Limits...
Cellular scaling rules for the brain of Artiodactyla include a highly folded cortex with few neurons.

Kazu RS, Maldonado J, Mota B, Manger PR, Herculano-Houzel S - Front Neuroanat (2014)

Bottom Line: Our findings suggest that the scaling rules found to be shared across modern afrotherians, glires, and artiodactyls applied to the common Eutherian ancestor, such as the relationship between the mass of the cerebral cortex as a whole and its number of neurons.In turn, the distribution of neurons along the surface of the cerebral cortex, which is related to its degree of gyrification, appears to be a clade-specific characteristic.If the neuronal scaling rules for artiodactyls extend to all cetartiodactyls, we predict that the large cerebral cortex of cetaceans will still have fewer neurons than the human cerebral cortex.

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, CNPq/MCT, São Paulo, Brazil.

ABSTRACT
Quantitative analysis of the cellular composition of rodent, primate, insectivore, and afrotherian brains has shown that non-neuronal scaling rules are similar across these mammalian orders that diverged about 95 million years ago, and therefore appear to be conserved in evolution, while neuronal scaling rules appear to be free to vary in a clade-specific manner. Here we analyze the cellular scaling rules that apply to the brain of artiodactyls, a group within the order Cetartiodactyla, believed to be a relatively recent radiation from the common Eutherian ancestor. We find that artiodactyls share non-neuronal scaling rules with all groups analyzed previously. Artiodactyls share with afrotherians and rodents, but not with primates, the neuronal scaling rules that apply to the cerebral cortex and cerebellum. The neuronal scaling rules that apply to the remaining brain areas are, however, distinct in artiodactyls. Importantly, we show that the folding index of the cerebral cortex scales with the number of neurons in the cerebral cortex in distinct fashions across artiodactyls, afrotherians, rodents, and primates, such that the artiodactyl cerebral cortex is more convoluted than primate cortices of similar numbers of neurons. Our findings suggest that the scaling rules found to be shared across modern afrotherians, glires, and artiodactyls applied to the common Eutherian ancestor, such as the relationship between the mass of the cerebral cortex as a whole and its number of neurons. In turn, the distribution of neurons along the surface of the cerebral cortex, which is related to its degree of gyrification, appears to be a clade-specific characteristic. If the neuronal scaling rules for artiodactyls extend to all cetartiodactyls, we predict that the large cerebral cortex of cetaceans will still have fewer neurons than the human cerebral cortex.

No MeSH data available.


Uniform variation in the O/N ratio with neuronal density, but not structure mass. (A) Ratio between numbers of other (non-neuronal) and neuronal cells, O/N, varies in no uniform fashion across structures (cerebral cortex, circles; cerebellum, squares; rest of brain, triangles) and species (each symbol) as a function of the mass of each structure. (B) In contrast, the O/N ratio varies uniformly across brain structures and species as a function of average neuronal density in the structure. The power function plotted in b applies to the non-artiodactyl species in the sample, and has and exponent of -0.917 ± 0.028. Artiodactyl species in black, primates in red, glires in green, afrotherians in blue, insectivores in orange, scandentia in gray. Data from Herculano-Houzel et al. (2006, 2007, 2011), Azevedo et al. (2009), Sarko et al. (2009), Gabi et al. (2010) and Neves et al. (2014).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4228855&req=5

Figure 7: Uniform variation in the O/N ratio with neuronal density, but not structure mass. (A) Ratio between numbers of other (non-neuronal) and neuronal cells, O/N, varies in no uniform fashion across structures (cerebral cortex, circles; cerebellum, squares; rest of brain, triangles) and species (each symbol) as a function of the mass of each structure. (B) In contrast, the O/N ratio varies uniformly across brain structures and species as a function of average neuronal density in the structure. The power function plotted in b applies to the non-artiodactyl species in the sample, and has and exponent of -0.917 ± 0.028. Artiodactyl species in black, primates in red, glires in green, afrotherians in blue, insectivores in orange, scandentia in gray. Data from Herculano-Houzel et al. (2006, 2007, 2011), Azevedo et al. (2009), Sarko et al. (2009), Gabi et al. (2010) and Neves et al. (2014).

Mentions: The ratio between the numbers of other cells and neurons in each structure (the O/N ratio), which approximates the glia/neuron ratio, varies between 0.184 (in the blesbok cerebellum) and 32.333 (in the giraffe rest of brain) across structures and species in these artiodactyls (Figure 7). The O/N ratio in the artiodactyl cerebral cortex exceeds 10 when both gray and white matter are included, and within the cortical gray matter alone it varies between 7.2 and 8.5 across species (Table 1). The O/N ratio varies widely across structures and species as a function of structure mass, with no single relationship evident (Figure 7A). In contrast, the O/N ratio varies as a common power function of neuronal density across all artiodactyl structures with an exponent of -1.082 ± 0.035 (p < 0.0001), in a distribution that overlaps with the variation of O/N as a function of neuronal density across non-artiodactyl species (exponent, -0.917 ± 0.028, p < 0.0001; Figure 7B). The addition of artiodactyl structures to the distribution does not change the exponent significantly (-0.935 ± 0.024, p < 0.0001).


Cellular scaling rules for the brain of Artiodactyla include a highly folded cortex with few neurons.

Kazu RS, Maldonado J, Mota B, Manger PR, Herculano-Houzel S - Front Neuroanat (2014)

Uniform variation in the O/N ratio with neuronal density, but not structure mass. (A) Ratio between numbers of other (non-neuronal) and neuronal cells, O/N, varies in no uniform fashion across structures (cerebral cortex, circles; cerebellum, squares; rest of brain, triangles) and species (each symbol) as a function of the mass of each structure. (B) In contrast, the O/N ratio varies uniformly across brain structures and species as a function of average neuronal density in the structure. The power function plotted in b applies to the non-artiodactyl species in the sample, and has and exponent of -0.917 ± 0.028. Artiodactyl species in black, primates in red, glires in green, afrotherians in blue, insectivores in orange, scandentia in gray. Data from Herculano-Houzel et al. (2006, 2007, 2011), Azevedo et al. (2009), Sarko et al. (2009), Gabi et al. (2010) and Neves et al. (2014).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4228855&req=5

Figure 7: Uniform variation in the O/N ratio with neuronal density, but not structure mass. (A) Ratio between numbers of other (non-neuronal) and neuronal cells, O/N, varies in no uniform fashion across structures (cerebral cortex, circles; cerebellum, squares; rest of brain, triangles) and species (each symbol) as a function of the mass of each structure. (B) In contrast, the O/N ratio varies uniformly across brain structures and species as a function of average neuronal density in the structure. The power function plotted in b applies to the non-artiodactyl species in the sample, and has and exponent of -0.917 ± 0.028. Artiodactyl species in black, primates in red, glires in green, afrotherians in blue, insectivores in orange, scandentia in gray. Data from Herculano-Houzel et al. (2006, 2007, 2011), Azevedo et al. (2009), Sarko et al. (2009), Gabi et al. (2010) and Neves et al. (2014).
Mentions: The ratio between the numbers of other cells and neurons in each structure (the O/N ratio), which approximates the glia/neuron ratio, varies between 0.184 (in the blesbok cerebellum) and 32.333 (in the giraffe rest of brain) across structures and species in these artiodactyls (Figure 7). The O/N ratio in the artiodactyl cerebral cortex exceeds 10 when both gray and white matter are included, and within the cortical gray matter alone it varies between 7.2 and 8.5 across species (Table 1). The O/N ratio varies widely across structures and species as a function of structure mass, with no single relationship evident (Figure 7A). In contrast, the O/N ratio varies as a common power function of neuronal density across all artiodactyl structures with an exponent of -1.082 ± 0.035 (p < 0.0001), in a distribution that overlaps with the variation of O/N as a function of neuronal density across non-artiodactyl species (exponent, -0.917 ± 0.028, p < 0.0001; Figure 7B). The addition of artiodactyl structures to the distribution does not change the exponent significantly (-0.935 ± 0.024, p < 0.0001).

Bottom Line: Our findings suggest that the scaling rules found to be shared across modern afrotherians, glires, and artiodactyls applied to the common Eutherian ancestor, such as the relationship between the mass of the cerebral cortex as a whole and its number of neurons.In turn, the distribution of neurons along the surface of the cerebral cortex, which is related to its degree of gyrification, appears to be a clade-specific characteristic.If the neuronal scaling rules for artiodactyls extend to all cetartiodactyls, we predict that the large cerebral cortex of cetaceans will still have fewer neurons than the human cerebral cortex.

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, CNPq/MCT, São Paulo, Brazil.

ABSTRACT
Quantitative analysis of the cellular composition of rodent, primate, insectivore, and afrotherian brains has shown that non-neuronal scaling rules are similar across these mammalian orders that diverged about 95 million years ago, and therefore appear to be conserved in evolution, while neuronal scaling rules appear to be free to vary in a clade-specific manner. Here we analyze the cellular scaling rules that apply to the brain of artiodactyls, a group within the order Cetartiodactyla, believed to be a relatively recent radiation from the common Eutherian ancestor. We find that artiodactyls share non-neuronal scaling rules with all groups analyzed previously. Artiodactyls share with afrotherians and rodents, but not with primates, the neuronal scaling rules that apply to the cerebral cortex and cerebellum. The neuronal scaling rules that apply to the remaining brain areas are, however, distinct in artiodactyls. Importantly, we show that the folding index of the cerebral cortex scales with the number of neurons in the cerebral cortex in distinct fashions across artiodactyls, afrotherians, rodents, and primates, such that the artiodactyl cerebral cortex is more convoluted than primate cortices of similar numbers of neurons. Our findings suggest that the scaling rules found to be shared across modern afrotherians, glires, and artiodactyls applied to the common Eutherian ancestor, such as the relationship between the mass of the cerebral cortex as a whole and its number of neurons. In turn, the distribution of neurons along the surface of the cerebral cortex, which is related to its degree of gyrification, appears to be a clade-specific characteristic. If the neuronal scaling rules for artiodactyls extend to all cetartiodactyls, we predict that the large cerebral cortex of cetaceans will still have fewer neurons than the human cerebral cortex.

No MeSH data available.