Elsevier

NeuroImage

Volume 18, Issue 4, April 2003, Pages 880-894
NeuroImage

Regular article
Sexual dimorphism and asymmetries in the gray–white composition of the human cerebrum

https://doi.org/10.1016/S1053-8119(03)00034-XGet rights and content

Abstract

Using high resolution MRI scans and automated tissue segmentation, gray and white matter (GM, WM) volumes of the frontal, temporal, parietal, and occipital lobes, cingulate gyrus, and insula were calculated. Subjects included 23 male and 23 female healthy, right-handed subjects. For all structures, male volumes were greater than female, but the gray/white (G/W) ratio was consistently higher across structures in women than men. Sexual dimorphism was greater for WM than GM: most of the G/W ratio sex differences can be attributed to variation in WM volume. The corpus callosum, although larger in men, is less sexually dimorphic than the WM as a whole. Several regions demonstrate pair-wise asymmetries in G/W ratio and WM volume. Both the cingulate gyrus and insula exhibit strong asymmetries. The left cingulate gyrus is significantly larger than the right, and the G/W ratio of the left insula is significantly greater than that of the right. Although statistically significant sex differences and asymmetries are present at this level of analysis, we argue that researchers should be wary of ascribing cognitive functional significance to these patterns at this time. This is not to say, however, that these patterns are not important for understanding the natural history of the human brain, and its evolution and development.

Introduction

Across mammal species, the relative composition of gray and white matter (GM and WM) in the (neo)cortex is remarkably uniform (Zhang and Sejnowski, 2000). Humans conform to the general mammalian trend. However, volumetric magnetic resonance imaging (MRI) studies indicate that GM and WM composition varies with sex, age, and health status. In children, GM growth outpaces WM growth during the first 2 years of life (approximately), but thereafter, WM growth predominates (although GM growth also continues into adolescence) Courchesne et al 2000, Matsuzawa et al 2001, Paus et al 2001. After the age of 50, WM volume typically decreases more quickly than GM volume; thus the GM—WM ratio increases slightly with advanced age Miller et al 1980, Jernigan et al 2001. Abnormal changes in GM and WM composition have been reported in several diseases, such as schizophrenia Gur et al 2000, Mathalon et al 2001 and bipolar illness (Brambilla et al., 2001). In Alzheimer’s disease, prefrontal GM and WM decline at a similar rate, while in normal aging, WM reduction is typically more pronounced than GM reduction (Salat et al., 1999).

Sex differences have been reported for the GM–WM composition of the cerebrum. Earlier studies with relatively small numbers of subjects indicated that sexual dimorphism is greater for WM than GM, because significant differences in WM but not GM volumes were found Filipek et al 1994, Passe et al 1997. This has been confirmed by larger studies, which have shown that while both GM and WM volumes are smaller in women than men, the WM difference is more pronounced, with the result that women have a higher overall proportion of GM than men Peters et al 1998, Gur et al 1999. Sexual dimorphism in the GM composition of some anatomical subregions (dorsolaeral prefronal cortex and superior temporal gyrus; Schlaepfer et al., 1995) and for several gyri (Goldstein et al., 2001) has also been reported. In terms of sex differences in the overall GM–WM composition of the human cerebrum, a basic issue emerges: should the fact that women have a higher percentage of GM than men be interpreted as women having “more” GM or “less” WM? Gur and colleagues (1999) argue that the higher relative GM composition of women’s brains may compensate for smaller cranial capacity, by devoting more of that space to “computation” rather than “information transfer.”

To date, MRI-based studies of normal variation in GM–WM composition have focused on large sectors of the brain (hemisphere or whole) Gur et al 1999, Blatter et al 1995, have been based on brains resized in the process of automated parcellation (Nopoulos et al., 2000), or have used arbitrary criteria to define regions of the brain (Pfefferbaum et al., 1994) or slice-wise sampling strategies (Raz et al., 1997). In this paper, we address sexual dimorphism and lateral asymmetry in the GM–WM volumes of the major lobes and selected gyri of the human cerebrum (frontal, parietal, temporal, and occipital lobes, and the cingulate gyrus, and insula), in a sample of 46 healthy, right-handed adults. Parcellation of the brain was based on strict neuroanatomical criteria, and regions of interest were manually traced on each slice of high resolution MRI-scans. Our results provide an anatomically robust account of sexual dimorphism and asymmetry in GM and WM composition in the major anatomical subregions of the cerebrum.

Section snippets

Subjects

Subjects were 23 men (mean age = 32.1 years, SD = 8.8, range 22–49) and 23 women (mean age = 32.6 years, SD = 7.5, range 23–47) of European descent. All were right-handed (scores on the Oldfield-Geschwind Handedness Inventory: men, mean = +92, SD = 12.9; women, mean = +94, SD = 6.6) with no left-handedness in first-degree relatives, healthy, and with no history of neurological or psychiatric illness. All gave informed consent in accordance with institutional and federal rules. Subjects (sex and

Results

The GM and WM volume measures of the hemispheres, and frontal, temporal, parietal, and occipital lobes, and the cingulate gyrus and insula, for all subjects, are presented in Appendices 1–4.

Table 1 presents the GM and WM volumes and GM–WM ratio (G/W ratio) by sex and hemisphere for all brain regions measured. For nearly every structure, male GM, WM, and total volumes are significantly larger than female volumes. Exceptions include the gray and total volumes of the left occipital lobe, the gray

Discussion

The results from this study provide some important refinements of our view of volumetric sexual dimorphism and GM–WM asymmetries in the human brain. Like virtually every other previous MRI study, we found that male volumes were greater than female for most cerebral structures, ranging from the hemisphere to the insula. However, our segmentation and parcellation results indicate that sexual dimorphism in the cerebrum is not uniformly distributed across tissue types or regions.

Conclusion

This study provides normative data on sexual dimorphism and asymmetries in the GM and WM composition of the human brain. It demonstrates that the global parcellation of the cerebrum based on anatomical criteria yields patterns of GM and WM distribution that must be accounted for when looking at more localized distributions of these tissues. It also clearly demonstrates that the use of resized brains in MRI volumetric studies is likely to result in a substantial loss of measured variation

Acknowledgements

This research was supported by Program Project Grant NINDS NS 19632 and the Mathers Foundation. We thank J. Cole, K. Jones, and J. Spradling for technical assistance and support. Thanks to C. Kice Brown for help with statistical analysis.Appendix 1, Appendix 2, Appendix 3, Appendix 4

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