Brain scaling in mammalian evolution as a consequence of concerted and mosaic changes in numbers of neurons and average neuronal cell size.

Suzana Herculano-Houzel,Paul R Manger,Jon H Kaas

doi:10.3389/fnana.2014.00077

Abstract

Enough species have now been subject to systematic quantitative analysis of the relationship between the morphology and cellular composition of their brain that patterns begin to emerge and shed light on the evolutionary path that led to mammalian brain diversity. Based on an analysis of the shared and clade-specific characteristics of 41 modern mammalian species in 6 clades, and in light of the phylogenetic relationships among them, here we propose that ancestral mammal brains were composed and scaled in their cellular composition like modern afrotherian and glire brains: with an addition of neurons that is accompanied by a decrease in neuronal density and very little modification in glial cell density, implying a significant increase in average neuronal cell size in larger brains, and the allocation of approximately 2 neurons in the cerebral cortex and 8 neurons in the cerebellum for every neuron allocated to the rest of brain. We also propose that in some clades the scaling of different brain structures has diverged away from the common ancestral layout through clade-specific (or clade-defining) changes in how average neuronal cell mass relates to numbers of neurons in each structure, and how numbers of neurons are differentially allocated to each structure relative to the number of neurons in the rest of brain. Thus, the evolutionary expansion of mammalian brains has involved both concerted and mosaic patterns of scaling across structures. This is, to our knowledge, the first mechanistic model that explains the generation of brains large and small in mammalian evolution, and it opens up new horizons for seeking the cellular pathways and genes involved in brain evolution.

Highlights

In contrast to ancestral mammalian brains, which were small and lissencephalic (Luo et al, 2001; Rowe et al, 2011), modern mammalian brains vary over 100,000-fold in mass (Count, 1947), not uniformly: members of different clades can be distinguished by the relative volume of brain structures as well as by other morphological aspects, such as the layout and extent of cortical folds (Welker, 1990; Pillay and Manger, 2007)
Based on an analysis of the shared and clade-specific characteristics of 41 modern mammalian species in 6 clades, and in light of the phylogenetic relationships among them, here we propose that ancestral mammal brains were composed and scaled in their cellular composition like modern afrotherian and glire brains: with an addition of neurons that is accompanied by a decrease in neuronal density and very little modification in glial cell density, implying a significant increase in average neuronal cell size in larger brains, and the allocation of approximately 2 neurons in the cerebral cortex and 8 neurons in the cerebellum for every neuron allocated to the rest of brain
We propose that the primate cerebral cortex and the primate and eulipotyphlan cerebella diverged from these concerted relationships, branching off with modifications that allowed average neuronal cell size in these structures not to increase accompanying increases in average neuronal cell size in the rest of brain (Figures 7A,B), and allowing a departure in the relationship between average neuronal cell size in the cerebral cortex and cerebellum from the relationship that supposedly applied to the common ancestor and still applies to modern afrotherians, glires and artiodactyls (Figure 7E)

Summary

Introduction

In contrast to ancestral mammalian brains, which were small and lissencephalic (Luo et al, 2001; Rowe et al, 2011), modern mammalian brains vary over 100,000-fold in mass (Count, 1947), not uniformly: members of different clades can be distinguished by the relative volume of brain structures as well as by other morphological aspects, such as the layout and extent of cortical folds (Welker, 1990; Pillay and Manger, 2007). WHAT STAYS THE SAME IN MAMMALIAN BRAIN EVOLUTION: NON-NEURONAL SCALING RULES Across all 41 species of afrotherians, glires, eulipotyphlans, scandentia, primates and artiodactyls, the mass of each brain structure is found to vary as a similar, shared power function of the number of non-neuronal (other) cells in the structure of exponent 1.020 ± 0.026, p < 0.0001; Figure 2, top right).

Results

Conclusion