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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 cerebral cortex, cerebellum and olfactory bulb as a function of numbers of neurons in the rest of brain varies across 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). The phylogenetic scheme on the left indicates in blue the clades that share the same neuronal scaling rules for the rest of brain, and the presumed extension of these shared scaling rules to the common eutherian ancestor; clades that have divergent scaling rules are colored differently. (A) Scaling of numbers of neurons in the cerebral cortex as a function of numbers of neurons in the rest of brain across species. Power functions plotted have exponents 1.391 ± 0.158, p < 0.0001 (primates, in red), 1.852 ± 0.135, p = 0.0008 (artiodactyls, in pink), and 1.053 ± 0.061, p < 0.0001 (afrotherians, glires, scandentia and eulipotyphlans, in black). (B) Scaling of numbers of neurons in the cerebellum as a function of numbers of neurons in the rest of brain across species. Power functions plotted have exponents 1.315 ± 0.112, p < 0.0001 (primates, in red), 1.632 ± 0.222, p = 0.0148 (artiodactyls, in pink), and 1.154 ± 0.112, p < 0.0001 (afrotherians, glires, scandentia and eulipotyphlans, in black). (C) Scaling of numbers of neurons in the olfactory bulb as a function of numbers of neurons in the rest of brain across species. Power functions plotted have exponents 1.770 ± 0.578, p = 0.0548 (eulipotyphlans, in orange), 1.127 ± 0.638, p = 0.2194 (artiodactyls, in pink), and 0.714 ± 0.181, p = 0.0023 (afrotherians, glires, and scandentia, in black).
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Figure 8: Scaling of numbers of neurons in the cerebral cortex, cerebellum and olfactory bulb as a function of numbers of neurons in the rest of brain varies across 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). The phylogenetic scheme on the left indicates in blue the clades that share the same neuronal scaling rules for the rest of brain, and the presumed extension of these shared scaling rules to the common eutherian ancestor; clades that have divergent scaling rules are colored differently. (A) Scaling of numbers of neurons in the cerebral cortex as a function of numbers of neurons in the rest of brain across species. Power functions plotted have exponents 1.391 ± 0.158, p < 0.0001 (primates, in red), 1.852 ± 0.135, p = 0.0008 (artiodactyls, in pink), and 1.053 ± 0.061, p < 0.0001 (afrotherians, glires, scandentia and eulipotyphlans, in black). (B) Scaling of numbers of neurons in the cerebellum as a function of numbers of neurons in the rest of brain across species. Power functions plotted have exponents 1.315 ± 0.112, p < 0.0001 (primates, in red), 1.632 ± 0.222, p = 0.0148 (artiodactyls, in pink), and 1.154 ± 0.112, p < 0.0001 (afrotherians, glires, scandentia and eulipotyphlans, in black). (C) Scaling of numbers of neurons in the olfactory bulb as a function of numbers of neurons in the rest of brain across species. Power functions plotted have exponents 1.770 ± 0.578, p = 0.0548 (eulipotyphlans, in orange), 1.127 ± 0.638, p = 0.2194 (artiodactyls, in pink), and 0.714 ± 0.181, p = 0.0023 (afrotherians, glires, and scandentia, in black).

Mentions: Figure 8 shows that they do not: even across gross brain regions, such as the entire cerebral cortex, the entire cerebellum and the ensemble of brainstem, diencephalon and striatum (the “rest of brain”), the rate at which one structure gains neurons as another also gains neurons varies across clades. The cerebral cortex gains neurons as a linear function of numbers of neurons in the rest of brain that is shared across afrotherians, glires, scandentia and eulipotyphlans, with exponent 1.053 ± 0.061 (p < 0.0001, r2 = 0.939; Figure 8A, red). Artiodactyls, on the other, gain neurons in the cerebral cortex faster than they gain neurons in the rest of brain, as a power function of exponent 1.391 ± 0.158 (p < 0.0001, r2 = 0.885), and also have more neurons in the cerebral cortex than glires with similar numbers of neurons in the rest of brain, falling well outside of the 95% confidence interval that applies to the ensemble of afrotherians, glires, and scandentia (Figure 8A, pink). Primates on the other hand, gain neurons in the cerebral cortex at an even steeper rate as a function of neurons added to the rest of brain, with exponent 1.852 ± 0.135 (p < 0.0001, r2 = 0.984; Figure 8A, pink). The discrepancy between primates, artiodactyls, and the ensemble of other clades suggests that the former two clades diverged from the common ancestor with modifications that generated larger numbers of neurons in the cerebral cortex than in the rest of brain, that is, with an actual relative expansion of the neuronal population in the cerebral cortex over the brainstem, diencephalon and striatum.


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 cerebral cortex, cerebellum and olfactory bulb as a function of numbers of neurons in the rest of brain varies across 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). The phylogenetic scheme on the left indicates in blue the clades that share the same neuronal scaling rules for the rest of brain, and the presumed extension of these shared scaling rules to the common eutherian ancestor; clades that have divergent scaling rules are colored differently. (A) Scaling of numbers of neurons in the cerebral cortex as a function of numbers of neurons in the rest of brain across species. Power functions plotted have exponents 1.391 ± 0.158, p < 0.0001 (primates, in red), 1.852 ± 0.135, p = 0.0008 (artiodactyls, in pink), and 1.053 ± 0.061, p < 0.0001 (afrotherians, glires, scandentia and eulipotyphlans, in black). (B) Scaling of numbers of neurons in the cerebellum as a function of numbers of neurons in the rest of brain across species. Power functions plotted have exponents 1.315 ± 0.112, p < 0.0001 (primates, in red), 1.632 ± 0.222, p = 0.0148 (artiodactyls, in pink), and 1.154 ± 0.112, p < 0.0001 (afrotherians, glires, scandentia and eulipotyphlans, in black). (C) Scaling of numbers of neurons in the olfactory bulb as a function of numbers of neurons in the rest of brain across species. Power functions plotted have exponents 1.770 ± 0.578, p = 0.0548 (eulipotyphlans, in orange), 1.127 ± 0.638, p = 0.2194 (artiodactyls, in pink), and 0.714 ± 0.181, p = 0.0023 (afrotherians, glires, and scandentia, in black).
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Figure 8: Scaling of numbers of neurons in the cerebral cortex, cerebellum and olfactory bulb as a function of numbers of neurons in the rest of brain varies across 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). The phylogenetic scheme on the left indicates in blue the clades that share the same neuronal scaling rules for the rest of brain, and the presumed extension of these shared scaling rules to the common eutherian ancestor; clades that have divergent scaling rules are colored differently. (A) Scaling of numbers of neurons in the cerebral cortex as a function of numbers of neurons in the rest of brain across species. Power functions plotted have exponents 1.391 ± 0.158, p < 0.0001 (primates, in red), 1.852 ± 0.135, p = 0.0008 (artiodactyls, in pink), and 1.053 ± 0.061, p < 0.0001 (afrotherians, glires, scandentia and eulipotyphlans, in black). (B) Scaling of numbers of neurons in the cerebellum as a function of numbers of neurons in the rest of brain across species. Power functions plotted have exponents 1.315 ± 0.112, p < 0.0001 (primates, in red), 1.632 ± 0.222, p = 0.0148 (artiodactyls, in pink), and 1.154 ± 0.112, p < 0.0001 (afrotherians, glires, scandentia and eulipotyphlans, in black). (C) Scaling of numbers of neurons in the olfactory bulb as a function of numbers of neurons in the rest of brain across species. Power functions plotted have exponents 1.770 ± 0.578, p = 0.0548 (eulipotyphlans, in orange), 1.127 ± 0.638, p = 0.2194 (artiodactyls, in pink), and 0.714 ± 0.181, p = 0.0023 (afrotherians, glires, and scandentia, in black).
Mentions: Figure 8 shows that they do not: even across gross brain regions, such as the entire cerebral cortex, the entire cerebellum and the ensemble of brainstem, diencephalon and striatum (the “rest of brain”), the rate at which one structure gains neurons as another also gains neurons varies across clades. The cerebral cortex gains neurons as a linear function of numbers of neurons in the rest of brain that is shared across afrotherians, glires, scandentia and eulipotyphlans, with exponent 1.053 ± 0.061 (p < 0.0001, r2 = 0.939; Figure 8A, red). Artiodactyls, on the other, gain neurons in the cerebral cortex faster than they gain neurons in the rest of brain, as a power function of exponent 1.391 ± 0.158 (p < 0.0001, r2 = 0.885), and also have more neurons in the cerebral cortex than glires with similar numbers of neurons in the rest of brain, falling well outside of the 95% confidence interval that applies to the ensemble of afrotherians, glires, and scandentia (Figure 8A, pink). Primates on the other hand, gain neurons in the cerebral cortex at an even steeper rate as a function of neurons added to the rest of brain, with exponent 1.852 ± 0.135 (p < 0.0001, r2 = 0.984; Figure 8A, pink). The discrepancy between primates, artiodactyls, and the ensemble of other clades suggests that the former two clades diverged from the common ancestor with modifications that generated larger numbers of neurons in the cerebral cortex than in the rest of brain, that is, with an actual relative expansion of the neuronal population in the cerebral cortex over the brainstem, diencephalon and striatum.

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.