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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 cerebral cortex, that is, the relationship between cortical mass and number of neuronal cells, differs between primates and non-primates, but is shared across all non-primate species examined. Top right: scaling of cerebral cortical mass (gray and white matter combined) as a function of numbers of neurons in the structure across species; Bottom right: scaling of neuronal density as a function of numbers of neurons in the structure. Notice that neuronal density decreases uniformly across species as the cerebral cortex gains neurons, except in primates, which we suggest that branched off the mammalian ancestor (to which the same rules shared by current non-primates applied) when a modification nearly stopped average neuronal cell size from increasing (and thus, neuronal density from decreasing) as the cortex gained neurons (red arrow). Top: primates, function (not plotted for clarity) has exponent 1.087 ± 0.074; all others, joint power function plotted has exponent of 1.688 ± 0.051. Bottom: Primates, exponent −0.150 ± 0.064 (not plotted for clarity); non-primates, exponent −0.688 ± 0.052. Each symbol represents the average values for the cerebral cortex in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink). The phylogenetic scheme on the left indicates the clades that share the same neuronal scaling rules for the cerebral cortex, and the presumed extension of these shared scaling rules to the common ancestor to the non-primate clades while primates diverge from them.
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Figure 3: Neuronal scaling rules for the cerebral cortex, that is, the relationship between cortical mass and number of neuronal cells, differs between primates and non-primates, but is shared across all non-primate species examined. Top right: scaling of cerebral cortical mass (gray and white matter combined) as a function of numbers of neurons in the structure across species; Bottom right: scaling of neuronal density as a function of numbers of neurons in the structure. Notice that neuronal density decreases uniformly across species as the cerebral cortex gains neurons, except in primates, which we suggest that branched off the mammalian ancestor (to which the same rules shared by current non-primates applied) when a modification nearly stopped average neuronal cell size from increasing (and thus, neuronal density from decreasing) as the cortex gained neurons (red arrow). Top: primates, function (not plotted for clarity) has exponent 1.087 ± 0.074; all others, joint power function plotted has exponent of 1.688 ± 0.051. Bottom: Primates, exponent −0.150 ± 0.064 (not plotted for clarity); non-primates, exponent −0.688 ± 0.052. Each symbol represents the average values for the cerebral cortex in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink). The phylogenetic scheme on the left indicates the clades that share the same neuronal scaling rules for the cerebral cortex, and the presumed extension of these shared scaling rules to the common ancestor to the non-primate clades while primates diverge 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 cerebral cortex, that is, the relationship between cortical mass and number of neuronal cells, differs between primates and non-primates, but is shared across all non-primate species examined. Top right: scaling of cerebral cortical mass (gray and white matter combined) as a function of numbers of neurons in the structure across species; Bottom right: scaling of neuronal density as a function of numbers of neurons in the structure. Notice that neuronal density decreases uniformly across species as the cerebral cortex gains neurons, except in primates, which we suggest that branched off the mammalian ancestor (to which the same rules shared by current non-primates applied) when a modification nearly stopped average neuronal cell size from increasing (and thus, neuronal density from decreasing) as the cortex gained neurons (red arrow). Top: primates, function (not plotted for clarity) has exponent 1.087 ± 0.074; all others, joint power function plotted has exponent of 1.688 ± 0.051. Bottom: Primates, exponent −0.150 ± 0.064 (not plotted for clarity); non-primates, exponent −0.688 ± 0.052. Each symbol represents the average values for the cerebral cortex in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink). The phylogenetic scheme on the left indicates the clades that share the same neuronal scaling rules for the cerebral cortex, and the presumed extension of these shared scaling rules to the common ancestor to the non-primate clades while primates diverge from them.
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Related In: Results  -  Collection

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Figure 3: Neuronal scaling rules for the cerebral cortex, that is, the relationship between cortical mass and number of neuronal cells, differs between primates and non-primates, but is shared across all non-primate species examined. Top right: scaling of cerebral cortical mass (gray and white matter combined) as a function of numbers of neurons in the structure across species; Bottom right: scaling of neuronal density as a function of numbers of neurons in the structure. Notice that neuronal density decreases uniformly across species as the cerebral cortex gains neurons, except in primates, which we suggest that branched off the mammalian ancestor (to which the same rules shared by current non-primates applied) when a modification nearly stopped average neuronal cell size from increasing (and thus, neuronal density from decreasing) as the cortex gained neurons (red arrow). Top: primates, function (not plotted for clarity) has exponent 1.087 ± 0.074; all others, joint power function plotted has exponent of 1.688 ± 0.051. Bottom: Primates, exponent −0.150 ± 0.064 (not plotted for clarity); non-primates, exponent −0.688 ± 0.052. Each symbol represents the average values for the cerebral cortex in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink). The phylogenetic scheme on the left indicates the clades that share the same neuronal scaling rules for the cerebral cortex, and the presumed extension of these shared scaling rules to the common ancestor to the non-primate clades while primates diverge 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.