Sex differences in adolescent white matter architecture

Bava, Sunita; Boucquey, Veronique; Goldenberg, Diane; Thayer, Rachel E.; Ward, Megan; Jacobus, Joanna; Tapert, Susan F.

doi:10.1016/j.brainres.2010.12.051

Cited by 139 publications

(105 citation statements)

References 62 publications

(77 reference statements)

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“…They are also consistent with activation studies using functional MRI, which have reported greater interhemispheric activation in females on a language task, in which they excelled (44), and greater focal intrahemispheric activation in males on a spatial task, in which they excelled (45). With respect to development, DTI studies (23,24) have shown higher FA and lower MD in the CC in females during midadolescence, confirming a similar trend in our data. Although FA and MD provide measures of WM integrity, connectomic studies like ours are required to complete the picture of connection-wise systems.…”

Section: Discussionsupporting

confidence: 92%

“…Examination of DTI-based scalar measures (16) of fractional anisotropy (FA) and mean diffusivity (MD) has demonstrated diverse outcomes that include increased FA and decreased MD in males in major WM regions (17)(18)(19), higher CC-specific FA in females (20,21), and lower axial and radial diffusivity measures (22) in males. Throughout the developmental period, females displayed higher FA and lower MD in the midadolescent age (12-14 y) (23), and this result was established on a larger sample size (114 subjects) as well (24). On the other hand, sex differences on the entire age range (childhood to old age) demonstrated higher FA and lower MD in males (19,25,26).…”

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confidence: 76%

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Sex differences in the structural connectome of the human brain

Ingalhalikar

Smith

Parker

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

956

608

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Sex differences in human behavior show adaptive complementarity: Males have better motor and spatial abilities, whereas females have superior memory and social cognition skills. Studies also show sex differences in human brains but do not explain this complementarity. In this work, we modeled the structural connectome using diffusion tensor imaging in a sample of 949 youths (aged 8-22 y, 428 males and 521 females) and discovered unique sex differences in brain connectivity during the course of development. Connection-wise statistical analysis, as well as analysis of regional and global network measures, presented a comprehensive description of network characteristics. In all supratentorial regions, males had greater within-hemispheric connectivity, as well as enhanced modularity and transitivity, whereas between-hemispheric connectivity and cross-module participation predominated in females. However, this effect was reversed in the cerebellar connections. Analysis of these changes developmentally demonstrated differences in trajectory between males and females mainly in adolescence and in adulthood. Overall, the results suggest that male brains are structured to facilitate connectivity between perception and coordinated action, whereas female brains are designed to facilitate communication between analytical and intuitive processing modes. diffusion imaging | gender differences S ex differences are of enduring scientific and societal interest because of their prominence in the behavior of humans and nonhuman species (1). Behavioral differences may stem from complementary roles in procreation and social structure; examples include enhanced motor and spatial skills and greater proclivity for physical aggression in males and enhanced verbally mediated memory and social cognition in females (2, 3). With the advent of neuroimaging, multiple studies have found sex differences in the brain (4) that could underlie the behavioral differences. Males have larger crania, proportionate to their larger body size, and a higher percentage of white matter (WM), which contains myelinated axonal fibers, and cerebrospinal fluid (5), whereas women demonstrate a higher percentage of gray matter after correcting for intracranial volume effect (6). Sex differences in the relative size and shape of specific brain structures have also been reported (7), including the hippocampus, amygdala (8, 9), and corpus callosum (CC) (10). Furthermore, developmental differences in tissue growth suggest that there is an anatomical sex difference during maturation (11,12), although links to observed behavioral differences have not been established.Recent studies have used diffusion tensor imaging (DTI) to characterize WM architecture and underlying fiber tracts by exploiting the anisotropic water diffusion in WM (13-15). Examination of DTI-based scalar measures (16) of fractional anisotropy (FA) and mean diffusivity (MD) has demonstrated diverse outcomes that include increased FA and decreased MD in males in major WM regions (17-19), higher CC-specific...

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Section: Discussionsupporting

confidence: 92%

mentioning

confidence: 76%

Sex differences in the structural connectome of the human brain

Ingalhalikar

Smith

Parker

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

956

608

View full text Add to dashboard Cite

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“…Animal studies have also demonstrated that sex steroids affect myelination by acting on glial cells (Garcia-Segura and Melcangi, 2006). In humans, white matter sexual dimorphisms also become more prominent during puberty and adolescence: in boys, white matter microstructure increases more steeply than in girls (Bava et al, 2011), possibly under the influence of pubertal hormones. Recent human evidence indicates that the pubertal reorganization of white matter pathways is associated with increased levels of pubertal sex steroid hormones (Herting et al, 2012).…”

Section: Review Of Lombardo Et Almentioning

confidence: 99%

Sex Steroids and the Organization of the Human Brain

Peper

Koolschijn²

2012

J. Neurosci.

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Review of Lombardo et al.Studying the biological mechanisms underlying sexual differentiation in the human brain provides important insights into the etiology and trajectory of neurodevelopmental disorders in males and females (Baron-Cohen et al., 2011). Sex steroid hormones, the end products of the hypothalamus-pituitary-gonadal axis, exert powerful effects on the organization and sexual differentiation of brain structures. From animal studies, it has become clear that during early development, exposure of the brain to testosterone and estradiol leads to irreversible changes in the nervous system (McCarthy et al., 2012). Moreover, fetal exposure to sex steroids has a major impact on the sexual differentiation of the brain (McCarthy et al., 2012). For example, high levels of fetal testosterone (FT) result in brain masculinization in experimental animals, such as enlargements of the volume and soma size of the suprachiasmatic nucleus, bed nucleus of the stria terminalis, and ventromedial hypothalamus (Zuloaga et al., 2008).In humans, studies of the effects of FT often rely on indirect measures such as the ratio between the index finger (2D) and ring finger (4D) or on opposite-sex twin studies. Specifically, a smaller 2D:4D ratio correlates with higher FT exposure, and through the intrauterine presence of a male fetus, opposite-sex twin girls are exposed to higher FT levels than same-sex twin girls. Using the latter indirect measure of FT, earlier reports showed that total brain volume and cerebellum volume, typically found to be larger in males, were positively correlated with higher FT exposure (Peper et al., 2009).A recent paper by Lombardo et al. (2012) provided direct evidence for an association between FT levels and sexual differentiation of brain gray matter in humans. In this pioneering study of 28 developing boys, FT levels were determined from amniotic fluid. Amniocentesis was performed between 13 and 20 weeks of gestation, which is a critical period of brain masculinization. When these boys were 8 -11 years old, a structural MRI was made. Using voxel-based morphometry, gray matter regions within the whole brain of these 28 boys were identified showing significant correlations with FT levels. The amygdala and hypothalamus were included as a priori regions of interest. Then, in a second normative sample of 217 (101 boys) children (NIH Pediatric MRI Data Repository), sexual dimorphisms in gray matter were determined. Finally, a conjunction analysis was performed to isolate brain regions whose direction of the FT correlation was congruent with the direction of sexual dimorphism. Lombardo et al. (2012) hypothesized that the size of brain areas that were normally larger in males than in females would correlate positively with FT, whereas the size of brain areas that are normally larger in females would correlate negatively with FT. Results showed that higher levels of FT were associated with larger right temporal/parietal junction and posterior superior temporal sulcus. As predicted, these brain areas were la...

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“…Some of these variations include thicker cortices in the right inferior parietal and posterior temporal regions in women, which are present from childhood and are maintained throughout life 10 ; different intrahemispheric or interhemispheric cerebral metabolic rates for glucose 11 ; and differences in WM architecture as inferred from diffusion properties of the brain tissue. 12 The effect of sexual dimorphism in TLE associated with HS has also been stressed for variable seizure semiology in many studies. Ictal fear, 13 vocalization, 14 vegetative signs, 15 and sexual auras 16 occur more frequently in women than in men.…”

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confidence: 99%