Gender-specific left-right asymmetries in human visual cortex

Abstract

The structural correlates of gender differences in visuospatial processing are essentially unknown. Our quantitative analysis of the cytoarchitecture of the human primary visual cortex [V1/Brodmann area 17 (BA17)], neighboring area V2 (BA18), and the cytoarchitectonic correlate of the motion-sensitive complex (V5/MT+/hOc5) shows that the visual areas are sexually dimorphic and that the type of dimorphism differs among the areas. Gender differences exist in the interhemispheric asymmetry of hOc5 volumes and in the right-hemispheric volumetric ratio of hOc5 to BA17, an area that projects to V5/MT+/hOc5. Asymmetry was also observed in the surface area of hOc5 but not in its cortical thickness. The differences give males potentially more space in which to process additional information, a finding consistent with superior male processing in particular visuospatial tasks, such as mental rotation. Gender differences in hOc5 exist with similar volume fractions of cell bodies, implying that, overall, the visual neural circuitry is similar in males and females.

Figure 1.

A, Surface rendering of a 3D-reconstructed dataset of a human brain (female, 72 years of age). Right hemisphere, posterolateral view. hOc5 (red) was projected to the free surface of the brain. The area is mainly hidden in the depths of two sulci; the anterior occipital sulcus (aqua) and the inferior lateral occipital sulcus (yellow). The dotted line marks the approximate location of the histological section shown in B. B, The location of hOc5 is labeled in red. C, Cytoarchitecture of area hOc5 (red transparency) in the histological section at higher magnification.

Figure 2.

A, Definition of cortical borders of hOc5 in a cell-body-stained histological section of a postmortem brain using an observer-independent method (Schleicher et al., 1999). GLI image of a coronal section from the region of the anterior occipital sulcus (SOA) and the inferior lateral occipital sulcus (SOL₁). Arrowheads and lines indicate the borders between area hOc5 and the neighboring dorsal (D) and ventral (V) areas. The cortex is covered from the layer I/II border to the layer VI/white matter border by a series of traverses. Along these traverses, profiles, which capture laminar changes of the GLI (i.e., the volume fraction of cell bodies) from the surface to the white matter, i.e., the cytoarchitecture, were extracted. Profiles are numbered from 1 to 169. B, Multivariate distance D (Mahalanobis distance) as a measure of similarity of neighboring blocks of profiles in dependence on the profile number. Block size b = 14 profiles. Significant peaks of D indicate positions of cytoarchitectonic borders. They were found at positions 39 (dorsal border) and 126 (ventral border). C, The distance D was calculated for different block sizes ranging from b = 8 to 24. The distance for b = 14 is highlighted.

Figure 3.

Dorsal border of area hOc5 with area D. The sizes of pyramidal cells in sublayer IIIc are larger in area hOc5 than in area D. Roman numerals indicate cortical layers. Scale bar, 0.5 mm. Same border as in Figure 2 at position 39.

Figure 4.

Definition of the surfaces of area hOc5 in a 3D-reconstructed postmortem brain. A, Label of the area in a histological section. B, Region of interest of A but at higher magnification. Bold lines mark the outer (dark yellow) and inner (red) contours of the area. C, Surface reconstruction of the area, view from the sulcus. The approximate positions of the histological sections, in which hOc5 was delineated, are indicated by green lines. The topmost line corresponds to the section shown in A.

Figure 5.

Reconstruction of the inner (cortex–white matter) surface of BA17 in serial histological sections of a left hemisphere. View into the calcarine sulcus. A, The sequence of contours of the delineated area (“tubes”) in histological sections is projected to the surface. The distance between histological sections is 1.2 mm (distance between tubes). The calcarine sulcus can be identified as the elongated concave structure, which is surrounded by the “U-shaped” area. B and C show two regions with triangulation (yellow triangles) at higher magnification. Note the regular shape of the triangles. A total of 200,000 triangles have been generated in this particular area to create its surface. The arrow cross shows the orientation within the brain: green arrow, dorsal/ventral; blue arrow, caudal/rostral; red arrow, medial/lateral.

Figure 6.

Mean ± SE volumes and surface areas of areas hOc5 (top row), BA17 (middle row), and BA18 (bottom row) of right and left hemispheres, in males and females. The amount and direction of the bilateral asymmetry of hOc5 differs between genders (p < 0.05). Whereas males showed a significant right-larger-than-left asymmetry in volume and surface of hOc5, females were more symmetrical.

Figure 7.

Ratios (in percentage, ±SE) between volumes of hOc5-to-BA17 and hOc5-to-BA18 (top row) show a significant gender difference for right hOc5-to-BA17 (p < 0.05) and a similar but nonsignificant tendency for right hOc5-to-BA18 (p = 0.06). In the right hemisphere, the female ratios were approximately twice as small as they are in male brains (for both hOc5-to-BA17 and hOc5-to-BA18). Ratios did not differ between each other in the left hemisphere. Ratios between surfaces of the areas (bottom row) show similar directions of asymmetry (p > 0.05).

Figure 8.

Volume fraction of cell bodies (GLI ± SE) has significantly higher values on the right than left side, in all three areas, regardless of gender. The larger GLI values on the right mean that there are more cell bodies and less room for neuropil; dendrites, axons, synapses.

Figure 9.

Mean ± SD cortical thicknesses of areas hOc5, BA17, and BA18 for the left and the right hemisphere, separately for males (n = 5) and females (n = 5). Note that the thickness is smaller in BA17 plus BA18 than in hOc5. Females have a thicker cortex than males in BA18, whereas males have a thicker hOc5 cortex than females.