Multimodal MRI suggests that male homosexuality may be linked to cerebral midline structures

Abstract

The neurobiology of sexual preference is often discussed in terms of cerebral sex dimorphism. Yet, our knowledge about possible cerebral differences between homosexual men (HoM), heterosexual men (HeM) and heterosexual women (HeW) are extremely limited. In the present MRI study, we addressed this issue investigating measures of cerebral anatomy and function, which were previously reported to show sex difference. Specifically, we asked whether there were any signs of sex atypical cerebral dimorphism among HoM, if these were widely distributed (providing substrate for more general 'female' behavioral characteristics among HoM), or restricted to networks involved in self-referential sexual arousal. Cortical thickness (Cth), surface area (SA), subcortical structural volumes, and resting state functional connectivity were compared between 30 (HoM), 35 (HeM) and 38 (HeW). HoM displayed a significantly thicker anterior cingulate cortex (ACC), precuneus, and the left occipito-temporal cortex compared to both control groups. These differences seemed coordinated, since HoM also displayed stronger cortico-cortical covariations between these regions. Furthermore, functional connections within the default mode network, which mediates self- referential processing, and includes the ACC and precuneus were significantly weaker in HoM than HeM and HeW, whereas their functional connectivity between the thalamus and hypothalamus (important nodes for sexual behavior) was stronger. In addition to these singular features, HoM displayed 'female' characteristics, with a similar Cth in the left superior parietal and cuneus cortices as HeW, but different from HeM. These data suggest both singular and sex atypical features and motivate further investigations of cerebral midline structures in relation to male homosexuality.

Fig 1. Group comparisons for Cth.

The contrasts were calculated at p < .05, corrected for multiple comparisons (Monte Carlo permutation), using age as the covariate of no interest. The projection of cerebral hemispheres (MR images of the FreeSurfer atlas) is standardized. Scale is logarithmic and shows–log10(P), with cool colors indicating negative contrast, warm colors positive contrast. The two smaller images at the bottom illustrate Cth in HeM-HoM (left) and HeW–HoM (right) calculated without Monte Carlo correction; they were added to illustrate the HoM differed from both control groups in a similar manner.

Fig 2. Cortical thickness, conjunctional clusters HoM- Controls.

Sagital view of the standard brain MRI (atlas retrieved from the FreeSurfer program’s pipeline), showing regions in which HoM differed from both control groups with respect to Cth. Scale is logarithmic and shows–log10(P), with cool colors indicating negative contrast (thicker cortex in HoM than both control groups), warm colors positive contrast (thicker cortex in control groups).

Fig 3. Group comparisons for surface area.

The contrasts were calculated at p < .05, corrected for multiple comparisons (Monte Carlo permutation), using age as the covariate of no interest. The projection of cerebral hemispheres (MR images of the FreeSurfer atlas) is standardized. Scale is logarithmic and shows–log10(P), with cool colors indicating negative contrast, warm colors positive contrast. The two smaller images at the bottom illustrate Cth in HeM-HoM (left) and HeW–HoM (right) calculated without Monte Carlo correction; they were added to illustrate the HoM differed from both control groups in a similar manner.

Fig 4. Group differences in the default mode network (DMN).

The network (DMN) is depicted in yellow. Decreased connectivity in HoM compared to HeW is shown in pink, decreased connectivity in HoM compared to HeM in blue. Clusters calculated at p<0.05 FEW corrected. There were no significant differences among the controls. Cluster coordinates (MNI) in the figure are X = 10, Y = -42, Z = 28.