Coordinated scaling of cortical and cerebellar numbers of neurons

Abstract

While larger brains possess concertedly larger cerebral cortices and cerebella, the relative size of the cerebral cortex increases with brain size, but relative cerebellar size does not. In the absence of data on numbers of neurons in these structures, this discrepancy has been used to dispute the hypothesis that the cerebral cortex and cerebellum function and have evolved in concert and to support a trend towards neocorticalization in evolution. However, the rationale for interpreting changes in absolute and relative size of the cerebral cortex and cerebellum relies on the assumption that they reflect absolute and relative numbers of neurons in these structures across all species - an assumption that our recent studies have shown to be flawed. Here I show for the first time that the numbers of neurons in the cerebral cortex and cerebellum are directly correlated across 19 mammalian species of four different orders, including humans, and increase concertedly in a similar fashion both within and across the orders Eulipotyphla (Insectivora), Rodentia, Scandentia and Primata, such that on average a ratio of 3.6 neurons in the cerebellum to every neuron in the cerebral cortex is maintained across species. This coordinated scaling of cortical and cerebellar numbers of neurons provides direct evidence in favor of concerted function, scaling and evolution of these brain structures, and suggests that the common notion that equates cognitive advancement with neocortical expansion should be revisited to consider in its stead the coordinated scaling of neocortex and cerebellum as a functional ensemble.

Keywords: brain scaling; brain size; cerebellum; cerebral cortex; mosaic evolution; numbers of neurons.

Figure 1

Phylogenesis of the 19 species analyzed. Numbers in parentheses refer to brain mass (excluding olfactory bulb), and body mass. Data from Herculano-Houzel et al. (2006, 2007), Sarko et al. (2009) and Azevedo et al. (2009).

Figure 2

Discrepancy between the scaling of absolute and relative cortical and cerebellar mass. Each point represents the average values for one species (insectivores, orange; rodents, green; primates, red; scandentia, black), (A) cerebellar mass covaries with cerebral cortical mass in a similar fashion across Eulipotyphla (insectivore), rodent, scandentia and primate species. Power function exponents and 95% confidence intervals are indicated; all values of p < 0.01. The plotted power function applies to all species. The relationship for the ensemble of data is equally well fit with a linear function of slope 0.125 (p < 0.0001, r² = 1.000; not shown), (B) relative mass of the cerebral cortex (circles), shown as % of total brain mass, increases with total brain mass across all species, but relative cerebellar mass (squares) decreases slightly. Spearman correlation coefficients and p-values are shown. All data are from Herculano-Houzel et al. (2006, 2007), Azevedo et al. (2009) and Sarko et al. (2009).

Figure 3

Relative cortical and cerebellar mass does not reflect the relative number of brain neurons that each contains. Each point represents the average values for one species (insectivores, orange; rodents, green; primates, red; scandentia, black). Circles, relative mass and relative number of brain neurons in the cerebral cortex; squares, relative values for cerebellum. Spearman correlation coefficients and p-values are indicated. All data are from Herculano-Houzel et al. (2006, 2007), Azevedo et al. (2009) and Sarko et al. (2009).

Figure 4

Coordinated scaling of the number of neurons in the cerebral cortex and cerebellum of mammals. Each point represents the average values for one species. Eulipotyphla (insectivores), orange; rodents, green; primates, red; scandentia, black. (A) neuronal scaling rules relating structure mass and number of neurons (cerebral cortex, circles; cerebellum, squares). Power law exponents are indicated in the appropriate colors for Eulipotyphla, rodents, and combined scandentia and primates (all values of p < 0.01). (B) the 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). Slopes and r² values for insectivores, rodents, and combined scandentia and primates are indicated in different colors (all p < 0.01, except insectivores, for which p = 0.0463). All data are from Herculano-Houzel et al. (2006, 2007), Azevedo et al. (2009) and Sarko et al. (2009).

Figure 5

Average ratio between numbers of neurons in the cerebellum and in the cerebral cortex does not correlate with brain mass across species. Each point represents the average values for one species. Eulipotyphla (insectivores), orange; rodents, green; primates, red; scandentia, black. The average ratio ± standard deviation between number of neurons in the cerebellum and in the cerebral cortex within each order and among all 20 species are indicated in the corresponding colors. No correlation between cortex/cerebellar neuronal ratio and brain mass reaches significance (Spearman correlation, all p > 0.1). All data are from Herculano-Houzel et al. (2006, 2007), Azevedo et al. (2009) and Sarko et al. (2009).