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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 scaling rules for the olfactory bulb differ between eulipotyphlans, artiodactyls, primates and other clades. Top right: scaling of olfactory bulb mass as a function of numbers of neurons in the structure across species. Plotted power functions have exponent of 0.823 ± 0.071, p = 0.0014 (eulipotyphlans, orange), 1.309 ± 0.257, p = 0.0364 (artiodactyls, pink), and 1.185 ± 0.186, p < 0.0001 (in green: scandentia, afrotherians and glires, excluding the capybara; Ribeiro et al., 2014). Bottom right: scaling of neuronal density in the olfactory bulb as a function of numbers of neurons in the structure. Power functions are not significant, but neuronal density is highest in eulipotyphlans and lowest in artiodactyls, which we suggest that branched off the mammalian ancestor when modifications resulted in decreased and increased average neuronal cell sizes, respectively (orange and pink arrows). 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). The phylogenetic scheme on the left indicates in blue the clades that share the same neuronal scaling rules for the olfactory bulb, and the presumed extension of these shared scaling rules to the common ancestor to the non-artiodactyl clades, while artiodactyls and eulipotyphlans diverged from them.
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Figure 6: Neuronal scaling rules for the olfactory bulb differ between eulipotyphlans, artiodactyls, primates and other clades. Top right: scaling of olfactory bulb mass as a function of numbers of neurons in the structure across species. Plotted power functions have exponent of 0.823 ± 0.071, p = 0.0014 (eulipotyphlans, orange), 1.309 ± 0.257, p = 0.0364 (artiodactyls, pink), and 1.185 ± 0.186, p < 0.0001 (in green: scandentia, afrotherians and glires, excluding the capybara; Ribeiro et al., 2014). Bottom right: scaling of neuronal density in the olfactory bulb as a function of numbers of neurons in the structure. Power functions are not significant, but neuronal density is highest in eulipotyphlans and lowest in artiodactyls, which we suggest that branched off the mammalian ancestor when modifications resulted in decreased and increased average neuronal cell sizes, respectively (orange and pink arrows). 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). The phylogenetic scheme on the left indicates in blue the clades that share the same neuronal scaling rules for the olfactory bulb, and the presumed extension of these shared scaling rules to the common ancestor to the non-artiodactyl clades, while artiodactyls and eulipotyphlans diverged from them.

Mentions: Importantly, the relationships between brain structure mass and the number of neurons that compose the structure, that is, the neuronal scaling rules that apply to each brain structure, are not shared across all mammalian clades, but are also not exclusive of each clade. The neuronal scaling rules that apply to the cerebral cortex are shared by all clades analyzed here except primates (Figure 3); the neuronal scaling rules that apply to the cerebellum are shared by all clades except primates and eulipotyphlans (Figure 4); the neuronal scaling rules that apply to the rest of brain are shared by all (including primates) but exclude artiodactyls (Figure 5); and the neuronal scaling rules that apply to the olfactory bulb are shared only by afrotherians and glires, and not by eulipotyphlans, primates, or artiodactyls (Figure 6; Ribeiro et al., 2014). The exponents that apply to these relationships are given in the respective Figure legends.


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 scaling rules for the olfactory bulb differ between eulipotyphlans, artiodactyls, primates and other clades. Top right: scaling of olfactory bulb mass as a function of numbers of neurons in the structure across species. Plotted power functions have exponent of 0.823 ± 0.071, p = 0.0014 (eulipotyphlans, orange), 1.309 ± 0.257, p = 0.0364 (artiodactyls, pink), and 1.185 ± 0.186, p < 0.0001 (in green: scandentia, afrotherians and glires, excluding the capybara; Ribeiro et al., 2014). Bottom right: scaling of neuronal density in the olfactory bulb as a function of numbers of neurons in the structure. Power functions are not significant, but neuronal density is highest in eulipotyphlans and lowest in artiodactyls, which we suggest that branched off the mammalian ancestor when modifications resulted in decreased and increased average neuronal cell sizes, respectively (orange and pink arrows). 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). The phylogenetic scheme on the left indicates in blue the clades that share the same neuronal scaling rules for the olfactory bulb, and the presumed extension of these shared scaling rules to the common ancestor to the non-artiodactyl clades, while artiodactyls and eulipotyphlans diverged from them.
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Figure 6: Neuronal scaling rules for the olfactory bulb differ between eulipotyphlans, artiodactyls, primates and other clades. Top right: scaling of olfactory bulb mass as a function of numbers of neurons in the structure across species. Plotted power functions have exponent of 0.823 ± 0.071, p = 0.0014 (eulipotyphlans, orange), 1.309 ± 0.257, p = 0.0364 (artiodactyls, pink), and 1.185 ± 0.186, p < 0.0001 (in green: scandentia, afrotherians and glires, excluding the capybara; Ribeiro et al., 2014). Bottom right: scaling of neuronal density in the olfactory bulb as a function of numbers of neurons in the structure. Power functions are not significant, but neuronal density is highest in eulipotyphlans and lowest in artiodactyls, which we suggest that branched off the mammalian ancestor when modifications resulted in decreased and increased average neuronal cell sizes, respectively (orange and pink arrows). 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). The phylogenetic scheme on the left indicates in blue the clades that share the same neuronal scaling rules for the olfactory bulb, and the presumed extension of these shared scaling rules to the common ancestor to the non-artiodactyl clades, while artiodactyls and eulipotyphlans diverged from them.
Mentions: Importantly, the relationships between brain structure mass and the number of neurons that compose the structure, that is, the neuronal scaling rules that apply to each brain structure, are not shared across all mammalian clades, but are also not exclusive of each clade. The neuronal scaling rules that apply to the cerebral cortex are shared by all clades analyzed here except primates (Figure 3); the neuronal scaling rules that apply to the cerebellum are shared by all clades except primates and eulipotyphlans (Figure 4); the neuronal scaling rules that apply to the rest of brain are shared by all (including primates) but exclude artiodactyls (Figure 5); and the neuronal scaling rules that apply to the olfactory bulb are shared only by afrotherians and glires, and not by eulipotyphlans, primates, or artiodactyls (Figure 6; Ribeiro et al., 2014). The exponents that apply to these relationships are given in the respective Figure legends.

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.