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.

Highlights

  • The structural and connectional heterogeneity of cortical sulcal and gyral regions is well known in the context of laminar deformation (Welker, 1990) and, more recently, in the context of what may be increased axonal fiber density near the gyral crowns (e.g., Nie et al, 2012; Deng et al, 2013)

  • We found a consistent reduction from zones 1 and 2, where comparable numbers in zone 2 are, for TEd, FIGURE 7 | (A) No significant differences in density of sulcal and gyral white matter neurons (WMNs) were found between superior temporal gyrus (STG) and inferior temporal gyrus (TEd). (B) Significantly progressive fall-off in WMN density with distance from the gyral crown; the fall off in density of WMNs was significantly different between STG and TEd at the most distal zones. ∗p < 0.05

  • We report that there is an inhomogeneous arrangement of WMNs, especially in the outer 2.0 mm nearest the gyral crown, where WMNs typically exhibit a pattern of quasi-regular neuron-sparse circles, 120–250 μm in diameter

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Summary

Introduction

The structural and connectional heterogeneity of cortical sulcal and gyral regions is well known in the context of laminar deformation (Welker, 1990) and, more recently, in the context of what may be increased axonal fiber density near the gyral crowns (e.g., Nie et al, 2012; Deng et al, 2013). Overlooked in these discussions is what happens to the population of white matter. Transcriptomic analyses point to some association with cognitive conditions (HoerderSuabedissen et al, 2013; Hoerder-Suabedissen and Molnár, 2015)

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