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

Abstract

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.

Fig. 1.

Large brains appear several times in the mammalian radiation. Example species are illustrated for each major mammalian group. The mammalian radiation is based on the findings of Murphy et al. (18) and Kaas (19). Brain images are from the University of Wisconsin and Michigan State Comparative Mammalian Brain Collections (www.brainmuseum.org).

Fig. 2.

Comparison of allometric exponents for total brain mass, cerebral cortex mass, cerebellar mass, and the rest of the brain mass as a function of numbers of neurons (Upper) or nonneuronal cells (Lower). Exponents, given at the base of the radiation of each individual group (Glires, Primata/Scandentia, and Eulipotyphla), are illustrated by the intensity of the shading. Data are from studies by Herculano-Houzel and her colleagues (–27); exponents are from a study by Herculano-Houzel (20).

Fig. 3.

Shared nonneuronal scaling rules and structure- and order-specific neuronal scaling rules for mammalian brains. Each point represents the average values for one species (insectivores, blue; rodents, green; primates, red; Scandentia, orange). Arrows point to human data points, circles represent the cerebral cortex, squares represent the cerebellum, and triangles represent the rest of the brain (excluding the olfactory bulb). (A) Clade- and structure-specific scaling of brain structure mass as a function of numbers of neurons. Allometric exponents: cerebral cortex: 1.699 (Glires), 1.598 (insectivores), 1.087 or linear (primates); cerebellum: 1.305 (Glires), 1.028 or linear (insectivores), 0.976 or linear (primates); rest of the brain: 1.568 (Glires), 1.297 (insectivores), 1.198 (or 1.4 when corrected for phylogenetic relatedness in the dataset, primates). (B) Neuronal cell densities scale differently across structures and orders but are always larger in primates than in Glires. Allometric exponents: cerebral cortex: −0.424 (Glires), −0.569 (insectivores), −0.168 (primates); cerebellum: −0.271 (Glires), not significant (insectivores and primates); rest of the brain: −0.467 (Glires), not significant (insectivores), −0.220 (primates). (C) Mass of the cerebral cortex, cerebellum, and rest of the brain varies as a similar function of their respective numbers of nonneuronal cells. Allometric exponents: cerebral cortex: 1.132 (Glires), 1.143 (insectivores), 1.036 (primates); cerebellum: 1.002 (Glires), 1.094 (insectivores), 0.873 (primates); rest of the brain: 1.073 (Glires), 0.926 (insectivores), 1.065 (primates). (D) Average density of nonneuronal cells in each structure does not vary systematically with structure mass across species. Power functions are not plotted so as not to obscure the data points. Allometric exponents are from a study by Herculano-Houzel (20); data are from studies by Herculano-Houzel and her colleagues (–27).

Fig. 4.

Coordinated scaling of the number of neurons in the cerebral cortex and cerebellum of mammals. (A) Number of neurons in the cerebellum covaries with the number of neurons in the cerebral cortex across all species in a way that can be described as a linear function of slope 4.2 (P < 0.0001, r² = 0.995). (B) Increased relative cortical mass does not reflect an increased relative number of brain neurons. Each point represents the average values for one species (insectivores, blue; rodents, green; primates, red; Scandentia, orange). Circles represent relative mass and relative number of brain neurons in the cerebral cortex; squares represent relative values for the cerebellum. All Spearman correlation P values are >0.2. Data are from studies by Herculano-Houzel and her colleagues (–27). h, human data points.

Fig. 5.

G/N ratio scales differently across structures and orders with structure mass, but scales homogeneously with neuronal density. Each point represents the average other cell/neuron ratio (which approximates the G/N ratio) and structure mass (A) or neuronal density (B) in the cerebral cortex (circles), cerebellum (squares), or rest of brain (triangles) of a species. Notice that in contrast to the scattered distribution across species and structures in A, data points are aligned across species and structures in the lower plot, suggesting that it is smaller neuronal densities (i.e., larger average neuronal cell size), rather than larger structure mass, that is accompanied by a larger G/N ratio. Data are from studies by Herculano-Houzel and her colleagues (–27).

Fig. 6.

Total brain metabolism (measured as micromoles of glucose consumed per minute) scales as a linear function of the total number of neurons in the brain across rodents and primates alike, including humans (arrow). The function plotted is a power function of exponent 0.988, not significantly different from 1.0. Data are from a study by Herculano-Houzel (70).