Evolution of Increased Glia-neuron Ratios in the Human Frontal Cortex
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 c...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2006-09, Vol.103 (37), p.13606-13611 |
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| creator | Sherwood, Chet C. Stimpson, Cheryl D. Raghanti, Mary Ann Wildman, Derek E. Uddin, Monica Grossman, Lawrence I. Goodman, Morris Redmond, John C. Bonar, Christopher J. Erwin, Joseph M. Hof, Patrick R. |
| description | 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. |
| doi_str_mv | 10.1073/pnas.0605843103 |
| format | Article |
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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.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0605843103</identifier><identifier>PMID: 16938869</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Biological Evolution ; Biological Sciences ; Brain ; Brain - anatomy & histology ; Brain - cytology ; Cell Count ; Chimpanzees ; Energy metabolism ; Evolution ; Frontal Lobe - cytology ; Frontal Lobe - metabolism ; Gene expression ; Hominids ; Humans ; Language ; Macaca ; Macaca - anatomy & histology ; Metabolism ; Monkeys ; Neocortex ; Neuroglia ; Neuroglia - cytology ; Neurons ; Neurons - cytology ; Organ Size ; Pan troglodytes - anatomy & histology ; Primates</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2006-09, Vol.103 (37), p.13606-13611</ispartof><rights>Copyright 2006 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Sep 12, 2006</rights><rights>2006 by The National Academy of Sciences of the USA 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c596t-ed30876c06e6d8b6cc01f92772e4f1e53748af3ae72f79ae99644991857e3eef3</citedby><cites>FETCH-LOGICAL-c596t-ed30876c06e6d8b6cc01f92772e4f1e53748af3ae72f79ae99644991857e3eef3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/103/37.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/30050302$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/30050302$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16938869$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sherwood, Chet C.</creatorcontrib><creatorcontrib>Stimpson, Cheryl D.</creatorcontrib><creatorcontrib>Raghanti, Mary Ann</creatorcontrib><creatorcontrib>Wildman, Derek E.</creatorcontrib><creatorcontrib>Uddin, Monica</creatorcontrib><creatorcontrib>Grossman, Lawrence I.</creatorcontrib><creatorcontrib>Goodman, Morris</creatorcontrib><creatorcontrib>Redmond, John C.</creatorcontrib><creatorcontrib>Bonar, Christopher J.</creatorcontrib><creatorcontrib>Erwin, Joseph M.</creatorcontrib><creatorcontrib>Hof, Patrick R.</creatorcontrib><title>Evolution of Increased Glia-neuron Ratios in the Human Frontal Cortex</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>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. 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| subjects | Animals Biological Evolution Biological Sciences Brain Brain - anatomy & histology Brain - cytology Cell Count Chimpanzees Energy metabolism Evolution Frontal Lobe - cytology Frontal Lobe - metabolism Gene expression Hominids Humans Language Macaca Macaca - anatomy & histology Metabolism Monkeys Neocortex Neuroglia Neuroglia - cytology Neurons Neurons - cytology Organ Size Pan troglodytes - anatomy & histology Primates |
| title | Evolution of Increased Glia-neuron Ratios in the Human Frontal Cortex |
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