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

Herculano-Houzel S, Manger PR, Kaas JH - Front Neuroanat (2014)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro Rio de Janeiro, Brazil ; Instituto Nacional de Neurociência Translacional, Ministério de Ciência e Tecnologia São Paulo, Brazil.

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.

No MeSH data available.


Neuronal density varies concertedly between brain structures across species in most clades, but diverges in others. Plots show how neuronal densities in general vary concertedly across species between the cerebral cortex and rest of brain (A), between the cerebellum and rest of brain (B), between the olfactory bulb and rest of brain (C), between the olfactory bulb and the cerebral cortex (D), between the cerebellum and the cortex (E), and between the olfactory bulb and cerebellum (F). (A) Plotted function excludes primates (red), and has exponent 0.872 ± 0.041 (p < 0.0001). (B) Plotted function excludes primates (red) and eulipotyphlans (orange), with an exponent of 0.446 ± 0.058, p < 0.0001. (C) Plotted function excludes primates (red) and eulipotyphlans (orange), with an exponent of 0.991 ± 0.011, p < 0.0001. (D) Plotted function excludes primates (red) and eulipotyphlans (orange), and has an exponent of 1.133 ± 0.112, p < 0.0001. (E) Plotted function excludes primates (red) and eulipotyphlans (orange), with an exponent of 0.529 ± 0.050, p < 0.0001. (F) Plotted function includes all clades, with an exponent of 1.630 ± 0.166, p < 0.0001. Each symbol represents the average values for the rest of brain in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink).
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Figure 7: Neuronal density varies concertedly between brain structures across species in most clades, but diverges in others. Plots show how neuronal densities in general vary concertedly across species between the cerebral cortex and rest of brain (A), between the cerebellum and rest of brain (B), between the olfactory bulb and rest of brain (C), between the olfactory bulb and the cerebral cortex (D), between the cerebellum and the cortex (E), and between the olfactory bulb and cerebellum (F). (A) Plotted function excludes primates (red), and has exponent 0.872 ± 0.041 (p < 0.0001). (B) Plotted function excludes primates (red) and eulipotyphlans (orange), with an exponent of 0.446 ± 0.058, p < 0.0001. (C) Plotted function excludes primates (red) and eulipotyphlans (orange), with an exponent of 0.991 ± 0.011, p < 0.0001. (D) Plotted function excludes primates (red) and eulipotyphlans (orange), and has an exponent of 1.133 ± 0.112, p < 0.0001. (E) Plotted function excludes primates (red) and eulipotyphlans (orange), with an exponent of 0.529 ± 0.050, p < 0.0001. (F) Plotted function includes all clades, with an exponent of 1.630 ± 0.166, p < 0.0001. Each symbol represents the average values for the rest of brain in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink).

Mentions: Surprisingly, the analysis of variations in neuronal density across structures and species shows marked correlations, from which the primate and eulipotyphlan cerebellum and the primate cerebral cortex deviate as expected from the scenario described above. Neuronal densities in the cerebral cortex correlate uniformly with neuronal densities in the rest of brain across non-primate species, but primates have much higher neuronal densities in the cerebral cortex for the neuronal densities in their rest of brain compared to the other clades (Figure 7A). Neuronal densities in the cerebellum also correlate uniformly with neuronal densities in the rest of brain across non-primate, non-eulipotyphlan species, but primates and eulipotyphlans have much higher neuronal densities in the cerebellum for the neuronal densities in their rest of brain compared to the other clades (Figure 7B). Consistently, neuronal densities are correlated between the cerebellum and the cerebral cortex in the non-primate, non-eulipotyphlan species, while primates and eulipotyphlans have higher neuronal densities in the cerebellum than predicted from the neuronal densities in their cerebral cortices (Figure 7E). Neuronal densities are also correlated between the olfactory bulb and the rest of brain, cerebral cortex, and cerebellum (Figures 7C,D,F), although neuronal densities in the primate olfactory bulb are higher than predicted from the densities in their rest of brain (Figure 7C). Notice that, although neuronal densities are strongly correlated across all structures, they vary with different power exponents across structures (Figure 7). This implies that as one part of the brain gains somewhat larger neurons, neurons in different structures also become larger—but at different rates in different structures. As a consequence, there is no consistent relationship between total brain mass and neuronal densities in particular brain structures, although the mass of each structure is consistently associated with a predictable neuronal density as shown in Figures 3–6.


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

Herculano-Houzel S, Manger PR, Kaas JH - Front Neuroanat (2014)

Neuronal density varies concertedly between brain structures across species in most clades, but diverges in others. Plots show how neuronal densities in general vary concertedly across species between the cerebral cortex and rest of brain (A), between the cerebellum and rest of brain (B), between the olfactory bulb and rest of brain (C), between the olfactory bulb and the cerebral cortex (D), between the cerebellum and the cortex (E), and between the olfactory bulb and cerebellum (F). (A) Plotted function excludes primates (red), and has exponent 0.872 ± 0.041 (p < 0.0001). (B) Plotted function excludes primates (red) and eulipotyphlans (orange), with an exponent of 0.446 ± 0.058, p < 0.0001. (C) Plotted function excludes primates (red) and eulipotyphlans (orange), with an exponent of 0.991 ± 0.011, p < 0.0001. (D) Plotted function excludes primates (red) and eulipotyphlans (orange), and has an exponent of 1.133 ± 0.112, p < 0.0001. (E) Plotted function excludes primates (red) and eulipotyphlans (orange), with an exponent of 0.529 ± 0.050, p < 0.0001. (F) Plotted function includes all clades, with an exponent of 1.630 ± 0.166, p < 0.0001. Each symbol represents the average values for the rest of brain in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink).
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Figure 7: Neuronal density varies concertedly between brain structures across species in most clades, but diverges in others. Plots show how neuronal densities in general vary concertedly across species between the cerebral cortex and rest of brain (A), between the cerebellum and rest of brain (B), between the olfactory bulb and rest of brain (C), between the olfactory bulb and the cerebral cortex (D), between the cerebellum and the cortex (E), and between the olfactory bulb and cerebellum (F). (A) Plotted function excludes primates (red), and has exponent 0.872 ± 0.041 (p < 0.0001). (B) Plotted function excludes primates (red) and eulipotyphlans (orange), with an exponent of 0.446 ± 0.058, p < 0.0001. (C) Plotted function excludes primates (red) and eulipotyphlans (orange), with an exponent of 0.991 ± 0.011, p < 0.0001. (D) Plotted function excludes primates (red) and eulipotyphlans (orange), and has an exponent of 1.133 ± 0.112, p < 0.0001. (E) Plotted function excludes primates (red) and eulipotyphlans (orange), with an exponent of 0.529 ± 0.050, p < 0.0001. (F) Plotted function includes all clades, with an exponent of 1.630 ± 0.166, p < 0.0001. Each symbol represents the average values for the rest of brain in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink).
Mentions: Surprisingly, the analysis of variations in neuronal density across structures and species shows marked correlations, from which the primate and eulipotyphlan cerebellum and the primate cerebral cortex deviate as expected from the scenario described above. Neuronal densities in the cerebral cortex correlate uniformly with neuronal densities in the rest of brain across non-primate species, but primates have much higher neuronal densities in the cerebral cortex for the neuronal densities in their rest of brain compared to the other clades (Figure 7A). Neuronal densities in the cerebellum also correlate uniformly with neuronal densities in the rest of brain across non-primate, non-eulipotyphlan species, but primates and eulipotyphlans have much higher neuronal densities in the cerebellum for the neuronal densities in their rest of brain compared to the other clades (Figure 7B). Consistently, neuronal densities are correlated between the cerebellum and the cerebral cortex in the non-primate, non-eulipotyphlan species, while primates and eulipotyphlans have higher neuronal densities in the cerebellum than predicted from the neuronal densities in their cerebral cortices (Figure 7E). Neuronal densities are also correlated between the olfactory bulb and the rest of brain, cerebral cortex, and cerebellum (Figures 7C,D,F), although neuronal densities in the primate olfactory bulb are higher than predicted from the densities in their rest of brain (Figure 7C). Notice that, although neuronal densities are strongly correlated across all structures, they vary with different power exponents across structures (Figure 7). This implies that as one part of the brain gains somewhat larger neurons, neurons in different structures also become larger—but at different rates in different structures. As a consequence, there is no consistent relationship between total brain mass and neuronal densities in particular brain structures, although the mass of each structure is consistently associated with a predictable neuronal density as shown in Figures 3–6.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro Rio de Janeiro, Brazil ; Instituto Nacional de Neurociência Translacional, Ministério de Ciência e Tecnologia São Paulo, Brazil.

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.

No MeSH data available.