Not all brains are made the same: new views on brain scaling in evolution

Abstract

Evolution has generated mammalian brains that vary by a factor of over 100,000 in mass. Despite such tremendous diversity, brain scaling in mammalian evolution has tacitly been considered a homogeneous phenomenon in terms of numbers of neurons, neuronal density, and the ratio between glial and neuronal cells, with brains of different sizes viewed as similarly scaled-up or scaled-down versions of a shared basic plan. According to this traditional view, larger brains would have more neurons, smaller neuronal densities (and, hence, larger neurons), and larger glia/neuron ratios than smaller brains. Larger brains would also have a cerebellum that maintains its relative size constant and a cerebral cortex that becomes relatively larger to the point that brain evolution is often equated with cerebral cortical expansion. Here I review our recent data on the numbers of neuronal and nonneuronal cells that compose the brains of 28 mammalian species belonging to 3 large clades (Eulipotyphla, Glires, and Primata, plus the related Scandentia) and show that, contrary to the traditional notion of shared brain scaling, both the cerebral cortex and the cerebellum scale in size as clade-specific functions of their numbers of neurons. As a consequence, neuronal density and the glia/neuron ratio do not scale universally with structure mass and, most importantly, mammalian brains of a similar size can hold very different numbers of neurons. Remarkably, the increased relative size of the cerebral cortex in larger brains does not reflect an increased relative concentration of neurons in the structure. Instead, the cerebral cortex and cerebellum appear to gain neurons coordinately across mammalian species. Brain scaling in evolution, hence, should no longer be equated with an increasing dominance of the cerebral cortex but rather with the concerted addition of neurons to both the cerebral cortex and the cerebellum. Strikingly, all brains appear to gain nonneuronal cells in a similar fashion, with relatively constant nonneuronal cell densities. As a result, while brain size can no longer be considered a proxy for the number of brain neurons across mammalian brains in general, it is actually a very good proxy for the number of nonneuronal cells in the brain. Together, these data point to developmental mechanisms that underlie evolutionary changes in brain size in mammals: while the rules that determine how neurons are added to the brain during development have been largely free to vary in mammalian evolution across clades, the rules that determine how other cells are added in development have been mostly constrained and to this day remain largely similar both across brain structures and across mammalian groups.