Evolution of increased glia-neuron ratios in the human frontal cortex

Chet C. Sherwood, Cheryl D. Stimpson, Mary Ann Raghanti, Derek E. Wildman, Monica Uddin, Lawrence I. Grossman, Morris Goodman, John C. Redmond, Christopher J. Bonar, Joseph M. Erwin, Patrick R. Hof

Research output: Contribution to journalArticlepeer-review

285 Scopus citations

Abstract

Evidence from comparative studies of gene expression and evolution suggest that human neocortical neurons may be characterized by unusually high levels of energy metabolism. The current study examined whether there is a disproportionate increase in glial cell density in the human frontal cortex in comparison with other anthropoid primate species (New World monkeys. Old World monkeys, and hominoids) to support greater metabolic demands. Among 18 species of anthropoids, humans displayed the greatest departure from allometric scaling expectations for the density of glia relative to neurons in layer II/III of dorsolateral prefrontal cortex (area 9L). However, the human glia-neuron ratio in this prefrontal region did not differ significantly from allometric predictions based on brain size. Further analyses of glia-neuron ratios across frontal areas 4, 9L, 32, and 44 in a sample of humans, chimpanzees, and macaque monkeys showed that regions involved in specialized human cognitive functions, such as "theory of mind" (area 32) and language (area 44) have not evolved differentially higher requirements for metabolic support. Taken together, these findings suggest that greater metabolic consumption of human neocortical neurons relates to the energetic costs of maintaining expansive dendritic arbors and long-range projecting axons in the context of an enlarged brain.

Original languageEnglish
Pages (from-to)13606-13611
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume103
Issue number37
DOIs
StatePublished - 12 Sep 2006

Keywords

  • Allometry
  • Brain energy metabolism
  • Human evolution
  • Language evolution
  • Prefrontal cortex

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