Variability of the paracingulate sulcus and morphometry of the medial frontal cortex: associations with cortical thickness, surface area, volume, and sulcal depth

Abstract

The structural and functional consequences of interindividual variations in cortical morphology are poorly understood. In this study, we examined the relationship between one well-characterized variation of the medial frontal lobes, variability of the paracingulate sulcus (PCS), and grey matter volume, cortical thickness, surface area, and sulcal depth of the adjacent anterior cingulate cortex (ACC) and paracingulate cortex (PaC). Seventy-seven healthy individuals were assigned to one of four groups depending on PCS incidence in both hemispheres: left-present, right-absent; left-absent, right-present; both absent; or both present. Comparing these groups on each measure yielded four primary findings: (1) The presence of a PCS was associated with increased PaC and decreased ACC grey matter volume in the hemisphere in which it was apparent, with an almost identical pattern being observed for surface area; (2) there was a more complex relationship between PCS variability and regional thickness, such that a PCS in the left hemisphere was associated with increased left PaC and right ACC thickness, with no comparable effects being observed for the presence of a right PCS; (3) the depths of all major left hemisphere sulci in the region were strongly positively correlated, whereas no such associations were apparent in the right hemisphere; and (4) a leftward asymmetry in PaC thickness was specifically associated with better performance on a test of spatial working memory ability. These results provide evidence for a complex interhemispheric relationship between sulcal variability and cortical morphometry, and indicate that such relationships may be important for understanding individual differences in cognitive abilities.

Figure 1

Example of sulcal variability and corresponding region‐of‐interest (ROI) boundaries in a case with (A) an “absent” paracingulate sulcus (PCS) and “continuous” superior rostral sulcus (SRS) and (B) a “present” PCS and “separate” SRS. Left column presents a representative sagittal slice through the T1‐weighted image with major sulci marked in yellow. Middle column presents the reconstructed white matter (above) and pial (below) surfaces, again with the major sulci marked in yellow. The Sulci on the white matter surfaces are represented by indentations or “crevasses,” whereas gyri are represented by protrusions, or “ridges.” Right column presents the same white and pial surfaces with the six ROIs overlaid on top. The yellow lines correspond to the posterior border of the dorsal region (posterior line), the border between the dorsal and rostral regions (anterior line), and the posterior border of the subcallosal region (middle line inferior to genu). Following Vogt et al. [1995], the PaC was located in the dorsal bank of the cingulate sulcus (CS) in “absent” cases, and extended from the CS to the PCS in “present” cases. Accordingly, note how the PaC ROIs are not visible from the pial surface in case A, but are easily visualized on the white matter surface. See text for more details.

Figure 2

Steps used to calculate sulcal depth. The white and pial surfaces were averaged to create an intermediate surface that ran halfway through the cortical ribbon (the result is show in the top left). Multiple dilation and erosion operations were then applied to this surface to obtain a model of the cerebral hull (top middle). The geodesic distance from the hull to each point on the intermediate surface was measured (in mm) to produce a depth map of the entire surface [top right; see Van Essen, 2005, for more details]. Inclusive borders were delineated along the gyral crowns abutting the cingulate, paracingulate, and superior rostral sulci (CS, PCS, and SRS, respectively; bottom left). Beginning at the hull (i.e., 0 mm) and progressing deeper in increments of 0.5 mm, a threshold was set on the depth map of each individual to create a mask that comprised only buried cortex (i.e., cortex on gyral crowns was excluded; bottom middle). The thresholded mask was then applied to the inclusive sulcal traces to yield regions comprising only cortex buried in each sulcus (bottom right). In this regard, our depth measures are similar in principle to those described by Rettmann et al. [2006].

Figure 3

Mean grey matter volume (top row in mm³) and surface area (bottom row, in mm²) estimates for all six left hemisphere (left column) and right hemisphere (right column) regions, corrected for intracranial volume. In the left column, solid lines represent the groups with a left PCS and dotted lines represent groups without a left PCS. In the right column, solid lines represent groups with a right PCS and dotted lines represent groups without a right PCS. Squares represent groups that have an asymmetric PCS, triangles groups with a symmetric PCS. Error bars are not presented for ease of visualization. Standard deviations around the means are presented in the online supplementary table.

Figure 4

Mean thickness estimates for the left (LH) and right (RH) anterior cingulate cortex (ACC) and paracingulate cortex (PaC) for each PCS group, collapsed across dorsal, rostral, and subcallosal regions. Solid lines represent groups with a left PCS, dotted lines those without a left PCS. Squares represent groups showing a PCS asymmetry and triangles those with a symmetric PCS classification. Error bars are not presented for ease of visualization. Standard deviations around the means are presented in the online supplementary table.