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Cellular scaling rules of insectivore brains.

Sarko DK, Catania KC, Leitch DB, Kaas JH, Herculano-Houzel S - Front Neuroanat (2009)

Bottom Line: The olfactory bulbs of insectivores, however, offer a noteworthy exception in that neuronal density increases linearly with increasing structure mass.This implies that the average neuronal cell size decreases with increasing olfactory bulb mass in order to accommodate greater neuronal density, and represents the first documentation of a brain structure gaining neurons at a greater rate than mass.This might allow insectivore brains to concentrate more neurons within the olfactory bulbs without a prohibitively large and metabolically costly increase in structure mass.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Vanderbilt University Nashville, TN, USA.

ABSTRACT
Insectivores represent extremes in mammalian body size and brain size, retaining various "primitive" morphological characteristics, and some species of Insectivora are thought to share similarities with small-bodied ancestral eutherians. This raises the possibility that insectivore brains differ from other taxa, including rodents and primates, in cellular scaling properties. Here we examine the cellular scaling rules for insectivore brains and demonstrate that insectivore scaling rules overlap somewhat with those for rodents and primates such that the insectivore cortex shares scaling rules with rodents (increasing faster in size than in numbers of neurons), but the insectivore cerebellum shares scaling rules with primates (increasing isometrically). Brain structures pooled as "remaining areas" appear to scale similarly across all three mammalian orders with respect to numbers of neurons, and the numbers of non-neurons appear to scale similarly across all brain structures for all three orders. Therefore, common scaling rules exist, to different extents, between insectivore, rodent, and primate brain regions, and it is hypothesized that insectivores represent the common aspects of each order. The olfactory bulbs of insectivores, however, offer a noteworthy exception in that neuronal density increases linearly with increasing structure mass. This implies that the average neuronal cell size decreases with increasing olfactory bulb mass in order to accommodate greater neuronal density, and represents the first documentation of a brain structure gaining neurons at a greater rate than mass. This might allow insectivore brains to concentrate more neurons within the olfactory bulbs without a prohibitively large and metabolically costly increase in structure mass.

No MeSH data available.


Related in: MedlinePlus

Dissection techniques and morphology of the insectivore brains examined in the present study. (A) Dissection of an eastern mole brain [shown whole in (B) and illustrated in (C)] illustrates brain structures of interest including, from top to bottom, the olfactory bulbs, cortex (lateral view for the left cortex and medial view for the right cortex), left and right hippocampus (shown in the second row of structures lateral to the left and right cortex, respectively), cerebellum, and the remaining areas (bottom row of structures including the striatum peeled away from the cortex at the left and right with subcortical structures in the center). (C) Representative brains of the smoky shrew, short-tailed shrew, star-nosed mole, and eastern mole are illustrated at a lateral view to show macromorphology and relative size (hairy-tailed mole brain not shown, but is similar in size to a star-nosed mole brain – see Table 1).
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Figure 1: Dissection techniques and morphology of the insectivore brains examined in the present study. (A) Dissection of an eastern mole brain [shown whole in (B) and illustrated in (C)] illustrates brain structures of interest including, from top to bottom, the olfactory bulbs, cortex (lateral view for the left cortex and medial view for the right cortex), left and right hippocampus (shown in the second row of structures lateral to the left and right cortex, respectively), cerebellum, and the remaining areas (bottom row of structures including the striatum peeled away from the cortex at the left and right with subcortical structures in the center). (C) Representative brains of the smoky shrew, short-tailed shrew, star-nosed mole, and eastern mole are illustrated at a lateral view to show macromorphology and relative size (hairy-tailed mole brain not shown, but is similar in size to a star-nosed mole brain – see Table 1).

Mentions: Animals were given an overdose of sodium pentobarbital (at least 120 mg/kg) and perfused transcardially with 0.01 M phosphate-buffered saline (PBS, pH 7.2) followed by 4% paraformaldehyde in 0.01 M PBS (pH 7.2). The brains were removed from the skulls, then blocked at the level of the foramen magnum and dissected free of dura mater and superficial blood vessels followed by postfixation for 2–4 weeks by immersion in 4% phosphate-buffered paraformaldehyde. Each brain was dried of excess paraformaldehyde and weighed as a whole, then dissected. The cerebellum was dissected by cutting the cerebellar peduncles at the surface of the brainstem. The cerebral cortex in all animals was obtained by peeling away the striatum and other subcortical structures, excluding the hippocampus which was dissected separately from each hemisphere, under a Zeiss stereoscope. The olfactory bulbs were also dissected and weighed individually. All other brain structures were pooled and processed together as “remaining areas.” A representative dissection of one brain, that of an eastern mole, is shown in Figure 1A followed by an image of the intact whole brain (Figure 1B). Illustrations of the brains of smoky shrews, short-tailed shrews, star-nosed moles, and eastern moles are also given in order to show overall macromorphology and the relative size of each brain (Figure 1C). In all species, left and right cortical hemispheres, olfactory bulbs, and hippocampus were counted separately and added together to estimate numbers for the whole brain and to discriminate left/right differences. An unpaired Mann–Whitney U test was run using Statview, and p > 0.5 for the cortex, hippocampus, and olfactory bulbs, showing no significant difference between left and right regions and allowing them to be pooled together for analysis of each structure.


Cellular scaling rules of insectivore brains.

Sarko DK, Catania KC, Leitch DB, Kaas JH, Herculano-Houzel S - Front Neuroanat (2009)

Dissection techniques and morphology of the insectivore brains examined in the present study. (A) Dissection of an eastern mole brain [shown whole in (B) and illustrated in (C)] illustrates brain structures of interest including, from top to bottom, the olfactory bulbs, cortex (lateral view for the left cortex and medial view for the right cortex), left and right hippocampus (shown in the second row of structures lateral to the left and right cortex, respectively), cerebellum, and the remaining areas (bottom row of structures including the striatum peeled away from the cortex at the left and right with subcortical structures in the center). (C) Representative brains of the smoky shrew, short-tailed shrew, star-nosed mole, and eastern mole are illustrated at a lateral view to show macromorphology and relative size (hairy-tailed mole brain not shown, but is similar in size to a star-nosed mole brain – see Table 1).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2713736&req=5

Figure 1: Dissection techniques and morphology of the insectivore brains examined in the present study. (A) Dissection of an eastern mole brain [shown whole in (B) and illustrated in (C)] illustrates brain structures of interest including, from top to bottom, the olfactory bulbs, cortex (lateral view for the left cortex and medial view for the right cortex), left and right hippocampus (shown in the second row of structures lateral to the left and right cortex, respectively), cerebellum, and the remaining areas (bottom row of structures including the striatum peeled away from the cortex at the left and right with subcortical structures in the center). (C) Representative brains of the smoky shrew, short-tailed shrew, star-nosed mole, and eastern mole are illustrated at a lateral view to show macromorphology and relative size (hairy-tailed mole brain not shown, but is similar in size to a star-nosed mole brain – see Table 1).
Mentions: Animals were given an overdose of sodium pentobarbital (at least 120 mg/kg) and perfused transcardially with 0.01 M phosphate-buffered saline (PBS, pH 7.2) followed by 4% paraformaldehyde in 0.01 M PBS (pH 7.2). The brains were removed from the skulls, then blocked at the level of the foramen magnum and dissected free of dura mater and superficial blood vessels followed by postfixation for 2–4 weeks by immersion in 4% phosphate-buffered paraformaldehyde. Each brain was dried of excess paraformaldehyde and weighed as a whole, then dissected. The cerebellum was dissected by cutting the cerebellar peduncles at the surface of the brainstem. The cerebral cortex in all animals was obtained by peeling away the striatum and other subcortical structures, excluding the hippocampus which was dissected separately from each hemisphere, under a Zeiss stereoscope. The olfactory bulbs were also dissected and weighed individually. All other brain structures were pooled and processed together as “remaining areas.” A representative dissection of one brain, that of an eastern mole, is shown in Figure 1A followed by an image of the intact whole brain (Figure 1B). Illustrations of the brains of smoky shrews, short-tailed shrews, star-nosed moles, and eastern moles are also given in order to show overall macromorphology and the relative size of each brain (Figure 1C). In all species, left and right cortical hemispheres, olfactory bulbs, and hippocampus were counted separately and added together to estimate numbers for the whole brain and to discriminate left/right differences. An unpaired Mann–Whitney U test was run using Statview, and p > 0.5 for the cortex, hippocampus, and olfactory bulbs, showing no significant difference between left and right regions and allowing them to be pooled together for analysis of each structure.

Bottom Line: The olfactory bulbs of insectivores, however, offer a noteworthy exception in that neuronal density increases linearly with increasing structure mass.This implies that the average neuronal cell size decreases with increasing olfactory bulb mass in order to accommodate greater neuronal density, and represents the first documentation of a brain structure gaining neurons at a greater rate than mass.This might allow insectivore brains to concentrate more neurons within the olfactory bulbs without a prohibitively large and metabolically costly increase in structure mass.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Vanderbilt University Nashville, TN, USA.

ABSTRACT
Insectivores represent extremes in mammalian body size and brain size, retaining various "primitive" morphological characteristics, and some species of Insectivora are thought to share similarities with small-bodied ancestral eutherians. This raises the possibility that insectivore brains differ from other taxa, including rodents and primates, in cellular scaling properties. Here we examine the cellular scaling rules for insectivore brains and demonstrate that insectivore scaling rules overlap somewhat with those for rodents and primates such that the insectivore cortex shares scaling rules with rodents (increasing faster in size than in numbers of neurons), but the insectivore cerebellum shares scaling rules with primates (increasing isometrically). Brain structures pooled as "remaining areas" appear to scale similarly across all three mammalian orders with respect to numbers of neurons, and the numbers of non-neurons appear to scale similarly across all brain structures for all three orders. Therefore, common scaling rules exist, to different extents, between insectivore, rodent, and primate brain regions, and it is hypothesized that insectivores represent the common aspects of each order. The olfactory bulbs of insectivores, however, offer a noteworthy exception in that neuronal density increases linearly with increasing structure mass. This implies that the average neuronal cell size decreases with increasing olfactory bulb mass in order to accommodate greater neuronal density, and represents the first documentation of a brain structure gaining neurons at a greater rate than mass. This might allow insectivore brains to concentrate more neurons within the olfactory bulbs without a prohibitively large and metabolically costly increase in structure mass.

No MeSH data available.


Related in: MedlinePlus