A Survey of White Matter Neurons at the Gyral Crowns and Sulcal Depths in the Rhesus Monkey

Abstract

Gyrencephalic brains exhibit deformations of the six neocortical laminae at gyral crowns and sulcal depths, where the deeper layers are, respectively, expanded and compressed. The present study addresses: (1) the degree to which the underlying white matter neurons (WMNs) observe the same changes at gyral crowns and sulcal depths; and (2) whether these changes are consistent or variable across different cortical regions. WMNs were visualized by immunohistochemistry using the pan-neuronal label NeuN, and their density was quantified in eight rhesus monkey brains for four regions; namely, frontal (FR), superior frontal gyrus (SFG), parietal (Par) and temporal (TE). In all four regions, there were about 50% fewer WMNs in the sulcal depth, but there was also distinct variability from region to region. For the gyral crown, we observed an average density per 0.21 mm2 of 82 WMNs for the FR, 51 WMNs for SFG, 80 WMNs for Par and 93 WMNs for TE regions. By contrast, for the sulcal depth, the average number of WMNs per 0.21 mm2 was 41 for FR, 31 for cingulate sulcus (underlying the SFG), 54 for Par and 63 for TE cortical regions. Since at least some WMNs participate in cortical circuitry, these results raise the possibility of their differential influence on cortical circuitry in the overlying gyral and sulcal locations. The results also point to a possible role of WMNs in the differential vulnerability of gyral vs. sulcal regions in disease processes, and reinforce the increasing awareness of the WMNs as part of a complex, heterogeneous and structured microenvironment.

The distribution, number, and certain neurochemical identities of infracortical white matter neurons in a lar gibbon (Hylobates lar) brain

“…While the current study is based on a single specimen, this individual showed no neuropathologies and was in excellent condition when euthanized. Moreover, our results regarding the distribution, neurochemistry, and density gradients of WMICs in the lar gibbon are generally consistent with those previously reported in other mammalian species, including other primates (Barbaresi, Fabri, & Mensa, ; Barone & Kennedy, ; Chun & Shatz, ; Clancy et al, , ; García‐Marin et al, ; Meyer et al, ; Mortazavi et al, , ; Reep, ; Tomioka & Rockland, ). Thus, we assume that the description provided herein is likely to be representative of the lar gibbon as a species, but temper the strength of our conclusions according to the limitation of only having examined a single specimen.…”

“…Our analysis showed significant decreases in WMIC densities with depth in the white matter, that the densities are higher deep to gyral crowns rather than sulcal fundi, and that of all the subcortical white matters regions examined, that deep to the primary visual cortex exhibited the highest densities. While these findings are, for the most part, in agreement with previous qualitative assessments of the variation in WMIC densities (Barbaresi et al, 2014;Barone & Kennedy, 2000;Chun & Shatz, 1989;Clancy et al, 2001Clancy et al, , 2009García-Marin et al, 2010;Meyer et al, 1992;Mortazavi et al, 2016Mortazavi et al, , 2017Reep, 2000;Tomioka & Rockland, 2007), the increased density beneath primary visual cortex is of particular interest. It is well known that the primary visual cortex in primates exhibits a cell density at least two times higher than other cortical (reflecting the lower cortical cell densities in motor cortical regions, e.g., Collins et al, 2016;Turner et al, 2016) are only 1.5 times the median densities observed in the parietal and temporal lobes.…”

“…These cells are neuronal, with neurochemical studies showing both glutamatergic and GABAergic phenotypes (García‐Marin, Blazquez‐Llorca, Rodriguez, Gonzalez‐Soriano, & DeFelipe, ; Meyer, Wahle, Castaneyra‐Perdomo, & Ferres‐Torres, ; Suárez‐Solá et al, ; von Engelhardt et al, ). Given their sparse distribution and relative inaccessibility, the function, synaptic relationships, and connectivity of WMICs have only been studied sporadically; however, due to more recent findings concerning the relationship of the infracortical telencephalic white matter to cognition and neural dysfunction in humans (Connor, Crawford, & Akbarian, ; Fields, ; Filley & Fields, ), there is a resurgence of interest in various aspects of the morphology and physiology of the white matter, including the WMICs (Kostovic, Judas, & Sedmak, ; Mortazavi, Romano, Rosene, & Rockland, ; Mortazavi, Wang, Rosene, & Rockland, ; Suárez‐Solá et al, ).…”

“…findings concerning the relationship of the infracortical telencephalic white matter to cognition and neural dysfunction in humans (Connor, Crawford, & Akbarian, 2011;Fields, 2008;Filley & Fields, 2016), there is a resurgence of interest in various aspects of the morphology and physiology of the white matter, including the WMICs (Kostovic, Judas, & Sedmak, 2011;Mortazavi, Romano, Rosene, & Rockland, 2017;Mortazavi, Wang, Rosene, & Rockland, 2016;Suárez-Solá et al, 2009).…”

Projections to the putamen from neurons located in the white matter and the claustrum in the macaque

“…The results showed widespread labeling of both superficial and deep WMNs, demonstrating that this circuit is phylogenetically conserved across species and extending our knowledge concerning the local and long‐distance projections of these neurons. In fact, although several publications have characterized WMNs in terms of density, morphology, and neurochemical heterogeneity (rat: Clancy, Silva‐Filho, & Friedlander, ; human: Meyer, Wahle, Castaneyra‐Perdomo, & Ferres‐Torres, ; García‐Marín, Blazquez‐Llorca, Rodriguez, Gonzalez‐Soriano, & DeFelipe, ; NHP: Mortazavi, Wang, Rosene, & Rockland, ; Mortazavi, Romano, Rosene, & Rockland, ; Swiegers et al, and references therein), only scant attention has been paid to their connectivity.…”