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8 The Remarkable, Yet Not Extraordinary, Human Brain as a Scaled-Up Primate Brain and Its Associated Cost--Suzana Herculano-Houzel
Pages 127-148

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From page 127...
... 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 Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, 21941-902, Rio de Janeiro, Brazil; and Instituto Nacional de Neurociência Translacional, Instituto Nacional de Ciência e Tecnologia/Ministério de Ciência e Tecnologia, 04023-900, Sao Paulo, Brazil. E-mail: suzanahh@gmail.com.
From page 128...
... Humans also do not rank first, or even close to first, in relative brain size (expressed as a percentage of body mass) , in absolute size of the cerebral cortex, or in gyrification (Hofman, 1985)
From page 129...
... Such comparisons are based on the notion, implicit in most comparative studies to date, that different brains are just scaled-up or scaled-down versions of a common basic plan, such that larger brains always have more neurons than smaller brains and two brains of a similar size always have comparable numbers of neurons. However, this notion is in disagreement with the observation that animals of similar brain size but belonging to different mammalian orders, such as the cow and the chimpanzee (both at about 400 g of brain mass)
From page 130...
... ; the concerted scaling across mammalian brains of numbers of neurons in the cerebral cortex and cerebellum, despite the increase in relative size of the former in larger brains; the constraints imposed by the primate neuronal scaling rules on cortical connectivity; the relationship between brain metabolism and number of neurons; and, finally, how humans compare with other mammals in these aspects, and what that recent evidence implies about human brain evolution. NOT ALL BRAINS ARE MADE THE SAME: NEURONAL SCALING RULES Testing the possibility that large brains have evolved as different functions of their numbers of neurons across mammalian orders became possible when we determined the numbers of cells that compose the brain of over 30 species belonging to three mammalian orders (HerculanoHouzel, 2011b)
From page 131...
... . Brain images from the Wisconsin and Michigan State Comparative Mammalian Brain Collections (www.
From page 132...
... . SHARED SCALING RULES: NONNEURONAL CELLS In contrast to the structure- and order-specific neuronal scaling rules, the numerical relationship between brain structure mass and the respective number of nonneuronal cells seems similar across all structures and species analyzed so far, spanning about 90 million years of evolution (Figs.
From page 133...
... FIGURE 8.2  Comparison of allometric exponents for total brain mass, cerebral cortex mass, cerebellar mass, and rest of brain mass as a function of numbers of neurons (Left) or nonneuronal cells (Right)
From page 135...
... (C) Mass of the cerebral cortex, cerebellum, and rest of brain varies as a similar function of their respective numbers of nonneuronal cells.
From page 136...
... . SHARED SCALING RULES: CEREBRAL CORTEX AND CEREBELLUM Larger brains possess larger cerebral cortices and cerebella but with a slightly faster increase in the size of the former compared with the latter, such that over five orders of magnitude, larger brains possess relatively larger cerebral cortices, whereas the relative size of the cerebellum fails to increase with brain size (Stephan et al., 1981)
From page 137...
... . Circles, relative mass and relative number of brain neurons in the cerebral cortex; squares, relative values for cerebellum.
From page 138...
... functions that corticocerebellar circuits mediate as brain size increased on multiple, independent occasions in evolution. The coordinated addition of neurons to cerebral cortex and cerebellum thus argues for coordinated corticocerebellar function and a joint evolution of the processing abilities of the two structures (Whiting and Barton, 2003; Ramnani et al., 2006; Balsters et al., 2010)
From page 139...
... , cortical volume should increase with its number of neurons raised to the power of 4/3. A decrease in connectivity in larger primate brains is compatible with the view that the cerebral cortex displays among its neurons the connectivity properties of a small-world network, that is, a network in which distance between nodes (neurons)
From page 140...
... . Broken down into the cerebral cortex, cerebellum, and rest of the brain, the neuronal scaling rules that apply to primate brains also apply to the human brain (Azevedo et al., 2009)
From page 141...
... Although direct measurements of numbers of neurons are not yet available for whole elephant and whale brains, one can speculate on how those numbers might differ depending on the particular neuronal scaling rules that apply. Hypothetically, if cetacean brains scaled similar to primate brains [which is unlikely, given their steep decrease in neuronal density with increasing brain size (Tower, 1954)
From page 142...
... Contrary to expectations, dividing total glucose use per minute in the cerebral cortex or whole brain (Karbowski, 2007) by the number of brain neurons revealed a remarkably constant average glucose use per neuron across the mouse, rat, squirrel, monkey, baboon, and human, with no significant relationship to neuronal density and, therefore, to average neuronal size (Herculano-Houzel, 2011c)
From page 143...
... in the cerebral cortex (circles) , cerebellum (squares)
From page 144...
... That this represents an enormous 25% of the total body energetic cost is simply a result of the "economical" neuronal scaling rules that apply to primates in comparison to rodents, and probably to other mammals in general: For a similar brain size, more neurons will be found in a primate brain than in possibly any other mammalian brain (Herculano-Houzel, 2009, 2011a)
From page 145...
... . The evolution of the hominin brain, and of the human brain in particular, may thus have involved two parallel but not necessarily related phenomena: an increase in brain size and number of neurons, obeying the same cellular scaling rules that apply to other primates, and a moderate increase in body size, compared with gorillas and orangutans, whose body size increased greatly compared with other primates that diverged
From page 146...
... There is, however, an additional possibility to be explored, and that is that great apes do not have larger brains to match their larger bodies because they cannot afford the metabolic cost of supporting the larger number of neurons. The great apes lineage appears to have favored marked increases in body size rather than brain size from the common ancestor with the Homo lineage, whereas the Homo lineage seems to have favored a large brain, with a large number of neurons, instead of a large body.
From page 147...
... CONCLUSION: REMARKABLE, YET NOT EXTRAORDINARY Despite our ongoing efforts to understand biology under the light of evolution, we have often resorted to considering the human brain as an outlier to justify our cognitive abilities, as if evolution applied to all species except humans. Remarkably, all the characteristics that appeared to single out the human brain as extraordinary, a point off the curve, can now, in retrospect, be understood as stemming from comparisons against body size with the underlying assumptions that all brains are uniformly scaled-up or scaled-down versions of each other and that brain size (and, hence, number of neurons)
From page 148...
... 148 / Suzana Herculano-Houzel are taught in textbooks. The human brain has just the number of neurons and nonneuronal cells that would be expected for a primate brain of its size, with the same distribution of neurons between its cerebral cortex and cerebellum as in other species, despite the relative enlargement of the former; it costs as much energy as would be expected from its number of neurons; and it may have been a change from a raw diet to a cooked diet that afforded us its remarkable number of neurons, possibly responsible for its remarkable cognitive abilities.


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