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Prefrontal white matter volume is disproportionately larger in humans than in other primates

Nature Neuroscience volume 8, pages 242–252 (2005)Cite this article

Abstract

Determining how the human brain differs from nonhuman primate brains is central to understanding human behavioral evolution. There is currently dispute over whether the prefrontal cortex, which mediates evolutionarily interesting behaviors, has increased disproportionately. Using magnetic resonance imaging brain scans from 11 primate species, we measured gray, white and total volumes for both prefrontal and the entire cerebrum on each specimen (n = 46). In relative terms, prefrontal white matter shows the largest difference between human and nonhuman, whereas gray matter shows no significant difference. This suggests that connectional elaboration (as gauged by white matter volume) played a key role in human brain evolution.

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Figure 1: Three-dimensional renderings, from left lateral, anterior, and superior views (in correct left-right orientation as shown), indicating the cortical portions designated prefrontal in this study for a representative of each species.
Figure 2: Percentage of cerebral volume that is prefrontal for individual specimens in 11 primate species.
Figure 3: Relationship between the proportion of total white matter volume anterior to the corpus callosum (prefrontal percentage white) compared with proportion of total gray matter anterior to the corpus callosum (prefrontal percentage gray).
Figure 4: Relationships between prefrontal and non-prefrontal cerebral volume for all 46 specimens from 11 primate species.
Figure 5: Segmentation examples.
Figure 6: Effect of blurring on segmentation.

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References

  1. Deacon, T.W. The Symbolic Species: the Co-evolution of Language and the Brain (Norton, New York, 1997).

  2. Hofman, M.A. Energy metabolism, brain size, and longevity in mammals. Q. Rev. Biol. 58, 495–512 (1983).

    Article  CAS  Google Scholar 

  3. Harvey, P.H. & Clutton-Brock, T.H. Life history variation in primates. Evolution Int. J. Org. Evolution 39, 559–581 (1985).

    Article  Google Scholar 

  4. Stephan, H., Frahm, H. & Baron, G. New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol. (Basel) 35, 1–29 (1981).

    Article  CAS  Google Scholar 

  5. Holloway, R.L. The failure of the gyrification index (GI) to account for volumetric reorganization in the evolution of the human brain. J. Hum. Evol. 22, 163–170 (1992).

    Article  Google Scholar 

  6. Damasio, A.R. The frontal lobes. in Clinical Neuropsychology (eds. Heilman, K. & Valenstein, E.) 339–375 (Oxford University Press, Oxford, 1985).

    Google Scholar 

  7. Goldman-Rakic, P.S. The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. Phil. Trans. R. Soc. Lond. B Biol. Sci. 351, 1445–1453 (1996).

    Article  CAS  Google Scholar 

  8. Fuster, J.M. The prefrontal cortex, mediator of cross-temporal contingencies. Hum. Neurobiol. 4, 169–179 (1985).

    CAS  PubMed  Google Scholar 

  9. Gabrieli, J.D., Poldrack, R.A. & Desmond, J.E. The role of left prefrontal cortex in language and memory. Proc. Natl. Acad. Sci. USA 95, 906–913 (1998).

    Article  CAS  Google Scholar 

  10. Thompson-Schill, S.L. et al. Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. Proc. Natl. Acad. Sci. USA 95, 15855–15860 (1998).

    Article  CAS  Google Scholar 

  11. Vendrell, P. et al. The role of prefrontal regions in the Stroop task. Neuropsychologia 33, 341–352 (1995).

    Article  CAS  Google Scholar 

  12. de Bruin, J.P.C. Social behavior and the prefrontal cortex. in Progress in Brain Research (eds. Uylings, H.B.M. et al.) 485–497 (Elsevier, New York, 1990).

    Google Scholar 

  13. Von Bonin, G. The frontal lobe of primates: cytoarchitectural studies. in The Frontal Lobes: Proceedings of the Association for Research in Nervous and Mental Disease, December 12 and 13, 1947 67–83 (Williams & Wilkins, Baltimore, 1948).

    Google Scholar 

  14. Holloway, R.L. The evolution of the primate brain: some aspects of quantitative relations. Brain Res. 7, 121–172 (1968).

    Article  Google Scholar 

  15. Semendeferi, K., Lu, A., Schenker, N. & Damasio, H. Humans and great apes share a large frontal cortex. Nat. Neurosci. 5, 272–276 (2002).

    Article  CAS  Google Scholar 

  16. Bush, E.C. & Allman, J.M. The scaling of frontal cortex in primates and carnivores. Proc. Natl. Acad. Sci. USA 101, 3962–3966 (2004).

    Article  CAS  Google Scholar 

  17. Blinkov, S.M. & Glezer, I.I. The Human Brain in Figures and Tables (Plenum, New York, 1968).

    Google Scholar 

  18. Brodmann, K. Vergleichende Lokalisationsiehre der Grosshirnrinde in ihren Prinzipien Dargestellt auf Grund des Zellenbaues (Verlag, Leipzig, 1909).

    Google Scholar 

  19. Brodmann, K. Neue Ergebnisse über die vergleichende histologische localisation der grosshirnrinde mit besonderer berücksichtigung des stirnhirns. Anat. Anz. 41 (suppl.), 157–216 (1912).

    Google Scholar 

  20. Armstrong, E., Zilles, K., Curtis, M. & Schleicher, A. Cortical folding, the lunate sulcus and the evolution of the human brain. J. Hum. Evol. 20, 341–348 (1991).

    Article  Google Scholar 

  21. Semendeferi, K., Armstrong, E., Schleicher, A., Zilles, K. & Van Hoesen, G.W. Prefrontal cortex in humans and apes: a comparative study of area 10. Am. J. Phys. Anthropol. 114, 224–241 (2001).

    Article  CAS  Google Scholar 

  22. Rilling, J.K. & Insel, T.R. The primate neocortex in comparative perspective using magnetic resonance imaging. J. Hum. Evol. 37, 191–223 (1999).

    Article  CAS  Google Scholar 

  23. McBride, T., Arnold, S.E. & Gur, R.C. A comparative volumetric analysis of the prefrontal cortex in human and baboon MRI. Brain Behav. Evol. 54, 159–166 (1999).

    Article  CAS  Google Scholar 

  24. Uylings, H.B.M. & Van Eden, C.G. Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. in Progress in Brain Research, Vol. 85 (eds. Uylings, H.B M., Van Eden, C.G., De Bruin, J.P.C., Corner, M.A. & Feenstra, M.G.P.) 31–62 (Elsevier, New York 1990).

    Google Scholar 

  25. Semendeferi, K., Armstrong, E., Schleicher, A., Zilles, K. & Van Hoesen, G.W. Limbic frontal cortex in hominoids: a comparative study of area 13. Am. J. Phys. Anthropol. 106, 129–155 (1998).

    Article  CAS  Google Scholar 

  26. Fuster, J.M. The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe edn. 2 (Raven, New York, 1989).

  27. Ringo, J.L. Neuronal interconnection as a function of brain size. Brain Behav. Evol. 38, 1–6 (1991).

    Article  CAS  Google Scholar 

  28. Roberts, N., Puddephat, M.J. & McNulty, V. The benefit of stereology for quantitative radiology. Br. J. Radiol. 73, 679–697 (2000).

    Article  CAS  Google Scholar 

  29. Holloway, R.L. Brief communication: how much larger is the relative volume of area 10 of the prefrontal cortex in humans? Am. J. Phys. Anthropol. 118, 399–401 (2002).

    Article  Google Scholar 

  30. Melhem, E.R. et al. Diffusion tensor MR imaging of the brain and white matter tractography. AJR Am. J. Roentgenol. 178, 3–16 (2002).

    Article  Google Scholar 

  31. Rumbaugh, D.M., Savage-Rumbaugh, E.S. & Wasburn, D.A. Toward a new outlook on primate learning and behavior: complex learning and emergent processes in comparative perspective. Jpn. Psychol. Res. 38, 113–125 (1996).

    Article  CAS  Google Scholar 

  32. Krubitzer, L. The organization of neocortex in mammals: are species differences really so different? Trends Neurosci. 18, 408–417 (1995).

    Article  CAS  Google Scholar 

  33. Schoenemann, P.T., Budinger, T.F., Sarich, V.M. & Wang, W.S.-Y. Brain size does not predict general cognitive ability within families. Proc. Natl. Acad. Sci. USA 97, 4932–4937 (2000).

    Article  CAS  Google Scholar 

  34. Thompson, P.M. et al. Genetic influences on brain structure. Nat. Neurosci. 4, 1253–1258 (2001).

    Article  CAS  Google Scholar 

  35. Changizi, M.A. Principles underlying mammalian neocortical scaling. Biol. Cybern. 84, 207–215 (2001).

    Article  CAS  Google Scholar 

  36. Schoenemann, P.T. Syntax as an emergent characteristic of the evolution of semantic complexity. Minds Machines 9, 309–346 (1999).

    Article  Google Scholar 

  37. Savage-Rumbaugh, E.S. & Rumbaugh, D.M. The emergence of language. in Tools, Language and Cognition in Human Evolution (eds. Gibson, K.R. & Ingold, T.) 86–108 (Cambridge Univ. Press, Cambridge, 1993).

    Google Scholar 

  38. Aboitiz, F. & Garcia, V.R. The evolutionary origin of the language areas in the human brain. A neuroanatomical perspective. Brain Res. Brain Res. Rev. 25, 381–396 (1997).

    Article  CAS  Google Scholar 

  39. Lieberman, P. On the nature and evolution of the neural bases of human language. Yearb. Phys. Anthropol. 45, 36–62 (2002).

    Article  Google Scholar 

  40. Dunbar, R. Grooming, Gossip and the Evolution of Language (Faber and Faber, London, 1996).

    Google Scholar 

  41. Humphrey, N. The social function of intellect. in Consciousness Regained 14–28 (Oxford Univ. Press, Oxford, 1984).

    Google Scholar 

  42. Gray, J.R. & Thompson, P.M. Neurobiology of intelligence: science and ethics. Nat. Rev. Neurosci. 5, 471–482 (2004).

    Article  CAS  Google Scholar 

  43. Wynn, T. Archaeology and cognitive function. Behav. Brain Sci. 25, 389–438 (2002).

    PubMed  Google Scholar 

  44. Holloway, R.L. Toward a synthetic theory of human brain evolution. in Origins of the Human Brain (eds. Changeux, J.-P. & Chavaillon, J.) 42–54 (Clarendon, Oxford, 1995).

    Google Scholar 

  45. Zhang, Y., Brady, M. & Smith, S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imaging 20, 45–57 (2001).

    Article  CAS  Google Scholar 

  46. Guillemaud, R. & Brady, M. Estimating the bias field of MR images. IEEE Trans. Med. Imaging 16, 238–251 (1997).

    Article  CAS  Google Scholar 

  47. Elias, H., Hennig, A. & Schwartz, D.E. Stereology: applications to biomedical research. Physiol. Rev. 51, 158–199 (1971).

    Article  CAS  Google Scholar 

  48. Ankney, C.D. Sex differences in relative brain size: the mismeasure of woman, too? Intelligence 16, 329–336 (1992).

    Article  Google Scholar 

  49. Falk, D., Froese, N., Sade, D.S. & Dudek, B.C. Sex differences in brain/body relationships of Rhesus monkeys and humans. J. Hum. Evol. 36, 233–238 (1999).

    Article  CAS  Google Scholar 

  50. Jerison, H.J. Allometry, brain size, cortical surface, and convolutedness. in Primate Brain Evolution (eds. Armstrong, E. & Falk, D.) 77–84 (Plenum, New York, 1982).

    Chapter  Google Scholar 

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Acknowledgements

We thank J. Rilling and T. Insel for allowing us to analyze their collection of primate brain scans, and M. Grossman for six human male brains. S. Langin-Hooper and P. Silverman helped with data processing. We also thank the subjects who allowed themselves to be scanned.

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Authors and Affiliations

  1. Department of Anthropology, University of Pennsylvania, 3260 South St., Philadelphia, 19104-6398, Pennsylvania, USA

    P Thomas Schoenemann, Michael J Sheehan & L Daniel Glotzer

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  1. P Thomas Schoenemann
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Correspondence to P Thomas Schoenemann.

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Supplementary information

Supplementary Table 1

Effects of blurring on volume estimation. (PDF 40 kb)

Supplementary Table 2

Average absolute and relative voxel sizes. (PDF 48 kb)

Supplementary Table 3

Effects of increasing voxel size on volume estimation. (PDF 57 kb)

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Schoenemann, P., Sheehan, M. & Glotzer, L. Prefrontal white matter volume is disproportionately larger in humans than in other primates. Nat Neurosci 8, 242–252 (2005). https://doi.org/10.1038/nn1394

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