wells JCK (2002) Energetics and the evolution of the genus Homo. Annual Rev Anthropol 31(1):323–338. doi:10.1146/annurev.anthro.31.040402.085403

    Article  Google Scholar 

  • Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis. Curr Anthropol 36(2):199–221

    Article  Google Scholar 

  • Allen NJ, Barres BA (2005) Signaling between glia and neurons: focus on synaptic plasticity. Curr Opin Neurobiol 15(5):542–548

    Article  PubMed  CAS  Google Scholar 

  • Allman JC, McGuinness E (1988) Visual cortex in primates. In: Steklis H, Erwin JM (eds) Comparative primate biology, vol 4. Neurosciences. Alan R Liss, New York, pp 279–326

    Google Scholar 

  • Allman J, Tetreault N, Hakeem A, Manaye K, Semendeferi K, Erwin J, Park S, Goubert V, Hof P (2010) The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans. Brain Struct Funct 214(5):495–517. doi:10.1007/s00429-010-0254-0

    Article  PubMed  Google Scholar 

  • Araque A, Sangziri R, Parpura V, Haydon P (1999) Astrocyte-induced modulation of synaptic transmission. Can J Physiol Pharmacol 77(9):699–706

    Article  PubMed  CAS  Google Scholar 

  • Ashwell KWS, McAllan BM, Mai JK, Paxinos G (2008) Cortical cyto- and chemoarchitecture in three small Australian marsupial carnivores: Sminthopsis macroura, Antechinus stuartii and Phascogale calura. Brain Behav Evol. 72(3):215–232

  • Azevedo F, Ludmila R et al (2009) Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol 513:532–541

    Article  PubMed  Google Scholar 

  • Barres BA, Smith SJ (2001) Neurobiology: cholesterol–making or breaking the synapse. Science 294(5545):1296–1297. doi:10.1126/science.1066724

    Article  PubMed  CAS  Google Scholar 

  • Barton RA, Capellini I (2011) Maternal investment, life histories, and the costs of brain growth in mammals. Proc Natl Acad Sci 108(15):6169–6174. doi:10.1073/pnas.1019140108

    Article  PubMed  CAS  Google Scholar 

  • Beaulieu C (1993) Numerical data on neocortical neurons in adult rat, with special reference to the GABA population. Brain Res 609(1–2):284–292

    Article  PubMed  CAS  Google Scholar 

  • Bentourkia Mh, Bol A, Ivanoiu A, Labar D, Sibomana M, Coppens A, Michel C, Cosnard G, De Volder AG (2000) Comparison of regional cerebral blood flow and glucose metabolism in the normal brain: effect of aging. J Neurol Sci 181(1–2):19–28

    Article  PubMed  CAS  Google Scholar 

  • Bininda-Emonds O, Cardillo M, Jones K, MacPhee R, Beck R, Grenyer R et al (2007) The delayed rise of present-day mammals. Nature 446:507–512

    Article  PubMed  CAS  Google Scholar 

  • Bohnen NI, Minoshima S, Giordani B, Frey KA, Kuhl DE (1999) Motor correlates of occipital glucose hypometabolism in Parkinson’s disease without dementia. Neurology 52(3):541–546

    PubMed  CAS  Google Scholar 

  • Bourre J-M, Francois M, Youyou A, Dumont O, Piciotti M, Pascal G, Durand G (1989) The effects of dietary {alpha}-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. J Nutr 119(12):1880–1892

    PubMed  CAS  Google Scholar 

  • Boyd J, Marsubara J (2005) Repositioning the stria of Gennari [abstract]. Soc Neurosci

  • Broadhurst C, Wang Y, Crawford MA, Cunnane SC, Parkington JE, Schmidt WF (2002) Brain-specific lipids from marine, lacustrine, or terrestrial food resources: potential impact on early African Homo sapiens. Comp Biochem Physiol B Biochem Mol Biol 131:653–673

    Article  PubMed  Google Scholar 

  • Brodmann K (1909) Lokalisationslehre der Grosshirnrhinde

  • Bushong EA, Martone ME, Ellisman MH (2003) Examination of the relationship between astrocyte morphology and laminar boundaries in the molecular layer of adult dentate gyrus. J Comp Neurol 462(2):241–251. doi:10.1002/cne.10728

    Article  PubMed  Google Scholar 

  • Butti C, Sherwood C, Hakeem A, Allman J, Hof P (2009) Total number and volume of Von Economo neurons in the cerebral cortex of cetaceans. J Comp Neurol 515(2):243–259

    Article  PubMed  Google Scholar 

  • Caceres M, Lachuer J, Zapala MA, Redmond JC, Kudo L, Geschwind DH, Lockhart DJ, Preuss TM, Barlow C (2003) Elevated gene expression levels distinguish human from non-human primate brains. Proc Natl Acad Sci USA 100(22):13030–13035. doi:10.1073/pnas.2135499100

    Article  PubMed  CAS  Google Scholar 

  • Calsbeek R, Irschick DJ, Pfenning D (2009) The quick and the dead: correlational selection on morphology, performance, and habitat use in island lizards. Evolution 61(11):2493–2503. doi:10.1111/j.1558-5646.2007.00206.x

    Article  Google Scholar 

  • Capellini I, Venditti C, Barton R (2010) Phylogeny and metabolic scaling in mammals. Ecology 91(9):2783–2793

    Article  PubMed  Google Scholar 

  • Capellini I, Venditti C, Barton R (2011) Placentation and maternal investment in mammals. Am Nat 177(1):86–98

    Article  PubMed  Google Scholar 

  • Celio MR (1990) Calbindin D-28 k and parvalbumin in the rat nervous system. Neuroscience 35(2):375–475

    Article  PubMed  CAS  Google Scholar 

  • Changizi M (2001) Principles underlying mammalian neocortical scaling. Biol Cybern 84:207–215

    Article  PubMed  CAS  Google Scholar 

  • Collar DC, Wainwright PC, Alfaro ME (2008) Integrated diversification of locomotion and feeding in labrid fishes. Biol Lett 4:84–86

    Article  PubMed  Google Scholar 

  • Conley M, Fitzpatrick D, Diamond IT (1984) The laminar organization of the lateral geniculate body and the striate cortex in the tree shrew (Tupaia glis). J Neurosci 4:171–197

    PubMed  CAS  Google Scholar 

  • Crawford MA (2006) Docosahexaenoic acid in neural signaling systems. Nutr Health 18(3):263–276

    Article  PubMed  CAS  Google Scholar 

  • Cross DJ, Minoshima S, Nishimura S, Noda A, Tsukada H, Kuhl DE (2000) Three-dimensional stereotactic surface projection analysis of macaque brain pet: development and initial applications. J Nucl Med 41(11):1879–1887

    PubMed  CAS  Google Scholar 

  • Cunnane SC, Crawford MA (2003) Survival of the fattest: fat babies were the key to evolution of the large human brain. Comp Biochem Physiol Part A Mol Integr Physiol 136(1):17–26

    Article  CAS  Google Scholar 

  • Daniel PM, Whitteridge D (1961) The representation of the visual field on the cerebral cortex in monkeys. J Physiol 159(2):203–221

    PubMed  CAS  Google Scholar 

  • de Sousa AA, Sherwood CC, Schleicher A, Amunts K, MacLeod CE, Hof PR, Zilles K (2009) Comparative cytoarchitectural analyses of striate and extrastriate areas in Hominoids. Cereb Cortex 20(4):966–981. doi:10.1093/cercor/bhp158

    Article  PubMed  Google Scholar 

  • de Sousa AA, Sherwood CC, Mohlberg H, Amunts K, Schleicher A, MacLeod CE, Hof PR, Frahm H, Zilles K (2010) Hominoid visual brain structure volumes and the position of the lunate sulcus. J Hum Evol 58(4):281–291

    Article  PubMed  Google Scholar 

  • Defelipe J, González-Albo MC, Del Río MR, Elston GN (1999) Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. J Comp Neurol 412(3):515–526. doi:10.1002/(SICI)1096-9861(19990927)412:3<515::AID-CNE10>3.0.CO;2-1

    Article  PubMed  CAS  Google Scholar 

  • del Rio MR, de Felipe J (1997) Colocalization of parvalbumin and calbindin D-28°k in neurons including chandelier cells of the human temporal neocortex. J Chem Neuroanat 12(3):165–173

    Article  PubMed  Google Scholar 

  • Dicicco-Bloom E, Lu N, Pintar JE, Zhang J (1998) The PACAP ligand/receptor system regulates cerebral cortical neurogenesisa. Ann N Y Acad Sci 865(1):274–289. doi:10.1111/j.1749-6632.1998.tb11188.x

    Article  PubMed  CAS  Google Scholar 

  • Djemli-Shipkolye A, Raccah D, Pieroni G, Vague P, Coste T, Gerbi A (2003) Differential effect of omega3 PUFA supplementations on Na, K-ATPase and Mg-ATPase activities: possible role of the membrane omega6/omega3 ratio. J Membr Biol 191:37–47

    Article  PubMed  CAS  Google Scholar 

  • Drake J (2007) Parental investment and fecundity, but not brain size, are associated with establishment success in introduced fishes. Funct Ecol 21:963–968

    Article  Google Scholar 

  • Elliot MG, Crespi BJ (2009) Phylogenetic evidence for early hemochorial placentation in Eutheria. Placenta 30(11):949–967

    Article  PubMed  CAS  Google Scholar 

  • Enders AC, Carter AM (2004) What can studies of comparative placental structure tell us? Placenta 25(Suppl A):S3–S7

    Article  PubMed  CAS  Google Scholar 

  • Estes S, Arnold S (2007) Resolving the paradox of stasis: models with stabilizing selection explain evolutionary divergence on all timescales. Am Nat 169(2):227–244. doi:10.1086/510633

    Article  PubMed  Google Scholar 

  • Ferland R, Eyaid W, Collura R, Tully L, Hill R, Al-Nouri D, Al-Rumayyan A, Topcu M, Gascon G, Bodell A, Shugart Y, Ruvolo M, Walsh C (2004) Abnormal cerebellar development and axonal decussation due to mutations in AHI1 in Joubert syndrome. Nat Genet 36:1008–1013

    Article  PubMed  CAS  Google Scholar 

  • Friede R, van Houten W (1962) Neuronal extension and glial supply: functional significance of glia. Proc Natl Acad Sci USA 48:817–821

    Article  PubMed  CAS  Google Scholar 

  • Furutani R (2008) Laminar and cytoarchitectonic features of the cerebral cortex in the Risso’s dolphin (Grampus griseus), striped dolphin (Stenella coeruleoalba), and bottlenose dolphin (Tursiops truncatus). J Anat 213(3):241–248

    Article  PubMed  Google Scholar 

  • Gabi M, Collins CE, Wong P, Torres LB, Kaas JH, Herculano-Houzel S (2010) Cellular scaling rules for the brains of an extended number of primate species. Brain Behav Evol 76(1):32–44

    Article  PubMed  Google Scholar 

  • Garey LJ, Winkelmann E, Brauer K (1985) Golgi and Nissl studies of the visual cortex of the bottlenose dolphin. J Comp Neurol 240(3):305–321. doi:10.1002/cne.902400307

    Article  PubMed  CAS  Google Scholar 

  • Garland JT, Ives AR (2000) Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am Nat 155(3):346–364. doi:10.1086/303327

    Article  Google Scholar 

  • Garland JT, Dickerman A, Janis C, Jones J (1993) Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265–292

    Google Scholar 

  • Glezer II, Hof PR, Morgane PJ (1992) Calretinin-immunoreactive neurons in the primary visual cortex of dolphin and human brains. Brain Res 595(2):181–188

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Voyer A, Winberg S, Kolm N (2009) Distinct evolutionary patterns of brain and body size during adaptive radiation. Evolution 63:2266–2274

    Article  PubMed  Google Scholar 

  • Groemping U (2006) Relative importance for linear regression in R: the package relaimpo. J Stat Softw 17(1):1–27

    Google Scholar 

  • Groemping U (2007) Estimators of relative importance in linear regression based on variance decomposition. Am Stat 61:139–147

    Article  Google Scholar 

  • Grossman LI, Schmidt TR, Wildman DE, Goodman M (2001) Molecular evolution of aerobic energy metabolism in primates. Mol Phylogenet Evol 18(1):26–36

    Google Scholar 

  • Grossman LI, Wildman DE, Schmidt TR, Goodman M (2004) Accelerated evolution of the electron transport chain in anthropoid primates. Trends Genet 20(11):578–585

    Google Scholar 

  • Gundersen HJG, Jensen EBV (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147(3):229–263

    Article  PubMed  CAS  Google Scholar 

  • Gundersen H, Jensen E, Kieu K, Nielsen J (1999) The efficiency of systematic sampling in stereology–reconsidered. J Microsc 193(3):199–211

    Article  PubMed  CAS  Google Scholar 

  • Hakeem AY, Sherwood CC, Bonar CJ, Butti C, Hof PR, Allman JM (2009) Von Economo neurons in the elephant brain. Anat Rec Adv Integr Anat Evol Biol 292(2):242–248. doi:10.1002/ar.20829

    Article  Google Scholar 

  • Harrison KH, Hof PR, Wang SSH (2002) Scaling laws in the mammalian neocortex: does form provide clues to function? J Neurocytol 31(3):289–298. doi:10.1023/a:1024178127195

    Article  PubMed  CAS  Google Scholar 

  • Hartwig W (2002) The primate fossil record. Cambridge University Press, Cambridge

    Google Scholar 

  • Harvey PH, Krebs J (1990) Comparing brains. Science 249:140–146

    Article  PubMed  CAS  Google Scholar 

  • Hatten ME, Liem RKH, Mason CA (1986) Weaver mouse cerebellar granule neurons fail to migrate on wild-type astroglial processes in vitro. J Neurosci 6(9):2676–2683

    PubMed  CAS  Google Scholar 

  • Hatten ME, Lynch M, Rydel RE, Sanchez J, Joseph-Silverstein J, Moscatelli D, Rifkin DB (1988) In vitro neurite extension by granule neurons is dependent upon astroglial-derived fibroblast growth factor. Dev Biol 125(2):280–289

    Article  PubMed  CAS  Google Scholar 

  • Haug H (1987) Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: a stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant). Am J Anat 180:126–142

    Article  PubMed  CAS  Google Scholar 

  • Hawkins A, Oszewski J (1957) Glia/nerve cell index for cortex of the whale. Science 126:76–77

    Article  PubMed  CAS  Google Scholar 

  • Haydon PG (2001) Glia: listening and talking to the synapse. Nat Rev Neurosci 2(3):185–193

    Article  PubMed  CAS  Google Scholar 

  • Healy SD, Rowe C (2007) A critique of comparative studies of brain size. Proc R Soc B 274:453–464

    Article  PubMed  Google Scholar 

  • Herculano-Houzel S (2010) Coordinated scaling of cortical and cerebellar numbers of neurons. Frontiers Neuroanat 4:12. doi:10.3389/fnana.2010.00012

    Google Scholar 

  • Herculano-Houzel S, Collins CE, Wong P, Kaas JH (2007) Cellular scaling rules for primate brains. Proc Natl Acad Sci USA 204:3562–3567

    Article  CAS  Google Scholar 

  • Hertz L, Hansson E, Rönnbäck L (2001) Signaling and gene expression in the neuron-glia unit during brain function and dysfunction: Holger Hydén in memoriam. Neurochem Int 39(3):227–252

    Article  PubMed  CAS  Google Scholar 

  • Hidalgo A, Kinrade EFV, Georgiou M (2001) The drosophila neuregulin vein maintains glial survival during axon guidance in the CNS. Dev Cell 1(5):679–690

    Article  PubMed  CAS  Google Scholar 

  • Hladik C, Chivers DJ, Pasquet P (1999) On diet and gut size in non-human primates and humans: is there a relationship to brain size? Curr Anthropol 40(5):695–697

    Article  PubMed  Google Scholar 

  • Hof PR, Morrison J (1995) Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: a quantitative immunohistochemical analysis. J Comp Neurol 352(2):161–186

    Article  PubMed  CAS  Google Scholar 

  • Hof PR, Sherwood CC (2005) Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. Anat Rec 287A(1):1153–1163

    Article  CAS  Google Scholar 

  • Hof PR, Van Der Gucht E (2007) Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae). Anat Rec Adv Integr Anat Evol Biol 290(1):1–31. doi:10.1002/ar.20407

    Article  Google Scholar 

  • Hof PR, Glezer II, Archin N, Janssen WG, Morgane PJ, Morrison JH (1992) The primary auditory cortex in cetacean and human brain: a comparative analysis of neurofilament protein-containing pyramidal neurons. Neurosci Lett 146(1):91–95

    Article  PubMed  CAS  Google Scholar 

  • Hof PR, Glezer II, Conde F, Roxana F et al (1999) Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neur 16(2):77–116

    Article  CAS  Google Scholar 

  • Hof PR, Glezer II, Nimchinsky EA, Erwin JM (2000) Neurochemical and cellular specializations in the mammalian neocortex reflect phylogenetic relationships: evidence from primates, cetaceans, and artiodactyls. Brain Behav Evol 55(6):300–310

    Article  PubMed  CAS  Google Scholar 

  • Hof PR, Nimchinsky EA, Perl DP, Erwin JM (2001) An unusual population of pyramidal neurons in the anterior cingulate cortex of hominids contains the calcium-binding protein calretinin. Neurosci Lett 307(3):139–142

    Article  PubMed  CAS  Google Scholar 

  • Hof PR, Chanis R, Marino L (2005) Cortical complexity in cetacean brains. Anat Rec 287A(1):1142–1152

    Google Scholar 

  • Holmes G (1917) The organization of the visual cortex in man. Br J Ophthalmol 2:353–384

    Article  Google Scholar 

  • Homman-Ludiye J, Manger PR, Bourne JA (2010) Immunohistochemical parcellation of the ferret (Mustela putorius) visual cortex reveals substantial homology with the cat (Felis catus). J Comp Neurol 518(21):4439–4462

    Article  PubMed  Google Scholar 

  • Horner PJ, Palmer TD (2003) New roles for astrocytes: the nightlife of an ‘astrocyte’. La vida loca!. Trends Neurosci 26(11):597–603

    Article  PubMed  CAS  Google Scholar 

  • Howard C, Reed M (1998) Unbiased stereology: three-dimensional measurement in microscopy. Springer, Berlin

    Google Scholar 

  • Inouye T (1909) Visual disturbances following gunshot wounds of the cortical visual area (trans: Glickstein M., Fahle M.). Oxford University Press, Oxford

    Google Scholar 

  • Kang J, Jiang L, Goldman SA, Nedergaard M (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1(8):683–692

    Article  PubMed  CAS  Google Scholar 

  • Kornack DR (2000) Neurogenesis and the evolution of cortical diversity: mode, tempo, and partitioning during development and persistence in adulthood. Brain Behav Evol 55(6):336–344

    Article  PubMed  CAS  Google Scholar 

  • Kornack DR, Rakic P (1995) Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages. Neuron 15(2):311–321

    Article  PubMed  CAS  Google Scholar 

  • Kornack D, Rakic P (1998) Changes in cell-cycle kinetics during the development and evolution of primate neocortex. Proc Natl Acad Sci USA 95:1242–1246

    Article  PubMed  CAS  Google Scholar 

  • Laming PR, Kimelberg H, Robinson S, Salm A, Hawrylak N, Müller C, Roots B, Ng K (2000) Neuronal-glial interactions and behaviour. Neurosci Biobehav Rev 24(3):295–340

    Article  PubMed  CAS  Google Scholar 

  • Lande L, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37(6):1210–1226

    Article  Google Scholar 

  • Leonard WR, Snodgrass JJ, Robertson ML (2007) Effects of brain evolution on human nutrition and metabolism. Annu Rev Nutr 27(1):311–327. doi:10.1146/annurev.nutr.27.061406.093659

    Article  PubMed  CAS  Google Scholar 

  • Lewitus E, Soligo C (2011) Life-history correlates of placental structure in eutherian evolution. Evol Biol 38(3):287–305. doi:10.1007/s11692-011-9115-x

    Google Scholar 

  • Maddison W, Maddison D (2010) Mesquite: a modular system for evolutionary analysis. Version 2.73.http://mesquiteproject.org

  • Martin RD (1981) Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature 293:57–60

    Article  PubMed  CAS  Google Scholar 

  • Martin R (2008) Evolution of placentation in primates: implications of mammalian phylogeny. Evol Biol 35(2):125–145

    Article  Google Scholar 

  • McNab B (1989) Brain size and its relation to the rate of metabolism in mammals. Am Nat 133:157–167

    Article  Google Scholar 

  • Mossman H (1987) Vertebrate fetal membranes: comparative ontogeny and morphology, evolution, phylogenetic significance, basic functions, research opportunities. Rutgers University Press, New Brunswick

    Google Scholar 

  • Mounzih K, Qiu J, Ewart-Toland A, Chehab FF (1998) Leptin is not necessary for gestation and parturition but regulates maternal nutrition via a leptin resistance state. Endocrinology 139(12):5259–5262. doi:10.1210/en.139.12.5259

    Article  PubMed  CAS  Google Scholar 

  • Muller C (1993) Glial cell functions and activity-dependent plasticity of the mammalian visual cortex. Perspect Dev Neurobiol 1:169–177

    PubMed  CAS  Google Scholar 

  • Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26(10):523–530

    Article  PubMed  CAS  Google Scholar 

  • Nielsen R, Bustamante C, Clark AG, Glanowski S, Sackton TB, Hubisz MJ, Fledel-Alon A, Tanenbaum DM, Civello D, White TJ, Sninsky J, Adams MD, Cargill M (2005) A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 3(6):e170

    Article  PubMed  CAS  Google Scholar 

  • Nimchinsky EA, Vogt BA, Morrison JH, Hof PR (1995) Spindle neurons of the human anterior cingulate cortex. J Comp Neurol 355(1):27–37

    Article  PubMed  CAS  Google Scholar 

  • Nimchinsky EA, Gilissen E, Allman JM, Perl DP, Erwin JM, Hof PR (1999) A neuronal morphologic type unique to humans and great apes. Proc Natl Acad Sci USA 96(9):5268–5273

    Article  PubMed  CAS  Google Scholar 

  • Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211(11):1792–1804

    Article  PubMed  CAS  Google Scholar 

  • Noda A, Ohba H, Kakiuchi T, Futatsubashi M, Tsukada H, Nishimura S (2002) Age-related changes in cerebral blood flow and glucose metabolism in conscious rhesus monkeys. Brain Res 936(1–2):76–81

    Article  PubMed  CAS  Google Scholar 

  • Ogata K, Kosaka T (2003) Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience. 113(1):221–233

    Google Scholar 

  • Pagel M (1992) A method for the analysis of comparative data. J Theor Biol 156:431–442

    Article  Google Scholar 

  • Pelleymounter M, Cullen M, Baker M, Hecht R, Winters D, Boone T, Collins F (1995) Effects of the obese gene product on body weight regulation in ob/ob mice. Science 269:540–543

    Article  PubMed  CAS  Google Scholar 

  • Peters A, Sethares C (1991) Organization of pyramidal neurons in area 17 of monkey visual cortex. J Comp Neurol 306(1):1–23. doi:10.1002/cne.903060102

    Article  PubMed  CAS  Google Scholar 

  • Peters A, Yilmaz E (1993) Neuronal organization in area 17 of cat visual cortex. Cereb Cortex 3(1):49–68. doi:10.1093/cercor/3.1.49

    Article  PubMed  CAS  Google Scholar 

  • Pfrieger FW, Barres BA (1997) Synaptic efficacy enhanced by glial cells in vitro. Science 277(5332):1684–1687. doi:10.1126/science.277.5332.1684

    Article  PubMed  CAS  Google Scholar 

  • Preuss TM (2001) The discovery of cerebral diversity: an unwelcome scientific revolution. In: Falk D, Gibson K (eds) Evolutionary anatomy of the primate cerebral cortex. Cambridge University Press, Cambridge, pp 138–164

    Chapter  Google Scholar 

  • Preuss TM, Coleman GQ (2002) Human-specific organization of primary visual cortex: alternating compartments of dense Cat-301 and calbindin immunoreactivity in layer 4A. Cereb Cortex 12(7):671–691

    Article  PubMed  Google Scholar 

  • Preuss TM, Goldman-Rakic P (1991a) Architectonics of the parietal and temporal association cortex in the strepsirhine primate Galago compared to the anthropoid primate Macaca. J Comp Neurol 310:475–506

    Article  PubMed  CAS  Google Scholar 

  • Preuss TM, Goldman-Rakic P (1991b) Ipsilateral cortical connections of granular frontal cortex in the strepsirhine primate Galago, with comparative comments on anthropoid primates. J Comp Neurol 310:507–549

    Article  PubMed  CAS  Google Scholar 

  • Preuss TM, Goldman-Rakic P (1991c) Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca. J Comp Neurol 310:429–474

    Article  PubMed  CAS  Google Scholar 

  • Preuss TM, Kaas JH (1996) Parvalbumin-like immunoreactivity of layer V pyramidal cells in the motor and somatosensory cortex of adult primates. Brain Res 712(2):353–357

    Article  PubMed  CAS  Google Scholar 

  • Preuss TM, Qi H, Kaas JH (1999) Distinctive compartmental organization of human primary visual cortex. Proc Natl Acad Sci USA 96(20):11601–11606

    Article  PubMed  CAS  Google Scholar 

  • Prothero J (1997) Scaling of cortical neuron density and white matter volume in mammals. J Hirnforsch 38:513–524

    PubMed  CAS  Google Scholar 

  • Rakic P (2000) Molecular and cellular mechanisms of neuronal migration: relevance to cortical epilepsies. Adv Neurol 84:1–14

    PubMed  CAS  Google Scholar 

  • Rawn SM, Cross JC (2008) The evolution, regulation, and function of placenta-specific genes. Annu Rev Cell Dev Biol 24(1):159–181. doi:10.1146/annurev.cellbio.24.110707.175418

    Article  PubMed  CAS  Google Scholar 

  • Revell LJ, Harmon LJ (2008) Testing quantitative genetic hypotheses about the evolutionary rate matrix for continuous characters. Evol Ecol Res 10:311–321

    Google Scholar 

  • Rosa MGP (1999) Topographic organisation of extrastriate areas in the flying fox: implications for the evolution of mammalian visual cortex. J Comp Neurol 411:503–523

    Article  PubMed  CAS  Google Scholar 

  • Rosa MGP, Tweedale R (2005) Brain maps, great and small: lessons from comparative studies of primate visual cortical organization. Philos Trans R Soc B Biol Sci 360(1456):665–691. doi:10.1098/rstb.2005.1626

    Article  Google Scholar 

  • Ross CF, Kirk EC (2007) Evolution of eye size and shape in primates. J Hum Evol 52(3):294–313

    Google Scholar 

  • Schwartz E (1977) Afferent geometry in the primate visual cortex and the generation of neuronal trigger features. Biol Cybern 28:1–14

    Article  PubMed  CAS  Google Scholar 

  • Sherk H (1986) Location and connections of visual cortical areas in the cat’s suprasylvian sulcus. J Comp Neurol 247:1–31

    Article  PubMed  CAS  Google Scholar 

  • Sherwood CC, Hof PR (2007) The evolution of neuron types and cortical histology in apes and humans. In: Preuss TM, Kaas JH (eds) Evolution of nervous systems, vol. 4: The evolution of primate nervous systems. Academic Press, Oxford, pp 355–378

  • Sherwood CC, Raghanti MA, Simpson CD, Bonar CJ, de Sousa AA, Preuss TM, Hof PR (2006a) Scaling of inhibitory interneurons in areas V1 and V2 of anthropoid primates as revealed by calcium-binding protein immunohistochemistry. Brain Behav Evol 69(3):176–195

    Article  PubMed  Google Scholar 

  • Sherwood CC, Stimpson CD, Raghanti MA, Wildman DE, Uddin M, Grossman LI, Goodman M, Redmond JC, Bonar CJ, Erwin JM, Hof PR (2006b) Evolution of increased glia-neuron rations in the human frontal cortex. Proc Natl Acad Sci USA 203:13606–13611

    Article  Google Scholar 

  • Sherwood CC, Raghanti MA, Stimpson CD, Bonar CJ, de Sousa AA, Preuss TM et al (2007) Scaling of inhibitory interneurons in areas V1 and V2 of anthropoid primates as revealed by calcium-binding protein immunohistochemistry. Brain Behav Evol 69(3):176–195

    Google Scholar 

  • Sherwood C, Stimpson C, Butti C, Bonar C, Newton A, Allman J et al (2009) Neocortical neuron types in Xenarthra and Afrotheria: implications for brain evolution in mammals. Brain Struct Funct 213(3):301–328

    Google Scholar 

  • Skoglund TS, Pascher R, Berthold CH (1996) Heterogeneity in the columnar number of neurons in different neocortical areas in the rat. Neurosci Lett 208(2):97–100

    Article  PubMed  CAS  Google Scholar 

  • Slomianka L, West MJ (2005) Estimators of the precision of stereological estimates: an example based on the CA1 pyramidal cell layer of rats. Neuroscience 136(3):757–767

    Article  PubMed  CAS  Google Scholar 

  • Sokal R, Rohlf F (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. WH Freeman and Co., New York

    Google Scholar 

  • Song H, Stevens CF, Gage FH (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417(6884):39–44

    Article  PubMed  CAS  Google Scholar 

  • Suh J, Lu N, Nicot A, Tatsuno I, DiCicco-Bloom E (2001) PACAP is an anti-mitogenic signal in developing cerebral cortex. Nat Neurosci 4(2):123–124

    Article  PubMed  CAS  Google Scholar 

  • Talbot SA, Marshall WH (1941) Physiological studies on neural mechanisms of visual localization and discrimination. Am J Ophthalmol 24(11):1255–1264

    Google Scholar 

  • Tootell RBH, Hadjikhani N, Hall EK, Marrett S, Vanduffel W, Vaughan JT, Dale AM (1998) The Retinotopy of Visual Spatial Attention. Neuron 21(6):1409–1422

    Article  PubMed  CAS  Google Scholar 

  • Tower D (1954) Structural and functional organization of mammalian cerebral cortex: the correlation of neurone density with brain size. J Comp Neurol 101:19–51

    Article  PubMed  CAS  Google Scholar 

  • Tower D, Young O (1973) The activities of butyrylcholinesterase and carbonic anhydrase, the rate of anaerobic glycolysis, and the question of a constant density of glial cells in cerebral cortices of various mammalian species from mouse to whale. J Neurochem 20:269–278

    Article  PubMed  CAS  Google Scholar 

  • Trayhurn P, Duncan J, Hoggard N, Rayner D (1998) Regulation of leptin production: a dominant role for the sympathetic nervous system? Proc Nutr Soc 57:413–419

    Article  PubMed  CAS  Google Scholar 

  • Uddin M, Goodman M, Erez O, Romero R, Liu G, Islam M, Opazo JC, Sherwood CC, Grossman LI, Wildman DE (2008) Distinct genomic signatures of adaptation in pre- and postnatal environments during human evolution. Proc Natl Acad Sci 105(9):3215–3220. doi:10.1073/pnas.0712400105

    Article  PubMed  CAS  Google Scholar 

  • Ullian EM, Sapperstein SK, Christopherson KS, Barres BA (2001) Control of synapse number by glia. Science 291(5504):657–661. doi:10.1126/science.291.5504.657

    Article  PubMed  CAS  Google Scholar 

  • Vallender EJ, Mekel-Bobrov N, Lahn BT (2008) Genetic basis of human brain evolution. Trends Neurosci 31(12):637–644

    Article  PubMed  CAS  Google Scholar 

  • Valverde F (1986) Intrinsic neocortical organization: some comparative aspects. Neuroscience 18:1–23

    Article  PubMed  CAS  Google Scholar 

  • Walker JA (2007) A general model of functional constraints on phenotypic evolution. Am Nat 170:681–689

    Article  PubMed  Google Scholar 

  • Wang SSH, Shultz JR, Burish MJ, Harrison KH, Hof PR, Towns LC, Wagers MW, Wyatt KD (2008) Functional trade-offs in white matter axonal scaling. J Neurosci 28(15):4047–4056. doi:10.1523/jneurosci.5559-05.2008

    Article  PubMed  CAS  Google Scholar 

  • Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81(02):259–291. doi:10.1017/S1464793106007007

    Article  PubMed  Google Scholar 

  • Wildman DE, Chen C, Erez O, Grossman LI, Goodman M, Romero R (2006) Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc Natl Acad Sci USA 103(9):3203–3208

    Google Scholar 

  • Wong P, Kaas JH (2009) Architectonic subdivisions of neocortex in the tree shrew (Tupaia belangeri). Anat Rec Adv Integr Anat Evol Biol 292(7):994–1027

    Article  Google Scholar 

  • Wong-Riley MT, Hevner R, Cutlan R, Earnest M, Egan R, Frost J, Nguyen T (1993) Cytochrome oxidase in the human visual cortex: distribution in the developing and the adult brain. Vis Neurosci 10(1):41–58

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman J (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425–431

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Kunz TH, Tumba N, Clamon Schulz L, Li C, Reeves M, Widmaier EP (2003) Comparative analysis of expression and secretion of placental leptin in mammals. Am J Physiol Regul Integr Comp Physiol 285(2):R438–R446. doi:10.1152/ajpregu.00776.2002

    PubMed  CAS  Google Scholar 

  • Zilles K, Armstrong E, Schlaug G, Schleicher A (1986) Quantitative cytoarchitectonics of the posterior cingulate cortex in primates. J Comp Neurol 253:514–524

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported in part by a grant from the James S. McDonnell Foundation (22002078 to P.R.H. and C.C.S.), Brain Research Trust (E.L.) and University of London Central Research Fund (E.L.). E.L. would also like to thank Dr Archibald Fobbs for help with the neuroanatomical collection at the NMHM (Washington, D.C) and Evan Charles for discussion.

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  1. Department of Anthropology, University College London, London, WC1H 0BW, UK

    Eric Lewitus

  2. Department of Anthropology, The George Washington University, 2110 G Street, NW, Washington, DC, 20052, USA

    Chet C. Sherwood

  3. Fishberg Department of Neuroscience and Friedman Brain Institute, Mount Sinai School of Medicine, Box 1065, One Gustave L. Levy Place, New York, NY, 10029, USA

    Patrick R. Hof

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  1. Eric Lewitus
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Correspondence to Eric Lewitus.

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Lewitus, E., Sherwood, C.C. & Hof, P.R. Cellular signatures in the primary visual cortex of phylogeny and placentation. Brain Struct Funct 217, 531–547 (2012). https://doi.org/10.1007/s00429-011-0338-5

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