Sex differences in the brains of capuchin monkeys (Sapajus [Cebus] apella)

Abstract

This study reports an analysis of 20 T1-weighted magnetic resonance imaging scans from tufted capuchin monkeys (5 male, 15 female). We carried out a data-driven, whole-brain volumetric analysis on regional gray matter anatomy using voxel-based morphometry. This revealed that males showed statistically significant expansion of a region of the hypothalamus, while females showed significant expansion in a distributed set of regions, including the cerebellum, early visual cortex, and higher-order visual regions spanning occipital and temporal cortex. In order to elucidate the network connectivity of these regions, we employed probabilistic tractography on diffusion tensor imaging data. This showed that the female-enlarged regions connect with distributed association networks across the brain. Notably, this contrasts with rodent studies, where sex differences are focused in deep, ancestral limbic regions involved in the control of reproductive behavior. Additionally, in our data set, for several regions, male and female volumetric measures were completely nonoverlapping. This contrasts with human studies, where sex differences in cortical regions have been reported but are characterized by overlapping rather than divergent male and female values. We suggest that these results can be understood in the context of the different lifetime experiences of males and females, which may produce increased experience-dependent cortical plasticity in capuchins compared to rodents, and in humans compared to capuchins.

Sex differences in white matter tracts of capuchin monkey brains

“…and thus these results complement our previous work showing sex differences in gray matter volume of both ancestral limbic circuitry and higher-order visual regions in the same sample of tufted capuchin monkeys (Hecht et al, 2021). Paralleling that earlier, gray matter morphometry study, we found nonoverlapping values in males and females.…”

“…Moreover, studies that have investigated nonhuman primate FA have found results relating to the corpus callosum, but not sex differences (Hopkins et al, 2016;Phillips et al, 2013;Phillips & Hopkins, 2012). Here, we expand upon our previous results (Hecht et al, 2021) by determining whether we also see sex differences in white matter fractional anisotropy in tufted capuchin monkeys using tract-based spatial statistics analysis, a method for voxelwise statistical analysis of FA images incorporating whole-brain multiple comparisons correction (Smith et al, 2006). Based on our previous study, we hypothesized that there would be sexual dimorphisms in white matter tracts, particularly those associated with social processing.…”

“…In a previous study, we reported sex differences in capuchin monkey gray matter volume. Specifically, we found that males show expansion in a region of the hypothalamus, while females show expansion in the cerebellum, the early visual cortex, and other higher‐order regions across the occipital and temporal cortex (Hecht et al., 2021). Additionally, in the same study, results from diffusion tensor imaging (DTI) connectivity of those regions suggest that sex differences might exist across a network of areas associated with processing social information.…”

“…However, there is variation in this trait across species; female chimpanzees show higher structural T1-weighted MRI signal intensity values in the corpus callosum compared to males, while in capuchins the opposite pattern emerges (Phillips et al, 2009). Our previous analyses of tufted capuchins found sex differences in the gray matter morphometry of a network of regions associated with social processing, and established that these regions are structurally connected by white matter tracts (Hecht et al, 2021). The additional measure of fractional anisotropy would provide a more complete understanding of the underlying characteristics of white matter microstructure that contributes to these sex differences.…”

“…Fractional anisotropy (FA) is a measure of the nonrandomness in the directionality of water diffusion that is influenced by axon myelination and density within the white matter tracts of *Males who are the alpha of their social group and have undergone "secondary puberty" upon gaining alpha male status. Reproduced with permission from Hecht et al (2021).…”