Abstract

Quantitative analysis of the cellular composition of rodent, primate and eulipotyphlan brains has shown that non-neuronal scaling rules are similar across these mammalian orders that diverged about 95 million years ago, and therefore appear to be conserved in evolution, while neuronal scaling rules appear to be free to vary in evolution in a clade-specific manner. Here we analyze the cellular scaling rules that apply to the brain of afrotherians, believed to be the first clade to radiate from the common eutherian ancestor. We find that afrotherians share non-neuronal scaling rules with rodents, primates and eulipotyphlans, as well as the coordinated scaling of numbers of neurons in the cerebral cortex and cerebellum. Afrotherians share with rodents and eulipotyphlans, but not with primates, the scaling of number of neurons in the cortex and in the cerebellum as a function of the number of neurons in the rest of the brain. Afrotheria also share with rodents and eulipotyphlans the neuronal scaling rules that apply to the cerebral cortex. Afrotherians share with rodents, but not with eulipotyphlans nor primates, the neuronal scaling rules that apply to the cerebellum. Importantly, the scaling of the folding index of the cerebral cortex with the number of neurons in the cerebral cortex is not shared by either afrotherians, rodents, or primates. The sharing of some neuronal scaling rules between afrotherians and rodents, and of some additional features with eulipotyphlans and primates, raise the interesting possibility that these shared characteristics applied to the common eutherian ancestor. In turn, the clade-specific characteristics that relate to the distribution of neurons along the surface of the cerebral cortex and to its degree of gyrification suggest that these characteristics compose an evolutionarily plastic suite of features that may have defined and distinguished mammalian groups in evolution.

Highlights

  • Mammalian brain size varies by a factor of approximately 100,000 across species (Tower, 1954; Stolzenburg et al, 1989)

  • Here we find that the brains of small afrotherian mammals gain neurons more slowly than they gain mass, with decreasing neuronal densities in the cerebral cortex and cerebellum that indicate an increase in the average size of the neurons in these structures

  • The cerebral cortex and the cerebellum gain neurons in relation to the rest of brain at the same rate in Afrotheria as in Glires and Eulipotyphla, which is more slowly than the rate found in primates (Herculano-Houzel, 2011b)

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Summary

Introduction

Mammalian brain size varies by a factor of approximately 100,000 across species (Tower, 1954; Stolzenburg et al, 1989). Comparative studies have traditionally used volume or surface measurements to investigate this variation (Jerison, 1985; Haug, 1987; Zhang and Sejnowski, 2000), resting upon the assumption that, regarding cellular composition, all mammalian brains are scaled versions of the same model. A recent methodological development - the isotropic fractionator (Herculano-Houzel and Lent, 2005)— allows for the absolute number of neurons and non-neurons in anatomically defined brain regions to be readily quantified. This is a non-stereological method that yields similar results to stereology in a smaller amount of time (Bahney and von Bartheld, 2014). Studies employing the isotropic fractionator have revealed that cellular scaling rules are different both across different structures within the same brain and across mammalian orders, making the use of volume or surface as a proxy for cellular composition misleading (Herculano-Houzel et al, 2006, 2007; Sarko et al, 2009; Gabi et al, 2010)

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