Cerebral sex dimorphism and sexual orientation

Abstract

The neurobiology of sexual orientation is frequently discussed in terms of cerebral sex dimorphism (defining both functional and structural sex differences). Yet, the information about possible cerebral differences between sex-matched homo and heterosexual persons is limited, particularly among women. In this multimodal MRI study, we addressed these issues by investigating possible cerebral differences between homo and heterosexual persons, and by asking whether there is any sex difference in this aspect. Measurements of cortical thickness (Cth), subcortical volumes, and functional and structural resting-state connections among 40 heterosexual males (HeM) and 40 heterosexual females (HeF) were compared with those of 30 homosexual males (HoM) and 30 homosexual females (HoF). Congruent with previous reports, sex differences were detected in heterosexual controls with regard to fractional anisotropy (FA), Cth, and several subcortical volumes. Homosexual groups did not display any sex differences in FA values. Furthermore, their functional connectivity was significantly less pronounced in the mesial prefrontal and precuneus regions. In these two particular regions, HoM also displayed thicker cerebral cortex than other groups, whereas HoF did not differ from HeF. In addition, in HoM the parietal Cth showed "sex-reversed" values, not observed in HoF. Homosexual orientation seems associated with a less pronounced sexual differentiation of white matter tracts and a less pronounced functional connectivity of the self-referential networks compared to heterosexual orientation. Analyses of Cth suggest that male and female homosexuality are not simple analogues of each other and that differences from heterosexual controls are more pronounced in HoM.

Keywords: brain; cerebral sex dimorphism; sex; sexual orientation.

Figure 1

Group differences in cortical thickness. HoM = homosexual men; HeF = heterosexual women; HoM = homosexual men; HeM = heterosexual men. The contrasts were calculated at p < .05, FWE corrected for multiple comparisons (Monte Carlo permutation). The projection of cerebral hemispheres (MR images of the FreeSurfer atlas) is standardized. Scale is logarithmic and sHoFs −log 10(P), with cool colors indicating negative contrast, and warm colors positive contrast. The figure illustrates two major findings: (a) Whereas no differences were detected between HoF and HeF, the HoM‐HeM contrast displayed clusters suggesting both “sex reversed” (left parietal cortex) and singular (mPFC‐ and precuneus‐clusters) features. (b) Cth values in the left superior parietal cortex in the two homosexual groups were in‐between those of HeF and HeM

Figure 2

Group difference in FA values. The differences are illustrated in red–yellow and blue and superimposed on the group skeleton (green). These clusters were calculated at p < .05, FWE corrected for multiple comparisons. HeM‐HeF (upper row, indicated in red–yellow) and HoM‐HoF (lower raw, indicated in blue, showing only a small cluster). z coordinates of the MNI atlas are indicated. R = right side; L = left side

Figure 3

Group difference, in rs‐fMRI, default mode network (DMN) significant group differences in resting‐state functional connections within the default mode network (which was also used as a mask and is indicated in pale yellow). Differences between HeF and HoF are indicated in red–yellow; the corresponding cluster for the HeM‐HoM contrast is indicated in blue. Clusters calculated at p < .01, FWE corrected. MNI coordinates for the two clusters are indicated. The Y‐coordinate for the lower precuneus cluster is −50. See also Table 4