Sex differences in gray and white matter structure in age-matched unrelated males and females and opposite-sex siblings

International Journal of Psychological Research

Volumn 6, Issue SPEC. ISSUE, 2013, Pages 7-21

  Den Braber, Anouk ^a   Van't Ent, Dennis ^a   Stoffers, Diederick ^b   Linkenkaer Hansen, Klaus ^a   Boomsma, Dorret I ^a   De Geus, Eco J C ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

Diffusion tensor imaging; Fractional anisotropy; Opposite sex twins; Sex differences; Structural magnetic resonance imaging; Voxel based morphometry

Indexed keywords

EID: 84894142173     PISSN: 20112084     EISSN: 20117922     Source Type: Journal    
DOI: 10.21500/20112084.712     Document Type: Article

References (81)

1. Abe, O., Yamasue, H., Yamada, H., Masutani, Y., Kabasawa, H., Sasaki, H., ... Ohtomo, K. (2010). Sex dimorphism in gray/white matter volume and diffusion tensor during normal aging. NMR in Biomedicine, 23, 446-458.
2. Abel, K. M., Drake, R., Goldstein, J. M. (2010). Sex differences in schizophrenia. International Review of Psychiatry, 22, 417-428.
3. Alexander, G. E., DeLong, M. R., & Strick, P. L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience, 9, 357-381.
4. Allen, J. S., Damasio, H., Grabowski, T. J., Bruss, J., & Zhang, W. (2003). Sexual dimorphism and asymmetries in the gray-white composition of the human cerebrum. Neuroimage, 18, 880-894.
5. Altemus, M. (2006). Sex differences in depression and anxiety disorders: potential biological determinants. Hormones and Behavior, 50, 534-538.
6. Assaf, Y., & Pasternak, O. (2008). Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. Journal of Molecular Neuroscience, 34, 51-61.
7. Bao A. M., & Swaab, D. F. (2010). Sex differences in the brain, behavior, and neuropsychiatric disorders. Neuroscientist, 16, 550-565.
8. Basser, P. J., & Pierpaoli, C. (1996). Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. Journal of Magnetic Resonance - Series B, 111(3), 209-219.
9. Beaulieu, C. (2002). The basis of anisotropic water diffusion in the nervous system - a technical review. NMR in Biomedicine, 15, 435-455.
10. Bekker, M. H., van Mens-Verhulst, J. (2007). Anxiety disorders: sex differences in prevalence, degree, and background, but gender-neutral treatment. Gender Medicine, 4(Suppl. B), S178-S193.
11. Bishop, K. M., & Wahlsten, D. (1997). Sex differences in the human corpus callosum: myth or reality? Neuroscience and Biobehavioral Reviews, 21, 581-601.
12. Brunetti, M., Babiloni, C., Ferretti, A., Del, G. C., Merla, A., Olivetti, B. M., & Romani, G. L. (2008). Hypothalamus, sexual arousal and psychosexual identity in human males: a functional magnetic resonance imaging study. European Journal of Neuroscience, 27, 2922-2927.
13. Burgaleta, M., Head, K., Alvarez-Linera, J., Martinez, K., Escorial, S., Haier, R., and Colom, R. (2012). Sex differences in brain volume are related to specific skills, not to general intelligence. Intelligence, 40(1), 60-68.
14. Buss, C., Lord, C., Wadiwalla, M., Hellhammer, D. H., Lupien, S. J., Meaney, M. J., & Pruessner, J. C. (2007). Maternal care modulates the relationship between prenatal risk and hippocampal volume in women but not in men. The Journal of Neuroscience, 27, 2592-2595.
15. Chou, K. H., Cheng, Y., Chen, I. Y., Lin, C. P., & Chu, W. C. (2011). Sex-linked white matter microstructure of the social and analytic brain. Neuroimage, 54, 725-733.
16. Cosgrove, K. P., Mazure, C. M., Staley, J. K. (2007). Evolving knowledge of sex differences in brain structure, function, and chemistry. Biological Psychiatry, 62, 847-855.
17. Critchley, H. D., Wiens, S., Rotshtein, P., Ohman, A., & Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7, 189-195.
18. de Courten-Myers, G. M. (1999). The human cerebral cortex: gender differences in structure and function. Journal of Neuropathology and Experimental Neurology, 58, 217-226.
19. den Braber, A., Bohlken, M. M., Brouwer, R. M., van 't Ent, D., Kanai, R., Kahn, R. S., ... Boomsma, D. I. (2013). Heritability of subcortical brain measures: A perspective for future genome-wide association studies. Neuroimage, 83, 98-102.
20. den Braber A, van 't Ent, D., Cath, D. C., Wagner, J., Boomsma, D. I., & de Geus, E. J. (2010). Brain activation during cognitive planning in twins discordant or concordant for obsessive-compulsive symptoms. Brain, 133, 3123-3140.
21. Eagly, A. H., & Wood, W. (1999). The origins of sex differences in human behavior - Evolved dispositions versus social roles. American Psychologist, 54, 408-423.
22. Giedd, J. N., Castellanos, F. X., Rajapakse, J. C., Vaituzis, A. C., Rapoport, J. L. (1997). Sexual dimorphism of the developing human brain. Progress in Neuro-psychopharmacology and Biological Psychiatry, 21, 1185-1201.
23. Giedd J. N., Raznahan, A., Mills, K. L., Lenroot, R. K. (2012). Review: magnetic resonance imaging of male/female differences in human adolescent brain anatomy. Biology of Sex Differences, 3, 1-9.
24. Goldstein, J, M., Seidman, L. J., Horton, N. J., Makris, N., Kennedy, D. N., Caviness, V. S, Jr., ... Tsuang, M. T. (2001). Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cerebral Cortex, 11, 490-497.
25. Good, C. D., Johnsrude, I., Ashburner, J., Henson, R. N., Friston, K. J., Frackowiak, R. S. (2001). Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains. Neuroimage, 14, 685-700.
26. Gur, R. C., Gunning-Dixon, F., Bilker, W. B., & Gur, R. E. (2002). Sex differences in temporo-limbic and frontal brain volumes of healthy adults. Cerebral Cortex, 12, 998-1003.
27. Gur, R. C., Turetsky, B. I., Matsui, M., Yan, M., Bilker, W., Hughett, P., & Gur, R. E. (1999). Sex differences in brain gray and white matter in healthy young adults: correlations with cognitive performance. The Journal of Neuroscience, 19, 4065-4072.
28. Haber, S. N. (2003). The primate basal ganglia: parallel and integrative networks. Journal of Chemical Neuroanatomy, 26, 317-330.
29. Halpern, D. F., (1997). Sex differences in intelligence. Implications for education. American Psychologist, 52, 1091-1102.
30. Hsu, J. L., Leemans, A., Bai, C. H., Lee, C. H., Tsai, Y. F., Chiu, H. C., & Chen, W. H. (2008). Gender differences and age-related white matter changes of the human brain: a diffusion tensor imaging study. Neuroimage, 39, 566-577.
31. Hsu, J. L., Van, H. W., Bai, C. H., Lee, C. H., Tsai, Y. F., Chiu, H. C., ... Leemans, A. (2010). Microstructural white matter changes in normal aging: a diffusion tensor imaging study with higher-order polynomial regression models. Neuroimage, 49, 32-43.
32. Im, K., Lee, J. M., Lee, J., Shin, Y. W., Kim, I. Y., Kwon, J. S., & Kim, S. I. (2006). Gender difference analysis of cortical thickness in healthy young adults with surface-based methods. Neuroimage, 31, 31-38.
33. Inano, S., Takao, H., Hayashi, N., Abe, O., & Ohtomo, K. (2011). Effects of age and gender on white matter integrity. American Journal of Neuroradiology, 32, 2103-2109.
34. Kang, X., Herron, T. J., Woods, D. L. (2011). Regional variation, hemispheric asymmetries and gender differences in pericortical white matter. Neuroimage, 56, 2011-2023.
35. Kochunov, P., Glahn, D. C., Lancaster, J., Thompson, P. M., Kochunov, V., Rogers, B., ... Williamson, D. E. (2011a). Fractional anisotropy of cerebral white matter and thickness of cortical gray matter across the lifespan. Neuroimage, 58,:41-49.
36. Kochunov, P., Glahn, D. C., Nichols, T. E., Winkler, A. M., Hong, E. L., Holcomb, H. H., ... Blangero, J. (2011b). Genetic analysis of cortical thickness and fractional anisotropy of water diffusion in the brain. Frontiers in Neuroscience, 5, 120.
37. Kochunov, P., Williamson, D. E., Lancaster, J., Fox, P., Cornell, J., Blangero, J., & Glahn, D. C. (2012). Fractional anisotropy of water diffusion in cerebral white matter across the lifespan. Neurobiology of Aging, 33, 9-20.
38. Lacoste-Utamsing, C., & Holloway R. L. (1982). Sexual dimorphism in the human corpus callosum. Science 216(4553), 1431-1432.
39. Le Bihan, D., Mangin, J. F., Poupon, C., Clark, C. A., Pappata, S., Molko, N., & Chabriat, H. (2001). Diffusion tensor imaging: concepts and applications. Journal of Magnetic Resonance Imaging, 13, 534-546.
40. Lenroot, R. K., & Giedd, J. N. (2010). Sex differences in the adolescent brain. Brain and Cognition, 72, 46-55.
41. Lentini, E., Kasahara, M., Arver, S., & Savic, I. (2013). Sex differences in the human brain and the impact of sex chromosomes and sex hormones. Cerebral Cortex, 23, 2322-2336.
42. Loring-Meier, S., Halpern, D. F., (1999). Sex differences in visuospatial working memory: components of cognitive processing. Psychonomic Bulletin and Review, 6, 464-471.
43. Luders, E., Narr, K. L., Thompson, P. M., Rex, D. E., Woods, R. P., Deluca, H., ... Toga, A. W. (2006). Gender effects on cortical thickness and the influence of scaling. Human Brain Mapping, 27, 314-324.
44. Lv, B., Li, J., He, H., Li, M., Zhao, M., Ai, L., ... Wang, Z. (2010). Gender consistency and difference in healthy adults revealed by cortical thickness. Neuroimage, 53, 373-382.
45. Mann, V. A., Sasanuma, S., Sakuma, N., Masaki, S., (1990). Sex differences in cognitive abilities: a cross-cultural perspective. Neuropsychologia, 28, 1063-1077.
46. Martin, E. I., Ressler, K. J., Binder, E., & Nemeroff, C. B. (2009). The neurobiology of anxiety disorders: brain imaging, genetics, and psychoneuroendocrinology. Psychiatric Clinics of North America, 32, 549-575.
47. McCarthy, M. M., & Arnold, A. P. (2011). Reframing sexual differentiation of the brain. Nature Neuroscience, 14, 677-683.
48. Menzler, K., Belke, M., Wehrmann, E., Krakow, K., Lengler, U., Jansen, A., ... Knake, S. (2011). Men and women are different: diffusion tensor imaging reveals sexual dimorphism in the microstructure of the thalamus, corpus callosum and cingulum. Neuroimage, 54, 2557-2562.
49. Mori, S., & Zhang, J. (2006). Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron, 51, 527-539.
50. Palazidou, E. (2012). The neurobiology of depression. British Medical Bulletin, 101, 127-145.
51. Parker, G., Brotchie, H. (2010). Gender differences in depression. International Review of Psychiatry, 22, 429-436.
52. Paus, T. (2013). How environment and genes shape the adolescent brain. Hormones and Behavior, 64, 195-202.
53. Peper, J. S., Brouwer, R. M., Schnack, H. G., van Baal, G. C., van Leeuwen, M., van den Berg, ... Hulshoff Pol, H. E. (2009a). Sex steroids and brain structure in pubertal boys and girls. Psychoneuroendocrinology, 34, 332-342.
54. Peper, J. S., Brouwer, R. M., van Baal, G. C., Schnack, H. G., van Leeuwen, M., Boomsma, D. I., ... Hulshoff Pol, H. E. (2009b). Does having a twin brother make for a bigger brain? European Journal of Endocrinology, 160, 739-746.
55. Pollatos, O., Gramann, K., & Schandry, R. (2007). Neural systems connecting interoceptive awareness and feelings. Human Brain Mapping, 28, 9-18.
56. Rao, H., Betancourt, L., Giannetta, J. M., Brodsky, N. L., Korczykowski, M., Avants, B. B., ... Farah, M. J. (2010). Early parental care is important for hippocampal maturation: evidence from brain morphology in humans. Neuroimage, 49, 1144-1150.
57. Raz, N., Gunning-Dixon, F., Head, D., Williamson, A., & Acker, J. D. (2001). Age and sex differences in the cerebellum and the ventral pons: a prospective MR study of healthy adults. American Journal of Neuroradiology, 22, 1161-1167.
58. Rhyu, I. J., Cho, T. H., Lee, N. J., Uhm, C. S., Kim, H., & Suh, Y. S. (1999). Magnetic resonance image-based cerebellar volumetry in healthy Korean adults. Neuroscience Letters, 270, 149-152.
59. Rucklidge, J. J. (2010). Gender differences in attention-deficit/ hyperactivity disorder. Psychiatric Clinics of North America, 33, 357-373.
60. Schmithorst, V. J., Holland, S. K., & Dardzinski, B. J. (2008). Developmental differences in white matter architecture between boys and girls. Human Brain Mapping, 29, 696-710.
61. Shenton, M, E., Dickey, C. C., Frumin, M., & McCarley, R. W. (2001). A review of MRI findings in schizophrenia. Schizophrenia Research, 49, 1-52.
62. Shin, Y. W., Kim, D. J., Ha, T. H., Park, H. J., Moon, W. J., Chung, ... Kwon, J. S. (2005). Sex differences in the human corpus callosum: diffusion tensor imaging study. Neuroreport, 16, 795-798.
63. Singer, H. S., & Minzer, K. (2003). Neurobiology of Tourette's syndrome: concepts of neuroanatomic localization and neurochemical abnormalities. Brain and Development, 25(Suppl. 1), S70-S84.
64. Singer, H. S., & Walkup, J. T. (1991). Tourette syndrome and other tic disorders. Diagnosis, pathophysiology, and treatment. Medicine, 70(1), 15-32.
65. Sisk, C. L., & Zehr, J. L. (2005). Pubertal hormones organize the adolescent brain and behavior. Frontiers in Neuroendocrinology, 26, 163-174.
66. Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., ... Behrens, T. E. (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage, 31, 1487-1505.
67. Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, ... Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage, 23 (Suppl. 1), S208-S219.
68. Song, S. K., Sun, S. W., Ju, W. K., Lin, S. J., Cross, A. H., & Neufeld, A. H. (2003). Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage, 20, 1714-1722.
69. Song, S. K., Sun, S. W., Ramsbottom, M. J., Chang, C., Russell, J., & Cross, A. H. (2002). Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage, 17, 1429-1436.
70. Song, S. K., Yoshino, J., Le, T. Q., Lin, S. J., Sun, S. W., Cross, A. H., & Armstrong, R. C. (2005). Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage, 26, 132-140.
71. Sowell, E. R, Peterson, B. S., Kan, E., Woods, R. P., Yoshii, J., Bansal, R., ... Toga, A. W. (2007). Sex differences in cortical thickness mapped in 176 healthy individuals between 7 and 87 years of age. Cerebral Cortex, 17, 1550-1560.
72. Sullivan, E. V., Rosenbloom, M. J., Desmond, J. E., Pfefferbaum, A. (2001). Sex differences in corpus callosum size: relationship to age and intracranial size. Neurobiology of Aging, 22, 603-611.
73. Swaab, D. F., Chung, W. C., Kruijver, F. P., Hofman, M. A., & Ishunina, T. A. (2002). Sexual differentiation of the human hypothalamus. Advances in Experimental Medicine and Biology, 511, 75-100.
74. Szeszko, P. R., Vogel, J., Ashtari, M., Malhotra, A. K, Bates, J., Kane, J. M., ... Lim, K. (2003). Sex differences in frontal lobe white matter microstructure: a DTI study. Neuroreport, 14, 2469-2473.
75. Thompson, P. M., Cannon, T. D., Narr, K. L., van Erp, T. G., Poutanen, V. P., Huttunen, M., ... Toga, A. W. (2001). Genetic influences on brain structure. Nature Neuroscience, 4, 1253-1258.
76. Tiemeier, H., Lenroot, R. K., Greenstein, D. K., Tran, L., Pierson, R., & Giedd, J. N. (2010). Cerebellum development during childhood and adolescence: a longitudinal morphometric MRI study. Neuroimage, 49, 63-70.
77. Toga, A. W., & Thompson, P. M. (2005). Genetics of brain structure and intelligence. Annual Review of Neuroscience, 28, 1-23.
78. Wakana, S., Jiang, H., Nagae-Poetscher, L. M., van Zijl, P. C., & Mori, S. (2004). Fiber tract-based atlas of human white matter anatomy. Radiology, 230, 77-87.
79. Wang, S. S. (2008). Functional tradeoffs in axonal scaling: implications for brain function. Brain, Behavior and Evolution, 72, 159-167.
80. Wicker, B., Keysers, C., Plailly, J., Royet, J. P., Gallese, V., & Rizzolatti, G. (2003). Both of us disgusted in My insula: the common neural basis of seeing and feeling disgust. Neuron, 40, 655-664.
81. Yeo, R. A., Martinez, D., Pommy, J., Ehrlich, S., Schulz, S. C., Ho, B. C., ... Calhoun, V. D. (2013). The impact of parent socio-economic status on executive functioning and cortical morphology in individuals with schizophrenia and healthy controls. Psychological Medicine, 1-9.