Asymmetry of Cerebral Gray and White Matter and Structural Volumes in Relation to Sex Hormones and Chromosomes

Overview

Journal Front Neurosci

Date 2014 Dec 16

PMID 25505869

Citations 13

Authors

Ivanka Savic

Affiliations

Soon will be listed here.

Abstract

Unlabelled: Whilst many studies show sex differences in cerebral asymmetry, their mechanisms are still unknown. This report describes the potential impact of sex hormones and sex chromosomes by comparing MR data from 39 male and 47 female controls and 33 men with an extra X-chromosome (47,XXY).

Methods: Regional asymmetry in gray and white matter volumes (GMV and WMV) was calculated using voxel based moprhometry (SPM5), by contrasting the unflipped and flipped individual GMV and WMV images. In addition, structural volumes were calculated for the thalamus, caudate, putamen, amygdala, and hippocampus, using the FreeSurfer software. Effects of plasma testosterone and estrogen on the GMV and WMV, as well on the right/left ratios of the subcortical volumes were tested by multi-regression analysis.

Results: All three groups showed a leftward asymmetry in the motor cortex and the planum temporale, and a rightward asymmetry of the middle occipital cortex. Both asymmetries were more pronounced in 46,XY males than 46,XX females and 47,XXY males, and were positively correlated with testosterone levels. There was also a rightward asymmetry of the vermis and leftward GMV asymmetry in the cerebellar hemispheres in all groups. Notably, cerebellar asymmetries were larger in 46,XX females and 47,XXY males, but were not related to sex hormone levels. No asymmetry differences between 46,XX females and 47,XXY males, and no overall effects of brain size were detected.

Conclusion: The asymmetry in the planum temporale area and the occipital cortex seem related to processes associated with testosterone, whereas the observed cerebellar asymmetries suggest a link with X-chromosome escapee genes. Sex differences in cerebral asymmetry are moderated by sex hormones and X-chromosome genes, in a regionally differentiated manner.

Citing Articles

Large-scale analysis of structural brain asymmetries during neurodevelopment: Associations with age and sex in 4265 children and adolescents.

Kurth F, Schijven D, van den Heuvel O, Hoogman M, van Rooij D, Stein D Hum Brain Mapp. 2024; 45(11):e26754.

PMID: 39046031 PMC: 11267452. DOI: 10.1002/hbm.26754.

Causal effects of serum testosterone levels on brain volume: a sex-stratified Mendelian randomization study.

Niu P, Wang X, Xu Y J Endocrinol Invest. 2023; 46(9):1787-1798.

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Age-volume associations in cerebellar lobules by sex and reproductive stage.

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Investigating Sexual Dimorphism of Human White Matter in a Harmonized, Multisite Diffusion Magnetic Resonance Imaging Study.

Seitz J, Cetin-Karayumak S, Lyall A, Pasternak O, Baxi M, Vangel M Cereb Cortex. 2020; 31(1):201-212.

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References

van Abeelen J, Janssens C, Crusio W, Lemmens W . Y-chromosomal effects on discrimination learning and hippocampal asymmetry in mice. Behav Genet. 1989; 19(4):543-9. DOI: 10.1007/BF01066253. View

Coates J, Gurnell M, Rustichini A . Second-to-fourth digit ratio predicts success among high-frequency financial traders. Proc Natl Acad Sci U S A. 2009; 106(2):623-8. PMC: 2626753. DOI: 10.1073/pnas.0810907106. View

Raz N, Gunning-Dixon F, Head D, Rodrigue K, Williamson A, Acker J . Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume. Neurobiol Aging. 2004; 25(3):377-96. DOI: 10.1016/S0197-4580(03)00118-0. View

NETLEY C, Rovet J . Hemispheric lateralization in 47,XXY Klinefelter's syndrome boys. Brain Cogn. 1984; 3(1):10-8. DOI: 10.1016/0278-2626(84)90002-2. View

Hering-Hanit R, Achiron R, Lipitz S, Achiron A . Asymmetry of fetal cerebral hemispheres: in utero ultrasound study. Arch Dis Child Fetal Neonatal Ed. 2001; 85(3):F194-6. PMC: 1721319. DOI: 10.1136/fn.85.3.f194. View

Savic I, Lindstrom P . PET and MRI show differences in cerebral asymmetry and functional connectivity between homo- and heterosexual subjects. Proc Natl Acad Sci U S A. 2008; 105(27):9403-8. PMC: 2453705. DOI: 10.1073/pnas.0801566105. View

Chi J, Dooling E, Gilles F . Left-right asymmetries of the temporal speech areas of the human fetus. Arch Neurol. 1977; 34(6):346-8. DOI: 10.1001/archneur.1977.00500180040008. View

Herve P, Crivello F, Perchey G, Mazoyer B, Tzourio-Mazoyer N . Handedness and cerebral anatomical asymmetries in young adult males. Neuroimage. 2005; 29(4):1066-79. DOI: 10.1016/j.neuroimage.2005.08.031. View

Hou G, Yang X, Yuan T . Hippocampal asymmetry: differences in structures and functions. Neurochem Res. 2013; 38(3):453-60. DOI: 10.1007/s11064-012-0954-3. View

10.

Manning J, Stewart A, Bundred P, Trivers R . Sex and ethnic differences in 2nd to 4th digit ratio of children. Early Hum Dev. 2004; 80(2):161-8. DOI: 10.1016/j.earlhumdev.2004.06.004. View

11.

Nguyen T, McCracken J, Ducharme S, Botteron K, Mahabir M, Johnson W . Testosterone-related cortical maturation across childhood and adolescence. Cereb Cortex. 2012; 23(6):1424-32. PMC: 3643718. DOI: 10.1093/cercor/bhs125. View

12.

Bear D, Schiff D, Saver J, Greenberg M, Freeman R . Quantitative analysis of cerebral asymmetries. Fronto-occipital correlation, sexual dimorphism and association with handedness. Arch Neurol. 1986; 43(6):598-603. DOI: 10.1001/archneur.1986.00520060060019. View

13.

Hirnstein M, Westerhausen R, Korsnes M, Hugdahl K . Sex differences in language asymmetry are age-dependent and small: a large-scale, consonant-vowel dichotic listening study with behavioral and fMRI data. Cortex. 2012; 49(7):1910-21. DOI: 10.1016/j.cortex.2012.08.002. View

14.

Carson D, Okuno A, Lee P, Stetten G, Didolkar S, Migeon C . Amniotic fluid steroid levels. Fetuses with adrenal hyperplasia, 46,XXY fetuses, and normal fetuses. Am J Dis Child. 1982; 136(3):218-22. View

15.

Aydin K, Ciftci K, Terzibasioglu E, Ozkan M, Demirtas A, Sencer S . Quantitative proton MR spectroscopic findings of cortical reorganization in the auditory cortex of musicians. AJNR Am J Neuroradiol. 2005; 26(1):128-36. PMC: 7975031. View

16.

Sun T, Patoine C, Abu-Khalil A, Visvader J, Sum E, Cherry T . Early asymmetry of gene transcription in embryonic human left and right cerebral cortex. Science. 2005; 308(5729):1794-8. PMC: 2756725. DOI: 10.1126/science.1110324. View

17.

Kim J, Chae J, Ko H, Latchoumane C, Banerjee A, Mandell D . Hemispheric asymmetry in non-linear interdependence of EEG in post-traumatic stress disorder. Psychiatry Clin Neurosci. 2012; 66(2):87-96. DOI: 10.1111/j.1440-1819.2011.02300.x. View

18.

Ellis R, Bruijn B, Norton A, Winner E, Schlaug G . Training-mediated leftward asymmetries during music processing: a cross-sectional and longitudinal fMRI analysis. Neuroimage. 2013; 75:97-107. PMC: 3705762. DOI: 10.1016/j.neuroimage.2013.02.045. View

19.

Ragbetli M, Aydinlioglu A, Kaplan S . Sex differences and right-left asymmetries in rat hippocampal components. Int J Neurosci. 2002; 112(1):81-95. DOI: 10.1080/00207450212016. View

20.

Guerguerian R, Lewine R . Brain torque and sex differences in schizophrenia. Schizophr Res. 1998; 30(2):175-81. DOI: 10.1016/s0920-9964(97)00144-8. View