Neuron densities vary across and within cortical areas in primates

Abstract

The numbers and proportion of neurons in areas and regions of cortex were determined for a single cortical hemisphere from two prosimian galagos, one New World owl monkey, one Old World macaque monkey, and one baboon. The results suggest that there is a common plan of cortical organization across the species examined here and also differences that suggest greater specializations in the Old World monkeys. In all primates examined, primary visual cortex (V1) was the most neuron-dense cortical area and the secondary visual areas had higher-than-average densities. Primary auditory and somatosensory areas tended to have high densities in the Old World macaque and baboon. Neuronal density varies less across cortical areas in prosimian galagos than in the Old World monkeys. Thus, cortical architecture varies greatly within and across primate species, but cell density is greater in cortex devoted to the early stages of sensory processing.cell density | cortex | isotropic fractionator | neuron number T he basic building blocks of information-processing circuits, the neurons and nonneuron cells of the cerebral cortex, have never been quantified in relation to identified cortical areas and regions across the entire cortical sheet. Several studies have reported total numbers of cells and neurons for the entire cortex (1-4). These reports are useful for examining cortical scaling principles across species, but because the cerebral cortex is such a heterogeneous structure with multiple parallel sensory and motor processing systems, whole-cortex cell number data have limited utility for understanding cortical information-processing circuits. Studies that have analyzed the cellular composition of particular cortical areas generally focused on a single cortical area or examined a limited number of areas. These studies (e.g., ref. 5) provide valuable comparative data, and a recent review thoughtfully considers differences between species (6). However, a global examination of the cellular composition of the cortical expanse with attention to cortical areas is clearly lacking in the published literature. A cellular and neuronal density map of the cortex of a number of species of primates and other mammals would contribute to interpretations of neuroimaging data in clinical and in cognitive neuroscience experimental settings. The density map also would improve our knowledge of processing circuits in the cortex and provide a foundation on which to build a cortical connection map (7) and on which to base neural network models of cortical function. The data presented here begin to fill this gap in our knowledge of cellular distribution patterns in the cortex.Although it seems obvious that areas and regions of the cortex vary in neuronal densities according to information-processing demands, there currently is little data on cell numbers and distribution across the cortex within and across species. Small data sets examining a few cortical areas often have generated erroneous conclusions. For example, results from one study are pervasive...

Large-Scale Gradients in Human Cortical Organization

“…While this labor-intensive approach provides a detailed account of cortical microstructure, the resulting descriptions typically remain qualitative and observer dependent (but see [14]). A more recent line of research takes a simplified view of cortical microstructure by reducing it to a single quantity: the number of neurons within a unit of surface area [15][16][17][18]. These studies have demonstrated a rostrocaudal gradient in neuron number in the cortices of a broad range of mammalian species, including several rodents, marsupials, and non-human primates.…”

“…For example, elevated neuron numbers have been reported in rostrolateral regions mapping to putative primary somatosensory cortex in multiple species [15,16,18]. Such observations raise the question of whether regular spatial patterns beyond the rostrocaudal gradient can be identified in cortical microstructure.…”

Parcellations and Connectivity Patterns in Human and Macaque Cerebral Cortex

“…In the macaque, a fivefold range of neuronal cell density (neurons per gram of cortex) has been demonstrated using quantitative methods of cell fractionation applied to small patches of cortical gray matter (Collins et al 2010). These cell density differences are correlated with the pattern of myelination, insofar as high neuronal density occurs in heavily myelinated early sensory and low density in the lightly myelinated 'higher' cortical areas (though the correlation is imperfect as heavily myelinated motor cortex has low neuronal density).…”

“…The cerebral neocortex is a sheet-like structure that in the macaque contains~1.4 billion neurons/hemisphere deployed over a surface area of~105 cm 2 per hemisphere-equivalent to a pair of~12 cm diameter cookies (Collins et al 2010;Van Essen et al 2012b). Human cortex has about fourfold more neurons (~8 billion/hemisphere) and ninefold greater surface area (~973 AE 88 cm 2 /hemisphere), equivalent to a pair of 35 cm pizzas (Azevedo et al 2009;Van Essen et al 2012c).…”

Epileptic baboons have lower numbers of neurons in specific areas of cortex

“…9 and 10) that vary according to their processing demands, connectivity (e.g., refs. 11 and 12), and intrinsic numbers of cells and neurons (13)(14)(15)(16). Chronic seizures have been associated with progressive changes in the region of the epileptic focus and in remote but functionally connected cortical or subcortical structures (3,17).…”