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Evidence for expansion of the precuneus in human evolution

Abstract

The evolution of neurocranial morphology in Homo sapiens is characterized by bulging of the parietal region, a feature unique to our species. In modern humans, expansion of the parietal surface occurs during the first year of life, in a morphogenetic stage which is absent in chimpanzees and Neandertals. A similar variation in brain shape among living adult humans is associated with expansion of the precuneus. Using MRI-derived structural brain templates, we compare medial brain morphology between humans and chimpanzees through shape analysis and geometrical modeling. We find that the main spatial difference is a prominent expansion of the precuneus in our species, providing further evidence of evolutionary changes associated with this area. The precuneus is a major hub of brain organization, a central node of the default-mode network, and plays an essential role in visuospatial integration. Together, the comparative neuroanatomical and paleontological evidence suggest that precuneus expansion is a neurological specialization of H. sapiens that evolved in the last 150,000 years that may be associated with recent human cognitive specializations.

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References

  1. Allen JS, Damasio H, Grabowski TJ (2002) Normal neuroanatomical variation in the human brain: an MRI-volumetric study. Am J Phys Anthropol 118:341–358

    Article  PubMed  Google Scholar 

  2. Barks SK, Parr LA, Rilling JL (2015) The default mode network in chimpanzees (Pan troglodytes) is similar to that of humans. Cereb Cortex 25:538–544

    Article  PubMed  Google Scholar 

  3. Bookstein FL (1991) Morphometric tools for landmark data. Cambridge University Press, Cambridge

    Google Scholar 

  4. Bookstein FL, Gunz P, Mitteroecker P, Prossinger H, Schaefer K, Seidler H (2003) Cranial integration in Homo: singular warps analysis of the midsagittal plane in ontogeny and evolution. J Hum Evol 44:167–187

    Article  PubMed  Google Scholar 

  5. Bruner E (2004) Geometric morphometrics and paleoneurology: brain shape evolution in the genus Homo. J Hum Evol 47:279–303

    Article  PubMed  Google Scholar 

  6. Bruner E, Iriki A (2015) Extending mind, visuospatial integration, and the evolution of the parietal lobes in the human genus. Quat Int. doi:10.1016/j.quaint.2015.05.019

    Google Scholar 

  7. Bruner E, Jacobs HIL (2013) Alzheimer’s disease: the downside of a highly evolved parietal lobe? J Alz Dis 35:227–240

    CAS  Google Scholar 

  8. Bruner E, Pearson O (2013) Neurocranial evolution in modern humans: the case of Jebel Irhoud 1. Anthropol Sci 121:31–41

    Article  Google Scholar 

  9. Bruner E, Manzi G, Arsuaga JL (2003) Encephalization and allometric trajectories in the genus Homo: evidence from the Neanderthal and modern lineages. Proc Natl Acad Sci USA 100:15335–15340

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Bruner E, Martin-Loeches M, Colom R (2010) Human midsagittal brain shape variation: patterns, allometry and integration. J Anat 216:589–599

    Article  PubMed  PubMed Central  Google Scholar 

  11. Bruner E, De la Cuétara JM, Holloway R (2011a) A bivariate approach to the variation of the parietal curvature in the genus Homo. Anat Rec 294:1548–1556

    Article  Google Scholar 

  12. Bruner E, Mantini S, Musso F, de la Cuétara JM, Ripani M, Sherkat S (2011b) The evolution of the meningeal vascular system in the human genus: from brain shape to thermoregulation. Am J Hum Biol 23:35–43

    Article  PubMed  Google Scholar 

  13. Bruner E, de la Cuétara JM, Masters M, Amano H, Ogihara N (2014a) Functional craniology and brain evolution: from paleontology to biomedicine. Front Neuroanat 8:19

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bruner E, Rangel de Lázaro G, de la Cuétara JM, Martín-Loeches M, Colom R, Jacobs HIL (2014b) Midsagittal brain variation and MRI shape analysis of the precuneus in adult individuals. J Anat 224:367–376

    Article  PubMed  PubMed Central  Google Scholar 

  15. Bruner E, Amano H, de la Cuétara JM, Ogihara N (2015a) The brain and the braincase: a spatial analysis on the midsagittal profile in adult humans. J Anat 227:268–276

    Article  PubMed  Google Scholar 

  16. Bruner E, Román FJ, de la Cuétara JM, Martin-Loeches M, Colom R (2015b) Cortical surface area and cortical thickness in the precuneus of adult humans. Neurosci 286:345–352

    CAS  Article  Google Scholar 

  17. Caminiti R, Innocenti GM, Battaglia-Mayer A (2015) Organization and evolution of parieto-frontal processing streams in macaque monkeys and humans. Neuosci Biobehav Rev 56:73–96

    Article  Google Scholar 

  18. Caspers S, Eickhoff SB, Rick T, von Kapri A, Kuhlen T, Huang R, Shah NJ, Zilles K (2011) Probabilistic fiber tract analysis of cytoarchitectonically defined human inferior parietal lobule areas reveals similarities to macaques. Neuroimage 58:362–380

    Article  PubMed  Google Scholar 

  19. Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583

    Article  PubMed  Google Scholar 

  20. Chen CH, Gutierrez ED, Thompson W, Panizzon MS, Jernigan TL, Eyler LT, Fennema-Notestine C, Jak AJ, Neale MC, Franz CE, Lyons MJ, Grant MD, Fischl B, Seidman LJ, Tsuang MT, Kremen WS, Dale AM (2012) Hierarchical genetic organization of human cortical surface area. Science 335:1634–1636

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Gómez-Robles A, Hopkins WD, Sherwood CC (2013) Increased morphological asymmetry, evolvability and plasticity in human brain evolution. Proc R Sci B 280:20130575

    Article  Google Scholar 

  22. Gómez-Robles A, Hopkins WD, Schapiro SJ, Sherwood CC (2015) Relaxed genetic control of cortical organization in human brains compared with chimpanzees. Proc Natl Acad Sci USA doi/. doi:10.1073/pnas.1512646112

    Google Scholar 

  23. Gunz P, Harvati K (2007) The Neanderthal “chignon”: variation, integration, and homology. J Hum Evol 52:262–274

    Article  PubMed  Google Scholar 

  24. Gunz P, Neubauer S, Maureille B, Hublin JJ (2010) Brain development after birth differs between Neanderthals and modern humans. Curr Biol 20:R921–R922

    CAS  Article  PubMed  Google Scholar 

  25. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6:e159

    Article  PubMed  PubMed Central  Google Scholar 

  26. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaentol Electron 4:1–9

    Google Scholar 

  27. Hills TT, Todd PM, Lazer D, Redish AD, Couzin ID, the Cognitive Search Research Group (2015) Exploration versus exploitation in space, mind, and society. Trends Cogn Sci 19:46–54

    Article  Google Scholar 

  28. Iriki A, Taoka M (2012) Triadic (ecological, neural, cognitive) niche construction: a scenario of human brain evolution extrapolating tool use and language from the control of reaching actions. Philos Trans R Soc London B Biol Sci 367:10–23

    Article  PubMed  PubMed Central  Google Scholar 

  29. Jolliffe IT (2002) Principal component analysis. Springer, Berlin

    Google Scholar 

  30. Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357

    Article  PubMed  Google Scholar 

  31. Kobayashi Y, Matsui T, Haizuka Y, Ogihara N, Hirai N, Matsumura G (2014) Cerebral sulci and gyri observed on macaque endocasts. In: Akazawa T, Ogihara N, Tanabe HC, Terashima H (eds) Dynamics of learning in Neanderthals and modern humans, vol 2. Springer, Japan, pp 131–137

    Chapter  Google Scholar 

  32. Kojima T, Onoe H, Hikosaka K, Tsutsui K, Tsukada H, Watanabe M (2009) Default mode of brain activity demonstrated by positron emission tomography imaging in awake monkeys: higher rest-related than working memory-related activity in medial cortical areas. J Neurosci 29:14463–14471

    CAS  Article  PubMed  Google Scholar 

  33. Land MF (2014) Do we have an internal model of the outside world? Phil Trans R Soc B 369:20130045

    Article  PubMed  PubMed Central  Google Scholar 

  34. Li L, Hu X, Preuss TM, Glasser MF, Damen FW, Qiu Y, Rilling J (2013) Mapping putative hubs in human, chimpanzee and rhesus macaque connectomes via diffusion tractography. Neuroimage 80:462–474

    Article  PubMed  PubMed Central  Google Scholar 

  35. Lieberman DE, McBratney BM, Krovitz G (2002) The evolution and development of cranial form in Homo sapiens. Proc Natl Acad Sci USA 99:1134–1139

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Maister L, Slater M, Sanchez-Vives MV, Tsakiris M (2015) Changing bodies changes minds: owning another body affects social cognition. Trends Cogn Sci 19:6–12

    Article  PubMed  Google Scholar 

  37. Mantini D, Gerits A, Nelissen K, Durand JB, Joly O, Simone L, Sawamura H, Wardak C, Orban GA, Buckner RL, Vanduffel W (2011) Default mode of brain function in monkeys. J Neurosci 31:12954–12956

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Margulies DS, Vincent JL, Kelly C, Lohmann G, Uddin LQ, Biswal BB, Villringer A, Castellanos FX, Milham MP, Petrides M (2009) Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci USA 106:20069–20074

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Mars R, Jbabdi S, Sallet J, O’Reilly JX, Croxson PL, Olivier E, Noonan MAP, Bergmann C, Mitchell AS, Baxter MG, Behrens TEJ, Johansen-Berg H, Tomassini V, Miller KL, Rushworth MFS (2011) Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J Neurosci 31:4087–4100

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Martin R, Barbour AD (1989) Aspects of line-fitting in bivariate allometric analyses. Folia Primatol 53:65–81

    CAS  Article  PubMed  Google Scholar 

  41. Moss ML, Young RW (1960) A functional approach to craniology. Am J Phys Anthropol 18:281–292

    CAS  Article  PubMed  Google Scholar 

  42. Neubauer S (2014) Endocasts: possibilities and limitations for the interpretation of human brain evolution. Brain Behav Evol 84:117–134

    Article  PubMed  Google Scholar 

  43. Neubauer S, Gunz P, Hublin JJ (2009) The pattern of endocranial ontogenetic shape changes in humans. J Anat 215:240–255

    Article  PubMed  PubMed Central  Google Scholar 

  44. Neubauer S, Gunz P, Hublin JJ (2010) Endocranial shape changes during growth in chimpanzees and humans: a morphometric analysis of unique and shared aspects. J Hum Evol 59:555–566

    Article  PubMed  Google Scholar 

  45. Orban GA, Claeys K, Nelissen K, Smans R, Sunaert S, Todd JT, Wardak C, Durand JB, Vanduffel W (2006) Mapping the parietal cortex of human and non-human primates. Neuropsychologia 44:2647–2667

    Article  PubMed  Google Scholar 

  46. Peer M, Salomon R, Goldberg I, Blanke O, Arzy S (2015) Brain system for mental orientation in space, time, and person. Proc Natl Acad Sci USA 112:11072–11077

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Rangel de Lázaro G, de la Cuétara JM, Píšová H, Lorenzo C, Bruner E (2015) Diploic vessels and computed tomography: segmentation and comparison in modern humans and fossil hominids. Am J Phys Anthropol. doi:10.1002/ajpa.22878

    PubMed  Google Scholar 

  48. Rilling JK (2006) Human and non-human primate brains: are they allometrically scaled versions of the same design? Evol Anthropol 15:65–67

    Article  Google Scholar 

  49. Rilling JK (2014) Comparative primate neuroimaging: insights into human brain evolution. Trends Cogn Sci 18:45–55

    Article  Google Scholar 

  50. Rilling JK, Seligman RA (2002) A quantitative morphometrics comparative analysis of the primate temporal lobe. J Hum Evol 42:505–533

    Article  PubMed  Google Scholar 

  51. Rilling JK, Barks SK, Parr LA, Preuss TM, Faber TL, Pagnoni G, Bremner JD, Votaw JR (2007) A comparison of resting-state brain activity in humans and chimpanzees. Proc Natl Acad Sci USA 104:17146–17151

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. Rohlf JF (2004) tpsSplin 1.20, department of ecology and evolution, SUNY. Stony Brook, New York

    Google Scholar 

  53. Rohlf JF (2013) tpsDig 2.17, department of ecology and evolution, SUNY. Stony Brook, New York

    Google Scholar 

  54. Rohlf JF (2014) tpsRelw 1.54, department of ecology and evolution, SUNY. Stony Brook, New York

    Google Scholar 

  55. Scheperjans F, Hermann K, Eickhoff SB, Amunts K, Schleicher A, Zilles K (2008a) Observer-independent cytoarchitectonic mapping of the human superior parietal cortex. Cerebral Cortex 18:846–867

    Article  PubMed  Google Scholar 

  56. Scheperjans F, Eickhoff SB, Hömke L, Mohlberg H, Hermann K, Amunts K, Zilles K (2008b) Probabilistic maps, morphometry, and variability of cytoarchitectonic areas in the human superior parietal cortex. Cereb Cortex 18:2141–2157

    Article  PubMed  PubMed Central  Google Scholar 

  57. Schneider D, Slaughter VP, Becker SI, Dux PE (2014) Implicit false-belief processing in the human brain. Neuroimage 101:268–275

    Article  PubMed  Google Scholar 

  58. Scott N, Neubauer S, Hublin JJ, Gunz P (2014) A shared pattern of postnatal endocranial development in extant hominoids. Evol Biol 41:572–594

    Article  Google Scholar 

  59. Sherwood CC, Rilling JK, Holloway RL, Hof PR (2009) Evolution of the brain in humans—specializations in a comparative perspective. In: Binder MD, Hirokawa N, Windhorst U, Hirsch MC (eds) Encyclopedia of neuroscience. Springer-Verlag, Berlin, pp 1334–1338

    Chapter  Google Scholar 

  60. Sotero RC, Iturria-Medina Y (2011) From blood oxygenation level dependent (BOLD) signals to brain temperature maps. B Math Biol 73:2731–2747

    CAS  Article  Google Scholar 

  61. Strait DS, Grine FE (2004) Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. J Hum Evol 47:399–452

    Article  PubMed  Google Scholar 

  62. Tomasi D, Wang GJ, Volkow ND (2013) Energetic cost of brain functional connectivity. Proc Natl Acad Sci USA 110:13642–13647

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. Utevsky AV, Smith DV, Huettel SA (2014) Precuneus is a functional core of the default-mode network. J Neurosci 34:932–940

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Wagner GP (1984) On the eigenvalue distribution of genetic and phenotypic dispersion matrices: evidence for a nonrandom organization of quantitative character variation. J Math Biol 21:77–95

    Article  Google Scholar 

  65. Wood B (2000) Investigating human evolutionary history. J Anat 197:3–17

    Article  PubMed  PubMed Central  Google Scholar 

  66. Zelditch ML, Swidersky DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists. Elsevier, San Diego

    Google Scholar 

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Acknowledgments

This work was supported by National Institutes of Health Grants P01AG026423 and National Center for Research Resources P51RR165 (superceded by the Office of Research Infrastructure Programs/OD P51OD11132), by the John Templeton Foundation (award 40463), and by the Center for Behavioral Neuroscience. EB is funded by the Spanish Government (CGL2012-38434-C03-02/03) and by the Italian Institute of Anthropology. We are grateful to an anonymous reviewer for comments and suggestions on an earlier version of this article.

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Correspondence to James K. Rilling.

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Bruner, E., Preuss, T.M., Chen, X. et al. Evidence for expansion of the precuneus in human evolution. Brain Struct Funct 222, 1053–1060 (2017). https://doi.org/10.1007/s00429-015-1172-y

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Keywords

  • Parietal lobes
  • Human evolution
  • Evolutionary neuroanatomy
  • Morphometrics