Abstract
How are neurons distributed along the cortical surface and across functional areas? Here we use the isotropic fractionator (Herculano-Houzel and Lent, 2005) to analyze the distribution of neurons across the entire isocortex of the mouse, divided into 18 functional areas defined anatomically. We find that the number of neurons underneath a surface area (the N/A ratio) varies 4.5-fold across functional areas and neuronal density varies 3.2-fold. The face area of S1 contains the most neurons, followed by motor cortex and the primary visual cortex. Remarkably, while the distribution of neurons across functional areas does not accompany the distribution of surface area, it mirrors closely the distribution of cortical volumes—with the exception of the visual areas, which hold more neurons than expected for their volume. Across the non-visual cortex, the volume of individual functional areas is a shared linear function of their number of neurons, while in the visual areas, neuronal densities are much higher than in all other areas. In contrast, the 18 functional areas cluster into three different zones according to the relationship between the N/A ratio and cortical thickness and neuronal density: these three clusters can be called visual, sensory, and, possibly, associative. These findings are remarkably similar to those in the human cerebral cortex (Ribeiro et al., 2013) and suggest that, like the human cerebral cortex, the mouse cerebral cortex comprises two zones that differ in how neurons form the cortical volume, and three zones that differ in how neurons are distributed underneath the cortical surface, possibly in relation to local differences in connectivity through the white matter. Our results suggest that beyond the developmental divide into visual and non-visual cortex, functional areas initially share a common distribution of neurons along the parenchyma that become delimited into functional areas according to the pattern of connectivity established later.
Highlights
How are neurons distributed across the surface of the cerebral cortex, and how does this distribution compare across functional areas as diverse as those that process specific sensory signals or associate information from various modalities? The mammalian cerebral cortex has traditionally been considered a homogeneous structure, with a constant number of neurons per surface area (N/A) across both cortical areas and species
Our analysis of the distribution of neurons across functional areas of the mouse cerebral cortex shows that most neurons are concentrated in the primary somatosensory cortex, which contains 25% of all cortical neurons, followed by the motor cortex, with 10% of all neurons, and the primary visual cortex, with 9%
The shared relationship across cortical areas between cortical volume and number of other cells indicates that the distribution of other cells is homogeneous across cortical volumes, with local variations in density that are related to local variations in neuronal density
Summary
How are neurons distributed across the surface of the cerebral cortex, and how does this distribution compare across functional areas as diverse as those that process specific sensory signals or associate information from various modalities? The mammalian cerebral cortex has traditionally been considered a homogeneous structure, with a constant number of neurons per surface area (N/A) across both cortical areas and species (with the exception of primary visual cortex; Rockel et al, 1980). Recent quantitative studies by our group and others have shown that the N/A ratio is neither homogeneous across primate species (HerculanoHouzel et al, 2008), nor homogeneous across the cortical surface of primates (Collins et al, 2010; Cahalane et al, 2012) The latter studies found the largest neuronal densities, which indicate the smallest average neuronal sizes, in the posterior, visual areas of the cerebral cortex, and the smallest neuronal densities, which indicate the largest average neuronal sizes (including all dendritic branches), in the frontal-most areas of primate cortex. Such differences are compatible with the sensory function of the visual areas, which relies heavily on local computation, and the associative function of the frontalmost areas, which requires massive integration of information from across the cerebral cortex
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