The Scaling of White Matter to Gray Matter in Cerebellum and Neocortex

Bush, Eliot C.; Allman, John M.

doi:10.1159/000068880

Cited by 63 publications

(47 citation statements)

References 15 publications

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“…In the brain, too, certain scaling phenomena have been explained functionally. White matter hyperscales relative to gray matter in neocortex, and this has been seen as a consequence of the need to maintain connectivity as brain size increases or as a reflection of systematic changes in axon diameter (1,48).…”

Section: Discussionmentioning

confidence: 99%

The scaling of frontal cortex in primates and carnivores

Bush

Allman

2004

Proc. Natl. Acad. Sci. U.S.A.

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125

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Size has a profound effect on the structure of the brain. Many brain structures scale allometrically, that is, their relative size changes systematically as a function of brain size. Here we use independent contrasts analysis to examine the scaling of frontal cortex in 43 species of mammals including 25 primates and 15 carnivores. We find evidence for significant differences in scaling between primates and carnivores. Primate frontal cortex hyperscales relative to the rest of neocortex and the rest of the brain. The slope of frontal cortex contrasts on rest of cortex contrasts is 1.18 (95% confidence interval, 1.06 -1.30) for primates, which is significantly greater than isometric. It is also significantly greater than the carnivore value of 0.94 (95% confidence interval, 0.82-1.07). This finding supports the idea that there are substantial differences in frontal cortex structure and development between the two groups. C omparative neuroanatomists have long been interested in the relationship between size and brain structure. Early work focused on how the brain scales with the body, and how gross morphological characteristics such as cortical folding change with size (1, 2). More recently, emphasis has been put on the scaling of various brain structures with each other and with overall brain size (3-6).The scaling of frontal cortex presents an interesting case. From the beginning, workers have been drawn to this region because of the supposition that volume increases occurred in the line leading to humans. Brodmann's regio frontalis consisted of frontal cortex minus areas 4 and 6 and parts of the cingulate. He described a ''progressive'' expansion of this region in the primate line going from prosimians to humans, and argued that primates more closely related to humans have a disproportionally larger regio frontalis (7). However, primates more closely related to humans also have larger brains. The disproportionate expansion of the frontal region could be due to allometric scaling only.Von Bonin (8) explicitly argued that frontal cortex hyperscales with brain size, and man has ''precisely the frontal lobe which he deserves by virtue of the overall size of his brain''. A number of subsequent workers used allometric lines as a kind of standard for comparing whether human frontal cortex is bigger or smaller than one would expect for a similarly sized primate (9-11). However, neither Von Bonin nor later workers had adequate data or methods to establish whether frontal cortex hyperscaling is a regular and systematic relationship with size, or simply an artifact of grade differences. As was originally pointed out by Felsenstein (12), the phylogenetic structure of a sample of species can make it appear that there is a systematic relationship between two variables where none exists.To make the distinction between a series of grade shifts and systematic allometry, one must apply a method such as independent contrasts, which can factor out the effects of phylogeny (12). In addition, one must have data from a phylogenetical...

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Section: Discussionmentioning

confidence: 99%

The scaling of frontal cortex in primates and carnivores

Bush

Allman

2004

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

125

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“…First, we calculated total grey matter volume by multiplying the surface area estimates by 2 mm, which is a reasonable estimate of cortical grey matter thickness in both humans [36][37][38] and macaques [38]. We then estimated white matter volume (cm 3 ) from grey matter volume (cm 3 ) using a reduced major axis (RMA) regression equation, using anthropoid primate neocortical data from [39]: t 19 ¼ 56.28, p , 0.001, r 2 ¼ 0.994 log 10 white ¼20.81 (95% CI: 20.72 to 20.93) þ 1.32 (95% CI: 1.24 to 1.43) Â log 10 grey. These parameters do not fall outside the 95% confidence intervals of those associated with a PGLM regression model using a tree from the 10k Trees Project.…”

Section: Methodsmentioning

confidence: 99%

New insights into differences in brain organization between Neanderthals and anatomically modern humans

2013

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Previous research has identified morphological differences between the brains of Neanderthals and anatomically modern humans (AMHs). However, studies using endocasts or the cranium itself are limited to investigating external surface features and the overall size and shape of the brain. A complementary approach uses comparative primate data to estimate the size of internal brain areas. Previous attempts to do this have generally assumed that identical total brain volumes imply identical internal organization. Here, we argue that, in the case of Neanderthals and AMHs, differences in the size of the body and visual system imply differences in organization between the same-sized brains of these two taxa. We show that Neanderthals had significantly larger visual systems than contemporary AMHs (indexed by orbital volume) and that when this, along with their greater body mass, is taken into account, Neanderthals have significantly smaller adjusted endocranial capacities than contemporary AMHs. We discuss possible implications of differing brain organization in terms of social cognition, and consider these in the context of differing abilities to cope with fluctuating resources and cultural maintenance.

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“…The issue then becomes accounting for how the cerebral cortex increases in size faster than the cerebellum as both gain neurons coordinately. As examined next, this differential scaling is probably related to how connectivity through the underlying white matter scales in the two structures, one of which carries massive long-range connections across cerebral cortical areas both within and across the hemispheres that are essential for the operation of associative networks (35), whereas the other is mostly composed of centrifugal and centripetal connections, with associative connections mostly restricted to the gray matter of the cerebellum (36). As a result, the cerebral subcortical white matter gains volume faster than the cerebellar white matter in larger brains (36,37), because overall neuronal size (including dendrites and axonal arborizations) increases faster in the cerebral cortex than in the cerebellum, as both gain neurons coordinately.…”

Section: Shared Scaling Rules: Cerebral Cortex and Cerebellummentioning

confidence: 99%

The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost

Herculano‐Houzel

2012

Proc. Natl. Acad. Sci. U.S.A.

507

372

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Neuroscientists have become used to a number of “facts” about the human brain: It has 100 billion neurons and 10- to 50-fold more glial cells; it is the largest-than-expected for its body among primates and mammals in general, and therefore the most cognitively able; it consumes an outstanding 20% of the total body energy budget despite representing only 2% of body mass because of an increased metabolic need of its neurons; and it is endowed with an overdeveloped cerebral cortex, the largest compared with brain size. These facts led to the widespread notion that the human brain is literally extraordinary: an outlier among mammalian brains, defying evolutionary rules that apply to other species, with a uniqueness seemingly necessary to justify the superior cognitive abilities of humans over mammals with even larger brains. These facts, with deep implications for neurophysiology and evolutionary biology, are not grounded on solid evidence or sound assumptions, however. Our recent development of a method that allows rapid and reliable quantification of the numbers of cells that compose the whole brain has provided a means to verify these facts. Here, I review this recent evidence and argue that, with 86 billion neurons and just as many nonneuronal cells, the human brain is a scaled-up primate brain in its cellular composition and metabolic cost, with a relatively enlarged cerebral cortex that does not have a relatively larger number of brain neurons yet is remarkable in its cognitive abilities and metabolism simply because of its extremely large number of neurons.

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The Scaling of White Matter to Gray Matter in Cerebellum and Neocortex

Cited by 63 publications

References 15 publications

The scaling of frontal cortex in primates and carnivores

The scaling of frontal cortex in primates and carnivores

New insights into differences in brain organization between Neanderthals and anatomically modern humans

The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost

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