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All brains are made of this: a fundamental building block of brain matter with matching neuronal and glial masses.

Mota B, Herculano-Houzel S - Front Neuroanat (2014)

Bottom Line: We propose that there is a fundamental building block of brain tissue: the glial mass that accompanies a unit of neuronal mass.We argue that the scaling of this glial mass is a consequence of a universal mechanism whereby numbers of glial cells are added to the neuronal parenchyma during development, irrespective of whether the neurons composing it are large or small, but depending on the average mass of the glial cells being added.We also show how evolutionary variations in neuronal cell mass, glial cell mass and number of neurons suffice to determine the most basic characteristics of brain structures, such as mass, glia/neuron ratio, neuron/glia mass ratio, and cell densities.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Física, Universidade Federal do Rio de Janeiro Rio de Janeiro, Brazil ; Instituto Nacional de Neurociência Translacional São Paulo, Brazil.

ABSTRACT
How does the size of the glial and neuronal cells that compose brain tissue vary across brain structures and species? Our previous studies indicate that average neuronal size is highly variable, while average glial cell size is more constant. Measuring whole cell sizes in vivo, however, is a daunting task. Here we use chi-square minimization of the relationship between measured neuronal and glial cell densities in the cerebral cortex, cerebellum, and rest of brain in 27 mammalian species to model neuronal and glial cell mass, as well as the neuronal mass fraction of the tissue (the fraction of tissue mass composed by neurons). Our model shows that while average neuronal cell mass varies by over 500-fold across brain structures and species, average glial cell mass varies only 1.4-fold. Neuronal mass fraction varies typically between 0.6 and 0.8 in all structures. Remarkably, we show that two fundamental, universal relationships apply across all brain structures and species: (1) the glia/neuron ratio varies with the total neuronal mass in the tissue (which in turn depends on variations in average neuronal cell mass), and (2) the neuronal mass per glial cell, and with it the neuronal mass fraction and neuron/glia mass ratio, varies with average glial cell mass in the tissue. We propose that there is a fundamental building block of brain tissue: the glial mass that accompanies a unit of neuronal mass. We argue that the scaling of this glial mass is a consequence of a universal mechanism whereby numbers of glial cells are added to the neuronal parenchyma during development, irrespective of whether the neurons composing it are large or small, but depending on the average mass of the glial cells being added. We also show how evolutionary variations in neuronal cell mass, glial cell mass and number of neurons suffice to determine the most basic characteristics of brain structures, such as mass, glia/neuron ratio, neuron/glia mass ratio, and cell densities.

No MeSH data available.


Glial cell mass scales to match neuronal cell mass across brain structures and species. Graphs show numbers of glial cells (Ng) in each brain structure in each species plotted (A) as a function of total neuronal mass (mnNn), (B) as a function of estimated average neuronal cell mass (mn), (C) as a function of number of neurons in the structure (Nn), (D) as a function of the neuronal mass per glial cell in the structure (mnNn/mg). (E) Total glial mass in each structure (mgNg) varies as a function of total neuronal mass in the structure (mnNn). Notice that numbers of glial cells in brain structures are well predicted by variations in total neuronal mass in the structure (A) and by the average neuronal mass per glial cell (D). All masses in picograms. Functions plotted are (A)Ng = 1.491 mn.Nn0.877 ± 0.022 (r2 = 0.952, p < 0.0001), (D) mn.Nn/mg, with Ng = 2.603 (mn.Nn/mg)0.913 ± 0.020 (r2 = 0.965, p < 0.0001), and (E)Mg = 3.078 Mn0.911 ± 0.019 (r2 = 0.968, p < 0.0001). Cerebral cortex plotted as circles, cerebellum as squares, and rest of brain as triangles; eulipotyphlans shown in orange, primates in red, and rodents in green. Data from Herculano-Houzel et al. (2006, 2007, 2011), Azevedo et al. (2009), Sarko et al. (2009), and Gabi et al. (2010).
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Figure 12: Glial cell mass scales to match neuronal cell mass across brain structures and species. Graphs show numbers of glial cells (Ng) in each brain structure in each species plotted (A) as a function of total neuronal mass (mnNn), (B) as a function of estimated average neuronal cell mass (mn), (C) as a function of number of neurons in the structure (Nn), (D) as a function of the neuronal mass per glial cell in the structure (mnNn/mg). (E) Total glial mass in each structure (mgNg) varies as a function of total neuronal mass in the structure (mnNn). Notice that numbers of glial cells in brain structures are well predicted by variations in total neuronal mass in the structure (A) and by the average neuronal mass per glial cell (D). All masses in picograms. Functions plotted are (A)Ng = 1.491 mn.Nn0.877 ± 0.022 (r2 = 0.952, p < 0.0001), (D) mn.Nn/mg, with Ng = 2.603 (mn.Nn/mg)0.913 ± 0.020 (r2 = 0.965, p < 0.0001), and (E)Mg = 3.078 Mn0.911 ± 0.019 (r2 = 0.968, p < 0.0001). Cerebral cortex plotted as circles, cerebellum as squares, and rest of brain as triangles; eulipotyphlans shown in orange, primates in red, and rodents in green. Data from Herculano-Houzel et al. (2006, 2007, 2011), Azevedo et al. (2009), Sarko et al. (2009), and Gabi et al. (2010).

Mentions: This finding corroborates our previous model, which proposed that the ratio Ng/Nn is achieved as glial cells of nearly invariant size infiltrate the neuronal parenchyma (of total neuronal mass defined here as Nn.mn) and proliferate until achieving confluency (Herculano-Houzel et al., 2006; Herculano-Houzel, 2011a), resulting in a glia/neuron numeric ratio that depends solely on the average size of neurons in the tissue. Thus, the final number of glial cells in the tissue should be a function of the volume of the neuronal parenchyma to be infiltrated. Here we find that, indeed, Ng varies across all structures and species as a single power function of the total neuronal mass of the structures (mn.Nn) such that Ng = 1.491 mn.Nn0.877 ± 0.022 (r2 = 0.952, p < 0.0001; Figure 12A). In contrast, Ng does not vary in a uniform manner across brain structures and species with variations in mn or in Mn alone (Figures 12B,C). Considering that, in brain development, glial cells are only added in large numbers once numbers of neurons are already established, our findings attribute variations in Ng to the product of variations in mn and in Nn, that is, in total neuronal mass in the tissue.


All brains are made of this: a fundamental building block of brain matter with matching neuronal and glial masses.

Mota B, Herculano-Houzel S - Front Neuroanat (2014)

Glial cell mass scales to match neuronal cell mass across brain structures and species. Graphs show numbers of glial cells (Ng) in each brain structure in each species plotted (A) as a function of total neuronal mass (mnNn), (B) as a function of estimated average neuronal cell mass (mn), (C) as a function of number of neurons in the structure (Nn), (D) as a function of the neuronal mass per glial cell in the structure (mnNn/mg). (E) Total glial mass in each structure (mgNg) varies as a function of total neuronal mass in the structure (mnNn). Notice that numbers of glial cells in brain structures are well predicted by variations in total neuronal mass in the structure (A) and by the average neuronal mass per glial cell (D). All masses in picograms. Functions plotted are (A)Ng = 1.491 mn.Nn0.877 ± 0.022 (r2 = 0.952, p < 0.0001), (D) mn.Nn/mg, with Ng = 2.603 (mn.Nn/mg)0.913 ± 0.020 (r2 = 0.965, p < 0.0001), and (E)Mg = 3.078 Mn0.911 ± 0.019 (r2 = 0.968, p < 0.0001). Cerebral cortex plotted as circles, cerebellum as squares, and rest of brain as triangles; eulipotyphlans shown in orange, primates in red, and rodents in green. Data from Herculano-Houzel et al. (2006, 2007, 2011), Azevedo et al. (2009), Sarko et al. (2009), and Gabi et al. (2010).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
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Figure 12: Glial cell mass scales to match neuronal cell mass across brain structures and species. Graphs show numbers of glial cells (Ng) in each brain structure in each species plotted (A) as a function of total neuronal mass (mnNn), (B) as a function of estimated average neuronal cell mass (mn), (C) as a function of number of neurons in the structure (Nn), (D) as a function of the neuronal mass per glial cell in the structure (mnNn/mg). (E) Total glial mass in each structure (mgNg) varies as a function of total neuronal mass in the structure (mnNn). Notice that numbers of glial cells in brain structures are well predicted by variations in total neuronal mass in the structure (A) and by the average neuronal mass per glial cell (D). All masses in picograms. Functions plotted are (A)Ng = 1.491 mn.Nn0.877 ± 0.022 (r2 = 0.952, p < 0.0001), (D) mn.Nn/mg, with Ng = 2.603 (mn.Nn/mg)0.913 ± 0.020 (r2 = 0.965, p < 0.0001), and (E)Mg = 3.078 Mn0.911 ± 0.019 (r2 = 0.968, p < 0.0001). Cerebral cortex plotted as circles, cerebellum as squares, and rest of brain as triangles; eulipotyphlans shown in orange, primates in red, and rodents in green. Data from Herculano-Houzel et al. (2006, 2007, 2011), Azevedo et al. (2009), Sarko et al. (2009), and Gabi et al. (2010).
Mentions: This finding corroborates our previous model, which proposed that the ratio Ng/Nn is achieved as glial cells of nearly invariant size infiltrate the neuronal parenchyma (of total neuronal mass defined here as Nn.mn) and proliferate until achieving confluency (Herculano-Houzel et al., 2006; Herculano-Houzel, 2011a), resulting in a glia/neuron numeric ratio that depends solely on the average size of neurons in the tissue. Thus, the final number of glial cells in the tissue should be a function of the volume of the neuronal parenchyma to be infiltrated. Here we find that, indeed, Ng varies across all structures and species as a single power function of the total neuronal mass of the structures (mn.Nn) such that Ng = 1.491 mn.Nn0.877 ± 0.022 (r2 = 0.952, p < 0.0001; Figure 12A). In contrast, Ng does not vary in a uniform manner across brain structures and species with variations in mn or in Mn alone (Figures 12B,C). Considering that, in brain development, glial cells are only added in large numbers once numbers of neurons are already established, our findings attribute variations in Ng to the product of variations in mn and in Nn, that is, in total neuronal mass in the tissue.

Bottom Line: We propose that there is a fundamental building block of brain tissue: the glial mass that accompanies a unit of neuronal mass.We argue that the scaling of this glial mass is a consequence of a universal mechanism whereby numbers of glial cells are added to the neuronal parenchyma during development, irrespective of whether the neurons composing it are large or small, but depending on the average mass of the glial cells being added.We also show how evolutionary variations in neuronal cell mass, glial cell mass and number of neurons suffice to determine the most basic characteristics of brain structures, such as mass, glia/neuron ratio, neuron/glia mass ratio, and cell densities.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Física, Universidade Federal do Rio de Janeiro Rio de Janeiro, Brazil ; Instituto Nacional de Neurociência Translacional São Paulo, Brazil.

ABSTRACT
How does the size of the glial and neuronal cells that compose brain tissue vary across brain structures and species? Our previous studies indicate that average neuronal size is highly variable, while average glial cell size is more constant. Measuring whole cell sizes in vivo, however, is a daunting task. Here we use chi-square minimization of the relationship between measured neuronal and glial cell densities in the cerebral cortex, cerebellum, and rest of brain in 27 mammalian species to model neuronal and glial cell mass, as well as the neuronal mass fraction of the tissue (the fraction of tissue mass composed by neurons). Our model shows that while average neuronal cell mass varies by over 500-fold across brain structures and species, average glial cell mass varies only 1.4-fold. Neuronal mass fraction varies typically between 0.6 and 0.8 in all structures. Remarkably, we show that two fundamental, universal relationships apply across all brain structures and species: (1) the glia/neuron ratio varies with the total neuronal mass in the tissue (which in turn depends on variations in average neuronal cell mass), and (2) the neuronal mass per glial cell, and with it the neuronal mass fraction and neuron/glia mass ratio, varies with average glial cell mass in the tissue. We propose that there is a fundamental building block of brain tissue: the glial mass that accompanies a unit of neuronal mass. We argue that the scaling of this glial mass is a consequence of a universal mechanism whereby numbers of glial cells are added to the neuronal parenchyma during development, irrespective of whether the neurons composing it are large or small, but depending on the average mass of the glial cells being added. We also show how evolutionary variations in neuronal cell mass, glial cell mass and number of neurons suffice to determine the most basic characteristics of brain structures, such as mass, glia/neuron ratio, neuron/glia mass ratio, and cell densities.

No MeSH data available.