Male brain ages faster: the age and gender dependence of subcortical volumes

Abstract

Effects of gender on grey matter (GM) volume differences in subcortical structures of the human brain have consistently been reported. Recent research evidence suggests that both gender and brain size influences volume distribution in subcortical areas independently. The goal of this study was to determine the effects of the interplay between brain size, gender and age contributing to volume differences of subcortical GM in the human brain. High-resolution T1-weighted images were acquired from 53 healthy males and 50 age-matched healthy females. Total GM volume was determined using voxel-based morphometry. We used model-based subcortical segmentation analysis to measure the volume of subcortical nuclei. Main effects of gender, brain volume and aging on subcortical structures were examined using multivariate analysis of variance. No significant difference was found in total brain volume between the two genders after correcting for total intracranial volume. Our analysis revealed significantly larger hippocampus volume for females. Additionally, GM volumes of the caudate nucleus, putamen and thalamus displayed a significant age-related decrease in males as compared to females. In contrast to this only the thalamic volume loss proved significant for females. Strikingly, GM volume decreases faster in males than in females emphasizing the interplay between aging and gender on subcortical structures. These findings might have important implications for the interpretation of the effects of unalterable factors (i.e. gender and age) in cross-sectional structural MRI studies. Furthermore, the volume distribution and changes of subcortical structures have been consistently related to several neuropsychiatric disorders (e.g. Parkinson’s disease, attention deficit hyperactivity disorder, etc.). Understanding these changes might yield further insight in the course and prognosis of these disorders.

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References

  1. Abedelahi, A., Hasanzadeh, H., Hadizadeh, H., & Joghataie, M. T. (2013). Morphometric and volumetric study of caudate and putamen nuclei in normal individuals by MRI: Effect of normal aging, gender and hemispheric differences. Pol J Radiol, 78(3), 7–14. doi:10.12659/PJR.889364.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Ahsan, R. L., Allom, R., Gousias, I. S., Habib, H., Turkheimer, F. E., Free, S., et al. (2007). Volumes, spatial extents and a probabilistic atlas of the human basal ganglia and thalamus. NeuroImage, 38(2), 261–270. doi:10.1016/j.neuroimage.2007.06.004.

    Article  PubMed  Google Scholar 

  3. Andersson, J. L. R., Jenkinson, M., & Smith, S. (2007). Non-linear optimisation. FMRIB technical report. Oxford.

  4. Ashburner, J., & Friston, K. J. (2000). Voxel-based morphometry–the methods. NeuroImage, 11(6 Pt 1), 805–821. doi:10.1006/nimg.2000.0582.

    CAS  Article  PubMed  Google Scholar 

  5. Barnes, J., Ridgway, G. R., Bartlett, J., Henley, S. M., Lehmann, M., Hobbs, N., et al. (2010). Head size, age and gender adjustment in MRI studies: a necessary nuisance? NeuroImage, 53(4), 1244–1255. doi:10.1016/j.neuroimage.2010.06.025.

    Article  PubMed  Google Scholar 

  6. Barron, A. M., & Pike, C. J. (2012). Sex hormones, aging, and alzheimer’s disease. Frontiers in Bioscience (Elite Edition), 4, 976–997.

    Google Scholar 

  7. Bisagno, V., & Cadet, J. L. (2014). Stress, sex, and addiction: potential roles of corticotropin-releasing factor, oxytocin, and arginine-vasopressin. Behavioural Pharmacology, 25(5–6), 445–457. doi:10.1097/FBP.0000000000000049.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Bourque, M., Dluzen, D. E., & Di Paolo, T. (2009). Neuroprotective actions of sex steroids in parkinson’s disease. Frontiers in Neuroendocrinology, 30(2), 142–157. doi:10.1016/j.yfrne.2009.04.014.

    CAS  Article  PubMed  Google Scholar 

  9. Cahill, L. (2003). Sex-related influences on the neurobiology of emotionally influenced memory. Annals of the New York Academy of Sciences, 985, 163–173.

    Article  PubMed  Google Scholar 

  10. Cahill, L. (2006). Why sex matters for neuroscience. Nature Reviews. Neuroscience, 7(6), 477–484. doi:10.1038/nrn1909.

    CAS  Article  PubMed  Google Scholar 

  11. Callaert, D. V., Ribbens, A., Maes, F., Swinnen, S. P., & Wenderoth, N. (2014). Assessing age-related gray matter decline with voxel-based morphometry depends significantly on segmentation and normalization procedures. Frontiers in Aging Neuroscience, 6, 124. doi:10.3389/fnagi.2014.00124.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Cheng, Y., Chou, K. H., Decety, J., Chen, I. Y., Hung, D., Tzeng, O. J., et al. (2009). Sex differences in the neuroanatomy of human mirror-neuron system: a voxel-based morphometric investigation. Neuroscience, 158(2), 713–720. doi:10.1016/j.neuroscience.2008.10.026.

    CAS  Article  PubMed  Google Scholar 

  13. Cosgrove, K. P., Mazure, C. M., & Staley, J. K. (2007). Evolving knowledge of sex differences in brain structure, function, and chemistry. Biological Psychiatry, 62(8), 847–855. doi:10.1016/j.biopsych.2007.03.001.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Courchesne, E., Chisum, H. J., Townsend, J., Cowles, A., Covington, J., Egaas, B., et al. (2000). Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. Radiology, 216(3), 672–682. doi:10.1148/radiology.216.3.r00au37672.

    CAS  Article  PubMed  Google Scholar 

  15. DeLacoste-Utamsing, C., & Holloway, R. L. (1982). Sexual dimorphism in the human corpus callosum. Science, 216(4553), 1431–1432.

    CAS  Article  PubMed  Google Scholar 

  16. Fattore, L., Melis, M., Fadda, P., & Fratta, W. (2014). Sex differences in addictive disorders. Frontiers in Neuroendocrinology, 35(3), 272–284. doi:10.1016/j.yfrne.2014.04.003.

    Article  PubMed  Google Scholar 

  17. Filipek, P. A., Richelme, C., Kennedy, D. N., & Caviness Jr., V. S. (1994). The young adult human brain: an MRI-based morphometric analysis. Cerebral Cortex, 4(4), 344–360.

    CAS  Article  PubMed  Google Scholar 

  18. Galea, L. A., Leuner, B., & Slattery, D. A. (2014). Hippocampal plasticity during the peripartum period: influence of sex steroids, stress and ageing. Journal of Neuroendocrinology. doi:10.1111/jne.12177.

    PubMed Central  Google Scholar 

  19. Ge, Y., Grossman, R. I., Babb, J. S., Rabin, M. L., Mannon, L. J., & Kolson, D. L. (2002a). Age-related total gray matter and white matter changes in normal adult brain. Part I: volumetric MR imaging analysis. AJNR. American Journal of Neuroradiology, 23(8), 1327–1333.

    PubMed  Google Scholar 

  20. Ge, Y., Grossman, R. I., Babb, J. S., Rabin, M. L., Mannon, L. J., & Kolson, D. L. (2002b). Age-related total gray matter and white matter changes in normal adult brain. Part II: quantitative magnetization transfer ratio histogram analysis. AJNR. American Journal of Neuroradiology, 23(8), 1334–1341.

    PubMed  Google Scholar 

  21. Geevarghese, R., Lumsden, D. E., Hulse, N., Samuel, M., & Ashkan, K. (2015). Subcortical structure volumes and correlation to clinical variables in parkinson’s disease. Journal of Neuroimaging, 25(2), 275–280. doi:10.1111/jon.12095.

    Article  PubMed  Google Scholar 

  22. Gershon, J. (2002). A meta-analytic review of gender differences in ADHD. Journal of Attention Disorders, 5(3), 143–154.

    CAS  Article  PubMed  Google Scholar 

  23. Gifuni, A. J., Ding, Y., Olie, E., Lawrence, N., Cyprien, F., Le Bars, E., et al. (2015). Subcortical nuclei volumes in suicidal behavior: nucleus accumbens may modulate the lethality of acts. Brain Imaging and Behavior. doi:10.1007/s11682-015-9369-5.

    Google Scholar 

  24. Gillies, G. E., Pienaar, I. S., Vohra, S., & Qamhawi, Z. (2014). Sex differences in parkinson’s disease. Frontiers in Neuroendocrinology. doi:10.1016/j.yfrne.2014.02.002.

    PubMed  PubMed Central  Google Scholar 

  25. Goldstein, J. M., Seidman, L. J., Horton, N. J., Makris, N., Kennedy, D. N., Caviness Jr., V. S., et al. (2001). Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cerebral Cortex, 11(6), 490–497.

    CAS  Article  PubMed  Google Scholar 

  26. Good, C. D., Johnsrude, I. S., Ashburner, J., Henson, R. N., Friston, K. J., & Frackowiak, R. S. (2001). A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage, 14(1 Pt 1), 21–36. doi:10.1006/nimg.2001.0786.

    CAS  Article  PubMed  Google Scholar 

  27. Goodro, M., Sameti, M., Patenaude, B., & Fein, G. (2012). Age effect on subcortical structures in healthy adults. Psychiatry Research, 203(1), 38–45. doi:10.1016/j.pscychresns.2011.09.014.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Gray, T. S., & Bingaman, E. W. (1996). The amygdala: corticotropin-releasing factor, steroids, and stress. Critical Reviews in Neurobiology, 10(2), 155–168.

    CAS  Article  PubMed  Google Scholar 

  29. Greer, J. M., & McCombe, P. A. (2011). Role of gender in multiple sclerosis: clinical effects and potential molecular mechanisms. Journal of Neuroimmunology, 234(1–2), 7–18. doi:10.1016/j.jneuroim.2011.03.003.

    CAS  Article  PubMed  Google Scholar 

  30. Guenzel, F. M., Wolf, O. T., & Schwabe, L. (2014). Sex differences in stress effects on response and spatial memory formation. Neurobiology of Learning and Memory, 109, 46–55. doi:10.1016/j.nlm.2013.11.020.

    Article  PubMed  Google Scholar 

  31. Gur, R. C., Mozley, P. D., Resnick, S. M., Gottlieb, G. L., Kohn, M., Zimmerman, R., et al. (1991). Gender differences in age effect on brain atrophy measured by magnetic resonance imaging. Proceedings of the National Academy of Sciences of the United States of America, 88(7), 2845–2849.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Guttmann, C. R., Jolesz, F. A., Kikinis, R., Killiany, R. J., Moss, M. B., Sandor, T., et al. (1998). White matter changes with normal aging. Neurology, 50(4), 972–978.

    CAS  Article  PubMed  Google Scholar 

  33. Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17(2), 825–841.

    Article  PubMed  Google Scholar 

  34. Jenkinson, M., & Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5(2), 143–156. doi: 10.1016/S1361-8415(01)00036-6

  35. Jung, R. E., Ryman, S. G., Vakhtin, A. A., Carrasco, J., Wertz, C., & Flores, R. A. (2014). Subcortical correlates of individual differences in aptitude. PloS One, 9(2), e89425. doi:10.1371/journal.pone.0089425.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Kauranen, K., & Vanharanta, H. (1996). Influences of aging, gender, and handedness on motor performance of upper and lower extremities. Perceptual and Motor Skills, 82(2), 515–525. doi:10.2466/pms.1996.82.2.515.

    CAS  Article  PubMed  Google Scholar 

  37. Kumari, A., & Thakur, M. K. (2014). Age-dependent decline of nogo-a protein in the mouse cerebrum. Cellular and Molecular Neurobiology. doi:10.1007/s10571-014-0088-z.

    PubMed  Google Scholar 

  38. Lemaitre, H., Crivello, F., Grassiot, B., Alperovitch, A., Tzourio, C., & Mazoyer, B. (2005). Age- and sex-related effects on the neuroanatomy of healthy elderly. NeuroImage, 26(3), 900–911. doi:10.1016/j.neuroimage.2005.02.042.

    Article  PubMed  Google Scholar 

  39. Li, W., van Tol, M. J., Li, M., Miao, W., Jiao, Y., Heinze, H. J., et al. (2014). Regional specificity of sex effects on subcortical volumes across the lifespan in healthy aging. Human Brain Mapping, 35(1), 238–247. doi:10.1002/hbm.22168.

    Article  PubMed  Google Scholar 

  40. Liu, Y., Wang, G., Zhao, L., Geng, M., Wang, L., Bai, X., et al. (2013). SWI phase asymmetries in deep gray matter of healthy adults: is there an association with handedness? Brain Imaging and Behavior, 7(2), 220–226. doi:10.1007/s11682-012-9217-9.

    Article  PubMed  Google Scholar 

  41. Luders, E., Gaser, C., Narr, K. L., & Toga, A. W. (2009). Why sex matters: brain size independent differences in gray matter distributions between men and women. The Journal of Neuroscience, 29(45), 14265–14270. doi:10.1523/JNEUROSCI.2261-09.2009.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Luders, E., Narr, K. L., Thompson, P. M., Rex, D. E., Woods, R. P., Deluca, H., et al. (2006). Gender effects on cortical thickness and the influence of scaling. Human Brain Mapping, 27(4), 314–324. doi:10.1002/hbm.20187.

    CAS  Article  PubMed  Google Scholar 

  43. Macgregor, E. A., Rosenberg, J. D., & Kurth, T. (2011). Sex-related differences in epidemiological and clinic-based headache studies. Headache, 51(6), 843–859. doi:10.1111/j.1526-4610.2011.01904.x.

    Article  PubMed  Google Scholar 

  44. MacMaster, F. P., Carrey, N., Langevin, L. M., Jaworska, N., & Crawford, S. (2014). Disorder-specific volumetric brain difference in adolescent major depressive disorder and bipolar depression. Brain Imaging and Behavior, 8(1), 119–127. doi:10.1007/s11682-013-9264-x.

    Article  PubMed  Google Scholar 

  45. Munro, C. A., McCaul, M. E., Wong, D. F., Oswald, L. M., Zhou, Y., Brasic, J., et al. (2006). Sex differences in striatal dopamine release in healthy adults. Biological Psychiatry, 59(10), 966–974. doi:10.1016/j.biopsych.2006.01.008.

    CAS  Article  PubMed  Google Scholar 

  46. Murphy, D. G., DeCarli, C., McIntosh, A. R., Daly, E., Mentis, M. J., Pietrini, P., et al. (1996). Sex differences in human brain morphometry and metabolism: an in vivo quantitative magnetic resonance imaging and positron emission tomography study on the effect of aging. Archives of General Psychiatry, 53(7), 585–594.

    CAS  Article  PubMed  Google Scholar 

  47. Patenaude, B., Smith, S. M., Kennedy, D. N., & Jenkinson, M. (2011). A bayesian model of shape and appearance for subcortical brain segmentation. NeuroImage, 56(3), 907–922. doi:10.1016/j.neuroimage.2011.02.046.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Pell, G. S., Briellmann, R. S., Chan, C. H., Pardoe, H., Abbott, D. F., & Jackson, G. D. (2008). Selection of the control group for VBM analysis: influence of covariates, matching and sample size. NeuroImage, 41(4), 1324–1335. doi:10.1016/j.neuroimage.2008.02.050.

    Article  PubMed  Google Scholar 

  49. Perlaki, G., Orsi, G., Plozer, E., Altbacker, A., Darnai, G., Nagy, S. A., et al. (2014). Are there any gender differences in the hippocampus volume after head-size correction? A volumetric and voxel-based morphometric study. Neuroscience Letters, 570, 119–123. doi:10.1016/j.neulet.2014.04.013.

    CAS  Article  PubMed  Google Scholar 

  50. Peters, A., Morrison, J. H., Rosene, D. L., & Hyman, B. T. (1998). Feature article: are neurons lost from the primate cerebral cortex during normal aging? Cerebral Cortex, 8(4), 295–300.

    CAS  Article  PubMed  Google Scholar 

  51. Qian, S., Zhang, Z., Li, B., & Sun, G. (2014). Functional-structural degeneration in dorsal and ventral attention systems for alzheimer’s disease, amnestic mild cognitive impairment. Brain Imaging and Behavior. doi:10.1007/s11682-014-9336-6.

    Google Scholar 

  52. Raz, N., Gunning, F. M., Head, D., Dupuis, J. H., McQuain, J., Briggs, S. D., et al. (1997). Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cerebral Cortex, 7(3), 268–282.

    CAS  Article  PubMed  Google Scholar 

  53. Riccardi, P., Park, S., Anderson, S., Doop, M., Ansari, M. S., Schmidt, D., et al. (2011). Sex differences in the relationship of regional dopamine release to affect and cognitive function in striatal and extrastriatal regions using positron emission tomography and [(1)(8)F]fallypride. Synapse, 65(2), 99–102. doi:10.1002/syn.20822.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. Rijpkema, M., Everaerd, D., van der Pol, C., Franke, B., Tendolkar, I., & Fernandez, G. (2012). Normal sexual dimorphism in the human basal ganglia. Human Brain Mapping, 33(5), 1246–1252. doi:10.1002/hbm.21283.

    Article  PubMed  Google Scholar 

  55. Ruff, R. M., & Parker, S. B. (1993). Gender- and age-specific changes in motor speed and eye-hand coordination in adults: normative values for the finger tapping and grooved pegboard tests. Perceptual and Motor Skills, 76(3 Pt 2), 1219–1230. doi:10.2466/pms.1993.76.3c.1219.

    CAS  Article  PubMed  Google Scholar 

  56. Salminen, L. E., Conturo, T. E., Laidlaw, D. H., Cabeen, R. P., Akbudak, E., Lane, E. M., et al. (2015). Regional age differences in gray matter diffusivity among healthy older adults. Brain Imaging and Behavior. doi:10.1007/s11682-015-9383-7.

    PubMed  Google Scholar 

  57. Scahill, R. I., Frost, C., Jenkins, R., Whitwell, J. L., Rossor, M. N., & Fox, N. C. (2003). A longitudinal study of brain volume changes in normal aging using serial registered magnetic resonance imaging. Archives of Neurology, 60(7), 989–994. doi:10.1001/archneur.60.7.989.

    Article  PubMed  Google Scholar 

  58. Schwab, N. A., Tanner, J. J., Nguyen, P. T., Schmalfuss, I. M., Bowers, D., Okun, M., et al. (2014). Proof of principle: transformation approach alters caudate nucleus volume and structure-function associations. Brain Imaging and Behavior. doi:10.1007/s11682-014-9332-x.

    Google Scholar 

  59. Smith, C. D., Chebrolu, H., Wekstein, D. R., Schmitt, F. A., & Markesbery, W. R. (2007). Age and gender effects on human brain anatomy: a voxel-based morphometric study in healthy elderly. Neurobiology of Aging, 28(7), 1075–1087. doi:10.1016/j.neurobiolaging.2006.05.018.

    Article  PubMed  Google Scholar 

  60. Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143–155. doi:10.1002/hbm.10062.

    Article  PubMed  Google Scholar 

  61. Smith, S. M., De Stefano, N., Jenkinson, M., & Matthews, P. M. (2001). Normalized accurate measurement of longitudinal brain change. Journal of Computer Assisted Tomography, 25(3), 466–475.

    CAS  Article  PubMed  Google Scholar 

  62. Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23(Suppl 1), S208–S219. doi:10.1016/j.neuroimage.2004.07.051.

    Article  PubMed  Google Scholar 

  63. Smith, S. M., & Nichols, T. E. (2009). Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage, 44(1), 83–98. doi:10.1016/j.neuroimage.2008.03.061.

    Article  PubMed  Google Scholar 

  64. Smith, S. M., Zhang, Y., Jenkinson, M., Chen, J., Matthews, P. M., Federico, A., et al. (2002). Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. NeuroImage, 17(1), 479–489. doi:10.1006/nimg.2002.1040.

    Article  PubMed  Google Scholar 

  65. Sowell, E. R., Peterson, B. S., Kan, E., Woods, R. P., Yoshii, J., Bansal, R., et al. (2007). Sex differences in cortical thickness mapped in 176 healthy individuals between 7 and 87 years of age. Cerebral Cortex, 17(7), 1550–1560. doi:10.1093/cercor/bhl066.

    Article  PubMed  Google Scholar 

  66. Sullivan, E. V., Rosenbloom, M., Serventi, K. L., & Pfefferbaum, A. (2004). Effects of age and sex on volumes of the thalamus, pons, and cortex. Neurobiology of Aging, 25(2), 185–192.

    Article  PubMed  Google Scholar 

  67. Taber, K. H., Murphy, D. D., Blurton-Jones, M. M., & Hurley, R. A. (2001). An update on estrogen: higher cognitive function, receptor mapping, neurotrophic effects. Journal of Neuropsychiatry and Clinical Neurosciences, 13(3), 313–317. doi:10.1176/Appi.Neuropsych.13.3.313.

    CAS  Article  PubMed  Google Scholar 

  68. Takahashi, R., Ishii, K., Kakigi, T., & Yokoyama, K. (2011). Gender and age differences in normal adult human brain: voxel-based morphometric study. Human Brain Mapping, 32(7), 1050–1058. doi:10.1002/hbm.21088.

    Article  PubMed  Google Scholar 

  69. Taki, Y., Goto, R., Evans, A., Zijdenbos, A., Neelin, P., Lerch, J., et al. (2004). Voxel-based morphometry of human brain with age and cerebrovascular risk factors. Neurobiology of Aging, 25(4), 455–463. doi:10.1016/j.neurobiolaging.2003.09.002.

    Article  PubMed  Google Scholar 

  70. Taki, Y., Thyreau, B., Kinomura, S., Sato, K., Goto, R., Kawashima, R., et al. (2011). Correlations among brain gray matter volumes, age, gender, and hemisphere in healthy individuals. PloS One, 6(7), e22734. doi:10.1371/journal.pone.0022734.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  71. Tang, T., Jiao, Y., Wang, X., & Lu, Z. (2013). Gender versus brain size effects on subcortical gray matter volumes in the human brain. Neuroscience Letters, 556, 79–83. doi:10.1016/j.neulet.2013.09.060.

    CAS  Article  PubMed  Google Scholar 

  72. Terry, R. D., DeTeresa, R., & Hansen, L. A. (1987). Neocortical cell counts in normal human adult aging. Annals of Neurology, 21(6), 530–539. doi:10.1002/ana.410210603.

    CAS  Article  PubMed  Google Scholar 

  73. Webb, S. J., Monk, C. S., & Nelson, C. A. (2001). Mechanisms of postnatal neurobiological development: implications for human development. Developmental Neuropsychology, 19(2), 147–171. doi:10.1207/S15326942DN1902_2.

    CAS  Article  PubMed  Google Scholar 

  74. Zhang, Y., Brady, M., & Smith, S. (2001). Segmentation of brain MR images through a hidden markov random field model and the expectation-maximization algorithm. IEEE Transactions on Medical Imaging, 20(1), 45–57. doi:10.1109/42.906424.

    CAS  Article  PubMed  Google Scholar 

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Acknowledgments

The study was supported by the MTA-SZTE Neuroscience Research Group, the project FNUSA-ICRC (no. CZ.1.05/1.1.00/02.0123) from the European Regional Development Fund, by European Union - project ICRC-ERA-HumanBridge (No. 316345), the National Brain Research Program (Grant No. KTIA_13_NAP-A-II/20.) and an OTKA [PD 104715] grant.

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Correspondence to Zsigmond Tamás Kincses.

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Király, A., Szabó, N., Tóth, E. et al. Male brain ages faster: the age and gender dependence of subcortical volumes. Brain Imaging and Behavior 10, 901–910 (2016). https://doi.org/10.1007/s11682-015-9468-3

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Keywords

  • Subcortical structures
  • Brain volume
  • Gender
  • Aging
  • MRI