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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.


Scaling of numbers of neurons in the olfactory bulb as a function of numbers of neurons in the cerebral cortex varies across clades, while numbers of neurons in the cerebellum vary coordinately with numbers of neurons in the cerebral cortex across all clades. Each symbol represents the average values for the structures indicated in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink). (A) Scaling of numbers of neurons in the olfactory bulb as a function of numbers of neurons in the cerebral cortex across species. Power functions plotted have exponents 2.129 ± 0.428, p = 0.0156 (eulipotyphlans, in orange), and 0.771 ± 0.188, p = 0.0046 (afrotherians, glires and scandentia, in green). The phylogenetic scheme on the left indicates in blue the clades that share the same neuronal scaling rules for the allocation of neurons in the olfactory bulb relative to the cerebral cortex, and the clades that have diverged from the presumed ancestral scaling rules (artiodactyls, eulipotyphlans, and primates). Primates are considered to also diverge from the ancestral scaling rules given their non-conformity to the relationship that applies jointly to afrotherians, glires, and scandentia. (B) Scaling of numbers of neurons in the cerebellum as a function of numbers of neurons in the cerebral cortex across species. The phylogenetic scheme on the left indicates in blue that all clades share similar neuronal scaling rules for the allocation of neurons in the cerebellum relative to the cerebral cortex. Power functions plotted are overlapping and have exponents 0.867 ± 0.108, p < 0.0001 (primates, in red), 0.904 ± 0.110, p = 0.0038 (artiodactyls, in pink), and 1.066 ± 0.111, p < 0.0001 (afrotherians, glires and scandentia, in green). The ensemble of species can be fitted by a linear function of slope 4.12 (p < 0.0001, not plotted).
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Figure 9: Scaling of numbers of neurons in the olfactory bulb as a function of numbers of neurons in the cerebral cortex varies across clades, while numbers of neurons in the cerebellum vary coordinately with numbers of neurons in the cerebral cortex across all clades. Each symbol represents the average values for the structures indicated in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink). (A) Scaling of numbers of neurons in the olfactory bulb as a function of numbers of neurons in the cerebral cortex across species. Power functions plotted have exponents 2.129 ± 0.428, p = 0.0156 (eulipotyphlans, in orange), and 0.771 ± 0.188, p = 0.0046 (afrotherians, glires and scandentia, in green). The phylogenetic scheme on the left indicates in blue the clades that share the same neuronal scaling rules for the allocation of neurons in the olfactory bulb relative to the cerebral cortex, and the clades that have diverged from the presumed ancestral scaling rules (artiodactyls, eulipotyphlans, and primates). Primates are considered to also diverge from the ancestral scaling rules given their non-conformity to the relationship that applies jointly to afrotherians, glires, and scandentia. (B) Scaling of numbers of neurons in the cerebellum as a function of numbers of neurons in the cerebral cortex across species. The phylogenetic scheme on the left indicates in blue that all clades share similar neuronal scaling rules for the allocation of neurons in the cerebellum relative to the cerebral cortex. Power functions plotted are overlapping and have exponents 0.867 ± 0.108, p < 0.0001 (primates, in red), 0.904 ± 0.110, p = 0.0038 (artiodactyls, in pink), and 1.066 ± 0.111, p < 0.0001 (afrotherians, glires and scandentia, in green). The ensemble of species can be fitted by a linear function of slope 4.12 (p < 0.0001, not plotted).

Mentions: The olfactory bulb gains neurons relative to the rest of brain at a rate that appears much faster in eulipotyphlans (exponent, 1.770 ± 0.578, p = 0.0548) than in the ensemble of afrotherians, glires, and scandentia (exponent, 0.714 ± 0.181, p = 0.0023), although the exponent does not reach significance in eulipotyphlans (Figure 8C). However, the olfactory bulb gains neurons at a significantly greater rate than the cerebral cortex in eulipotyphlans, as we have noted recently, as a power function of numbers of neurons in the cerebral cortex of exponent 2.129 ± 0.428 (p = 0.0156, r2 = 0.892; Figure 9A; Ribeiro et al., 2014), which suggests that, despite the statistical uncertainty, the eulipotyphlan olfactory bulb also gains neurons faster than the rest of brain. Afrotherians, glires and scandentia, in contrast, gain neurons more slowly in the olfactory bulb than in the cerebral cortex (exponent, 0.771 ± 0.188, p = 0.0046; Figure 9A), and the shared scaling across these clades suggests that this was the scaling rule that applied to ancestral mammals. Artiodactyls, primates and eulipotyphlans in turn diverged from the ancestral scaling rules with changes in the rate at which neurons are added to the olfactory bulb relative to both the rest of brain (Figure 8C) and to the cerebral cortex (Figure 9A), such that in eulipotyphlans these rates are greatly increased, but in artiodactyls and primates, numbers of neurons in the olfactory bulb are uncoupled from numbers of neurons in the cerebral cortex (and in the rest of brain).


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)

Scaling of numbers of neurons in the olfactory bulb as a function of numbers of neurons in the cerebral cortex varies across clades, while numbers of neurons in the cerebellum vary coordinately with numbers of neurons in the cerebral cortex across all clades. Each symbol represents the average values for the structures indicated in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink). (A) Scaling of numbers of neurons in the olfactory bulb as a function of numbers of neurons in the cerebral cortex across species. Power functions plotted have exponents 2.129 ± 0.428, p = 0.0156 (eulipotyphlans, in orange), and 0.771 ± 0.188, p = 0.0046 (afrotherians, glires and scandentia, in green). The phylogenetic scheme on the left indicates in blue the clades that share the same neuronal scaling rules for the allocation of neurons in the olfactory bulb relative to the cerebral cortex, and the clades that have diverged from the presumed ancestral scaling rules (artiodactyls, eulipotyphlans, and primates). Primates are considered to also diverge from the ancestral scaling rules given their non-conformity to the relationship that applies jointly to afrotherians, glires, and scandentia. (B) Scaling of numbers of neurons in the cerebellum as a function of numbers of neurons in the cerebral cortex across species. The phylogenetic scheme on the left indicates in blue that all clades share similar neuronal scaling rules for the allocation of neurons in the cerebellum relative to the cerebral cortex. Power functions plotted are overlapping and have exponents 0.867 ± 0.108, p < 0.0001 (primates, in red), 0.904 ± 0.110, p = 0.0038 (artiodactyls, in pink), and 1.066 ± 0.111, p < 0.0001 (afrotherians, glires and scandentia, in green). The ensemble of species can be fitted by a linear function of slope 4.12 (p < 0.0001, not plotted).
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Figure 9: Scaling of numbers of neurons in the olfactory bulb as a function of numbers of neurons in the cerebral cortex varies across clades, while numbers of neurons in the cerebellum vary coordinately with numbers of neurons in the cerebral cortex across all clades. Each symbol represents the average values for the structures indicated in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink). (A) Scaling of numbers of neurons in the olfactory bulb as a function of numbers of neurons in the cerebral cortex across species. Power functions plotted have exponents 2.129 ± 0.428, p = 0.0156 (eulipotyphlans, in orange), and 0.771 ± 0.188, p = 0.0046 (afrotherians, glires and scandentia, in green). The phylogenetic scheme on the left indicates in blue the clades that share the same neuronal scaling rules for the allocation of neurons in the olfactory bulb relative to the cerebral cortex, and the clades that have diverged from the presumed ancestral scaling rules (artiodactyls, eulipotyphlans, and primates). Primates are considered to also diverge from the ancestral scaling rules given their non-conformity to the relationship that applies jointly to afrotherians, glires, and scandentia. (B) Scaling of numbers of neurons in the cerebellum as a function of numbers of neurons in the cerebral cortex across species. The phylogenetic scheme on the left indicates in blue that all clades share similar neuronal scaling rules for the allocation of neurons in the cerebellum relative to the cerebral cortex. Power functions plotted are overlapping and have exponents 0.867 ± 0.108, p < 0.0001 (primates, in red), 0.904 ± 0.110, p = 0.0038 (artiodactyls, in pink), and 1.066 ± 0.111, p < 0.0001 (afrotherians, glires and scandentia, in green). The ensemble of species can be fitted by a linear function of slope 4.12 (p < 0.0001, not plotted).
Mentions: The olfactory bulb gains neurons relative to the rest of brain at a rate that appears much faster in eulipotyphlans (exponent, 1.770 ± 0.578, p = 0.0548) than in the ensemble of afrotherians, glires, and scandentia (exponent, 0.714 ± 0.181, p = 0.0023), although the exponent does not reach significance in eulipotyphlans (Figure 8C). However, the olfactory bulb gains neurons at a significantly greater rate than the cerebral cortex in eulipotyphlans, as we have noted recently, as a power function of numbers of neurons in the cerebral cortex of exponent 2.129 ± 0.428 (p = 0.0156, r2 = 0.892; Figure 9A; Ribeiro et al., 2014), which suggests that, despite the statistical uncertainty, the eulipotyphlan olfactory bulb also gains neurons faster than the rest of brain. Afrotherians, glires and scandentia, in contrast, gain neurons more slowly in the olfactory bulb than in the cerebral cortex (exponent, 0.771 ± 0.188, p = 0.0046; Figure 9A), and the shared scaling across these clades suggests that this was the scaling rule that applied to ancestral mammals. Artiodactyls, primates and eulipotyphlans in turn diverged from the ancestral scaling rules with changes in the rate at which neurons are added to the olfactory bulb relative to both the rest of brain (Figure 8C) and to the cerebral cortex (Figure 9A), such that in eulipotyphlans these rates are greatly increased, but in artiodactyls and primates, numbers of neurons in the olfactory bulb are uncoupled from numbers of neurons in the cerebral cortex (and in the rest of brain).

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.