No relative expansion of the number of prefrontal neurons in primate and human evolution
Mariana Gabi a,b,c, Kleber Neves a,b, Carolinne Masseron a,b, Pedro F. M. Ribeiro a,b, Lissa Ventura-Antunes a,b, Laila Torres d,e, Bruno Mota f, Jon H. Kaas c,1, and Suzana Herculano-Houzel a,b,c,g,1
Author Affiliations
aInstituto de Ciências Morfológicas, Universidade Federal do Rio De Janeiro, 21941-901, Rio de Janeiro, Brazil;
bInstituto Nacional de Neurociência Translacional, 04023-900, Sao Paulo, Brazil;
cDepartment of Psychology, Vanderbilt University, Nashville, TN 37240;
dUniversidade Federal de São Paulo, 04021-001, Sao Paulo, Brazil;
eMuseu Paraense Emílio Goeldi, 66040-170, Belem, Brazil;
fInstituto de Física, Universidade Federal do Rio De Janeiro, 21941-901, Rio de Janeiro, Brazil;
gDepartment of Biological Sciences, Vanderbilt University, Nashville, TN 37235
Contributed by Jon H. Kaas, June 29, 2016 (sent for review February 29, 2016; reviewed by Robert A. Barton and Randy L. Buckner)
Significance
Human brain evolution is often considered synonymous with cortical expansion, in particular of the prefrontal cortex, a cortical region required for our remarkable cognitive abilities such as personality expression, planning, and decision making. In this study, we show that the expansion of numbers of cortical neurons in human and nonhuman primate evolution occurred in a similar manner across the cortex, without an increase in the relative number of neurons in the prefrontal region, and without a relative increase in the number of cells in the prefrontal white matter. One thing that distinguishes the human brain from other primate brains is thus not the relative size of its prefrontal cortex but its absolute number of neurons.
Abstract
Human evolution is widely thought to have involved a particular expansion of prefrontal cortex. This popular notion has recently been challenged, although controversies remain. Here we show that the prefrontal region of both human and nonhuman primates holds about 8% of cortical neurons, with no clear difference across humans and other primates in the distribution of cortical neurons or white matter cells along the anteroposterior axis. Further, we find that the volumes of human prefrontal gray and white matter match the expected volumes for the number of neurons in the gray matter and for the number of other cells in the white matter compared with other primate species. These results indicate that prefrontal cortical expansion in human evolution happened along the same allometric trajectory as for other primate species, without modification of the distribution of neurons across its surface or of the volume of the underlying white matter. We thus propose that the most distinctive feature of the human prefrontal cortex is its absolute number of neurons, not its relative volume.
cortical expansion evolution number of neurons primate prefrontal cortex
Footnotes
1To whom correspondence may be addressed. Email: jon.h.kaas@vanderbilt.edu or suzana.herculano@vanderbilt.edu.
Author contributions: M.G., J.H.K., and S.H.-H. designed research; M.G., K.N., C.M., P.F.M.R., and L.V.-A. performed research; L.T., J.H.K., and S.H.-H. contributed new reagents/analytic tools; M.G., B.M., and S.H.-H. analyzed data; and M.G., J.H.K., and S.H.-H. wrote the paper.
Reviewers: R.A.B., Durham University; R.L.B., Harvard University.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1610178113/-/DCSupplemental.
FREE PDF GRATIS: PNAS
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EXCERPT FROM SCIENCE DAILY/EXCERTO DO SCIENCE DAILY:
"People need to drop the idea that the human brain is exceptional," said Vanderbilt University neuroscientist Suzana Herculano-Houzel, who directed the study. "Our brain is basically a primate brain. Because it is the largest primate brain, it does have one distinctive feature: It has the highest number of cortical neurons of any primate. Humans have 16 billion compared with 9 billion in gorillas and orangutans and six-to-seven billion in chimpanzees. It is remarkable, but it is not exceptional."
"People need to drop the idea that the human brain is exceptional," said Vanderbilt University neuroscientist Suzana Herculano-Houzel, who directed the study. "Our brain is basically a primate brain. Because it is the largest primate brain, it does have one distinctive feature: It has the highest number of cortical neurons of any primate. Humans have 16 billion compared with 9 billion in gorillas and orangutans and six-to-seven billion in chimpanzees. It is remarkable, but it is not exceptional."
