The heritability of volumes of brain structures and its relationship to age: A review of twin and family studies

Ageing Research Reviews

Volumn 13, Issue 1, 2014, Pages 1-9

  Batouli, Seyed Amir Hossein ^a   Trollor, Julian N ^a,b   Wen, Wei ^a,c   Sachdev, Perminder S ^a,c  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c PRINCE OF WALES HOSPITAL   (Australia)

Author keywords

Brain volume; Elderly; Healthy ageing; Heritability; Twins

Indexed keywords

AGE; AMYGDALOID NUCLEUS; BRAIN SIZE; CEREBELLUM; CORPUS CALLOSUM; CROSS-SECTIONAL STUDY; FAMILY STUDY; FRONTAL LOBE; GRAY MATTER; HERITABILITY; HIPPOCAMPUS; HUMAN; MIDDLE TEMPORAL GYRUS; OCCIPITAL LOBE; PARAHIPPOCAMPAL GYRUS; PARIETAL LOBE; POSTCENTRAL GYRUS; PUTAMEN; REVIEW; SUPERIOR FRONTAL GYRUS; SUPERIOR TEMPORAL GYRUS; SYSTEMATIC REVIEW; TEMPORAL LOBE; THALAMUS; TISSUE STRUCTURE; TWINS; WHITE MATTER;

BRAIN VOLUME; ELDERLY; HEALTHY AGEING; HERITABILITY; TWINS;

AGE FACTORS; AGING; BRAIN; GENOTYPE; HEREDITY; HUMANS; ORGAN SIZE; PHENOTYPE; TWIN STUDIES AS TOPIC; TWINS;

EID: 84888217465     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2013.10.003     Document Type: Review

References (95)

1. Allen J.S., Bruss J., Brown C.K., Damasio H. Normal neuroanatomical variation due to age: the major lobes and a parcellation of the temporal region. Neurobiology of Aging 2005, 26:1245-1260.
2. Attardi G., Schatz G. Biogenesis of mitochondria. Annual Review of Cell Biology 1988, 4:289-331.
3. Baare W.F.C., Hulshoff Pol H.E., Boomsma D.I., Posthuma D., de Geus E.J.C., Schnack H.G., van Haren N.E.M., van Oel C.J., Kahn R.S. Quantitative genetic modeling of variation in human brain morphology. Cerebral Cortex 2001, 11:816-824.
4. Bartley A., Jones D., Weinberger D. Genetic variability of human brain size and cortical gyral patterns. Brain 1997, 120:257-269.
5. Bartzokis G., Beckson M., Lu P.H., Nuechterlein K.H., Edwards N., Mintz J. Age-related changes in frontal and temporal lobe volumes in men: a magnetic resonance imaging study. Archives of General Psychiatry 2001, 58:461-465.
6. Bartzokis G., Cummings J.L., Sultzer D., Henderson V.W., Nuechterlein K.H., Mintz J. White matter structural integrity in healthy aging adults and patients with alzheimer disease: a magnetic resonance imaging study. Archives of Neurology 2003, 60:393-398.
7. Bartzokis G., Sultzer D., Lu P.H., Nuechterlein K.H., Mintz J., Cummings J.L. Heterogeneous age-related breakdown of white matter structural integrity: implications for cortical "disconnection" in aging and Alzheimer's disease. Neurobiology of Aging 2004, 25:843-851.
8. Betjemann R., Johnson E., Barnard H., Boada R., Filley C., Filipek P., Willcutt E., DeFries J., Pennington B. Genetic covariation between brain volumes and IQ, reading performance, and processing speed. Behavior Genetics 2010, 40:135-145.
9. Blokland G.A.M., de Zubicaray G.I., McMahon K.L., Wright M.J. Genetic and environmental influences on neuroimaging phenotypes: a meta-analytical perspective on twin imaging studies. Twin Research and Human Genetics 2012, 15:351-371.
10. Boomsma D., Busjahn A., Peltonen L. Classical twin studies and beyond. Nature Reviews Genetics 2002, 3:872-882.
11. Brouwer R.M., Mandl R.C.W., Schnack H.G., van Soelen I.L.C., van Baal G.C., Peper J.S., Kahn R.S., Boomsma D.I., Pol H.E.H. White matter development in early puberty: a longitudinal volumetric and diffusion tensor imaging twin study. PLoS ONE 2012, 7:e32316.
12. Carmelli D., Swan G.E., DeCarli C., Reed T. Quantitative genetic modeling of regional brain volumes and cognitive performance in older male twins. Biological Psychology 2002, 61:139-155.
13. Chee M.W.L., Chen K.H.M., Zheng H., Chan K.P.L., Isaac V., Sim S.K.Y., Chuah L.Y.M., Schuchinsky M., Fischl B., Ng T.P. Cognitive function and brain structure correlations in healthy elderly East Asians. NeuroImage 2009, 46:257-269.
14. Chen Z.G., Li T.-Q, Hindmarsh T. Diffusion tensor trace mapping in normal adult brain using single-shot EPI technique: a methodological study of the aging brain. Acta Radiologica 2001, 42:447-458.
15. Chiang M.-C., Barysheva M., Shattuck D.W., Lee A.D., Madsen S.K., Avedissian C., Klunder A.D., Toga A.W., McMahon K.L., de Zubicaray G.I., Wright M.J., Srivastava A., Balov N., Thompson P.M. Genetics of brain fiber architecture and intellectual performance. The Journal of Neuroscience 2009, 29:2212-2224.
16. Chou Y.Y., Leporé N., Chiang M.C., Avedissian C., Barysheva M., McMahon K.L., de Zubicaray G.I., Meredith M., Wright M.J., Toga A.W., Thompson P.M. Mapping genetic influences on ventricular structure in twins. NeuroImage 2009, 44:1312-1323.
17. Courchesne E., Chisum H.J., Townsend J., Cowles A., Covington J., Egaas B., Harwood M., Hinds S., Press G.A. Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. Radiology 2000, 216:672-682.
18. Craik F.I.M. Memory changes in normal aging. Current Directions in Psychological Science 1994, 3:155-158.
19. DeStefano A.L., Seshadri S., Beiser A., Atwood L.D., Massaro J.M., Au R., Wolf P.A., DeCarli C. Bivariate heritability of total and regional brain volumes: the Framingham Study. Alzheimer Disease & Associated Disorders 2009, 23:218-223. 10.1097/WAD.1090b1013e31819cadd31818.
20. Elbert T., Pantev C., Wienbruch C., Rockstroh B., Taub E. Increased cortical representation of the fingers of the left hand in string players. Science 1995, 270:305-307.
21. Finch C.E. Longevity, Senescence, and the Genome 1990, University of Chicago Press, Chicago.
22. Finkel D., Pedersen N.L., Plomin R., McClearn G.E. Longitudinal and cross-sectional twin data on cognitive abilities in adulthood: the Swedish Adoption/Twin Study of Aging. Developmental Psychology 1998, 34:1400-1413.
23. Fjell A.M., Walhovd K.B., Fennema C., McEvoy L.K., Hagler D.J., Holland D., Brewer J.B., Dale A.M. One-year brain atrophy evident in healthy aging. Journal of Neuroscience 2009, 29:15223-15231.
24. Galluzzi S., Beltramello A., Filippi M., Frisoni G. Aging. Neurological Sciences 2008, 29:296-300.
25. Ge Y., Grossman R.I., Babb J.S., Rabin M.L., Mannon L.J., Kolson D.L. Age-related total gray matter and white matter changes in normal adult brain. Part II: Quantitative magnetization transfer ratio histogram analysis. American Journal of Neuroradiology 2002, 23:1334-1341.
26. Geschwind D.H., Miller B.L., DeCarli C., Carmelli D. Heritability of lobar brain volumes in twins supports genetic models of cerebral laterality and handedness. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:3176-3181.
27. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., Paus T., Evans A.C., RapoportF J.L. Brain development during childhood and adolescence: a longitudinal MRI study. Nature Neuroscience 1999, 2:861-863.
28. Giedd J.N., Schmitt J.E., Neale M.C. Structural brain magnetic resonance imaging of pediatric twins. Human Brain Mapping 2007, 28:474-481.
29. Gilmore J.H., Schmitt J.E., Knickmeyer R.C., Smith J.K., Lin W., Styner M., Gerig G., Neale M.C. Genetic and environmental contributions to neonatal brain structure: a twin study. Human Brain Mapping 2010, 31:1174-1182.
30. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., Nugent T.F., Herman D.H., Clasen L.S., Toga A.W., Rapoport J.L., Thompson P.M. Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:8174-8179.
31. Golzio C., Willer J., Talkowski M.E., Oh E.C., Taniguchi Y., Jacquemont S., Reymond A., Sun M., Sawa A., Gusella J.F., Kamiya A., Beckmann J.S., Katsanis N. KCTD13 is a major driver of mirrored neuroanatomical phenotypes of the 16p11.2 copy number variant. Nature 2012, 485:363-367.
32. Haworth C.M.A., Kovas Y., Harlaar N., Hayiou-Thomas M.E., Petrill S.A., Dale P.S., Plomin R. Generalist genes and learning disabilities: a multivariate genetic analysis of low performance in reading, mathematics, language and general cognitive ability in a sample of 8000 12-year-old twins. Journal of Child Psychology and Psychiatry 2009, 50:1318-1325.
33. Head D., Buckner R.L., Shimony J.S., Williams L.E., Akbudak E., Conturo T.E., McAvoy M., Morris J.C., Snyder A.Z. Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging. Cerebral Cortex 2004, 14:410-423.
34. Hedden T., Gabrieli J. Insights into the ageing mind: a view from cognitive neuroscience. Nature Reviews Neuroscience 2004, 5:87-96.
35. Hulshoff P., Hilleke E., Posthuma D., Baare W.F.C., De Geus E.J.C., Schnack H.G., van Haren N.E.M., van Oel C.J., Kahn R.S., Boomsma D.I. Twin-singleton differences in brain structure using structural equation modelling. Brain 2002, 125:384-390.
36. Kovas Y., Haworth C.M.A., Dale P.S., Plomin R. The genetic and environmental origins of learning abilities and disabilities in the early school years. Monographs of the Society for Research in Child Development 2007, 72:1-13.
37. Kremen W.S., Prom-Wormley E., Panizzon M.S., Eyler L.T., Fischl B., Neale M.C., Franz C.E., Lyons M.J., Pacheco J., Perry M.E., Stevens A., Schmitt J.E., Grant M.D., Seidman L.J., Thermenos H.W., Tsuang M.T., Eisen S.A., Dale A.M., Fennema-Notestine C. Genetic and environmental influences on the size of specific brain regions in midlife: the VETSA MRI study. NeuroImage 2010, 49:1213-1223.
38. Lee T., Henry J.D., Trollor J.N., Sachdev P.S. Genetic influences on cognitive functions in the elderly: a selective review of twin studies. Brain Research Reviews 2010, 64:1-13.
39. Lenroot R.K., Giedd J.N. The changing impact of genes and environment on brain development during childhood and adolescence: initial findings from a neuroimaging study of pediatric twins. Development and Psychopathology 2008, 20:1161-1175.
40. Lessov-Schlaggar C.N., Hardin J., DeCarli C., Krasnow R.E., Reed T., Wolf P.A., Swan G.E., Carmelli D. Longitudinal genetic analysis of brain volumes in normal elderly male twins. Neurobiology of Aging 2012, 33:636-644.
41. Lind J., Larsson A., Persson J., Ingvar M., Nilsson L.-G., Bäckman L., Adolfsson R., Cruts M., Sleegers K., Van Broeckhoven C., Nyberg L. Reduced hippocampal volume in non-demented carriers of the apolipoprotein E e4: relation to chronological age and recognition memory. Neuroscience Letters 2006, 396:23-27.
42. Liu R.S.N., Lemieux L., Bell G.S., Sisodiya S.M., Shorvon S.D., Sander J.W.A.S., Duncan J.S. A longitudinal study of brain morphometrics using quantitative magnetic resonance imaging and difference image analysis. NeuroImage 2003, 20:22-33.
43. Lustig C., Shah P., Seidler R., Reuter-Lorenz P. Aging training, and the brain: a review and future directions. Neuropsychology Review 2009, 19:504-522.
44. Maguire E.A., Gadian D.G., Johnsrude I.S., Good C.D., Ashburner J., Frackowiak R.S.J., Frith C.D. Navigation-related structural change in the hippocampi of taxi drivers. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:4398-4403.
45. Mattay V.S., Goldberg T.E., Sambataro F., Weinberger D.R. Neurobiology of cognitive aging: insights from imaging genetics. Biological Psychology 2008, 79:9-22.
46. Meyer-Lindenberg A., Buckholtz J.W., Kolachana B.R., Hariri A., Pezawas L., Blasi G., Wabnitz A., Honea R., Verchinski B., Callicott J.H., Egan M., Mattay V., Weinberger D.R. Neural mechanisms of genetic risk for impulsivity and violence in humans. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:6269-6274.
47. Mx: Statistical Modeling 1994, Department of Psychiatry, Box 710 MCV, Richmond, VA 23298. M.C. Neale (Ed.).
48. Pedersen N.L. Genetics of human aging: Swedish twin studies. Generations 2000, 24:31-35.
49. Pennington B.F., Filipek P.A., Lefly D., Chhabildas N., Kennedy D.N., Simon J.H., Filley C.M., Galaburda A., Defries J.C. A twin MRI study of size variations in the human brain. Journal of Cognitive Neuroscience 2000, 12:223-232.
50. Peper J.S., Brouwer R.M., Boomsma D.I., Kahn R.S., Pol H.E.H. Genetic influences on human brain structure: a review of brain imaging studies in twins. Human Brain Mapping 2007, 28:464-473.
51. Peper J.S., Schnack H.G., Brouwer R.M., Baal G.C., Pjetri E., Székely E., van Leeuwen M., van den Berg S.M., Collins D.L., Evans A.C., Boomsma D.I., Kahn R.S., Pol H.E.H. Heritability of regional and global brain structure at the onset of puberty: a magnetic resonance imaging study in 9-year-old twin pairs. Human Brain Mapping 2009, 30:2184-2196.
52. Pezawas L., Verchinski B.A., Mattay V.S., Callicott J.H., Kolachana B.S., Straub V.E., Egan M.F., Meyer-Lindenberg A., Weinberger D.R. The brain-derived neurotrophic factor val66met polymorphism and variation in human cortical morphology. The Journal of Neuroscience 2004, 24:10099-10102.
53. Pfefferbaum A., Mathalon D.H., Sullivan E.V., Rawles J.M., Zipursky R.B., Lim K.O. A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Archives of Neurology 1994, 51:874-887.
54. Pfefferbaum A., Sullivan E.V., Carmelli D. Morphological changes in aging brain structures are differentially affected by time-linked environmental influences despite strong genetic stability. Neurobiology of Aging 2004, 25:175-183.
55. Pfefferbaum A., Sullivan E.V., Swan G.E., Carmelli D. Brain structure in men remains highly heritable in the seventh and eighth decades of life. Neurobiology of Aging 2000, 21:63-74.
56. Plomin R., Craig I. Human behavioural genetics of cognitive abilities and disabilities. BioEssays 1997, 19:1117-1124.
57. Plomin R., Kosslyn S.M. Genes, brain and cognition. Nature Neuroscience 2001, 4:1153-1154.
58. Plomin R., Pedersen N.L., Lichtenstein P., McClearn G.E. Variability and stability in cognitive abilities are largely genetic later in life. Behavior Genetics 1994, 24:207-215.
59. Posthuma D., Baaré W.F.C., Hulshoff Pol H.E., Kahn R.S., Boomsma D.I., Geus E.J.C.D Genetic correlations between brain volumes and the WAIS-III dimensions of verbal comprehension, working memory, perceptual organization, and processing speed. Twin Research 2003, 6:131-139.
60. Posthuma D., De Geus E.J.C., Baaré W.F.C., Hulshoff Pol H.E., Kahn R.S., Boomsma D.I. The association between brain volume and intelligence is of genetic origin. Nature Neuroscience 2002, 5:83-84.
61. Posthuma D., de Geus E.J.C., Neale M.C., Hulshoff Pol H.E., Baaré W.E.C., Kahn R.S., Boomsma D. Multivariate genetic analysis of brain structure in an extended twin design. Behavior Genetics 2000, 30:311-319.
62. Rapoport J.L., Gogtay N. Brain neuroplasticity in healthy hyperactive and psychotic children: insights from neuroimaging. Neuropsychopharmacology 2007, 33:181-197.
63. Raz N. Aging of the brain and its impact on cognitive performance: integration of structural and functional findings. The Handbook of Aging and Cognition 2000, 1-90. Lawrence Erlbaum Associates Publishers, Mahwah, NJ, US. 2nd ed. F.I.M. Craik, T.A. Salthouse (Eds.).
64. Raz N., Briggs S.D., Marks W., Acker J.D. Age-related deficits in generation and manipulation of mental images: II. The role of dorsolateral prefrontal cortex. Psychology and Aging 1999, 14:436-444.
65. Raz N., Rodrigue K.M. Differential aging of the brain: patterns, cognitive correlates and modifiers. Neuroscience & Biobehavioral Reviews 2006, 30:730-748.
66. Resnick S.M., Goldszal A.F., Davatzikos C., Golski S., Kraut M.A., Metter E.J., Bryan R.N., Zonderman A.B. One-year age changes in MRI brain volumes in older adults. Cerebal Cortex 2000, 10:464-472.
67. Riddle W.R., DonLevy S.C., Lee H. Modeling brain tissue volumes over the lifespan: quantitative analysis of postmortem weights and in vivo MR images. Magnetic Resonance Imaging 2010, 28:716-720.
68. Riello R., Sabattoli F., Beltramello A., Bonetti M., Bono G., Falini A., Magnani G., Minonzio G., Piovan E., Alaimo G., Ettori M., Galluzzi S., Locatelli E., Noiszewska M., Testa C., Frisoni G. Brain volumes in healthy adults aged 40 years and over: a voxel-based morphometry study. Aging Clinical and Experimental Research 2005, 17:329-336.
69. Rogers J., Kochunov P., Zilles K., Shelledy W., Lancaster J., Thompson P., Duggirala R., Blangero J., Fox P.T., Glahn D.C. On the genetic architecture of cortical folding and brain volume in primates. NeuroImage 2010, 53:1103-1108.
70. Sarah E.B., Gardner C.O., Kendler K.S. Age-related changes in heritability of behavioral phenotypes over adolescence and young adulthood: a meta-analysis. Twin Research and Human Genetics 2007, 10:423-433.
71. Schmitt J.E., Eyler L.T., Giedd J.N., Kremen W.S., Kendler K.S., Neale M.C. Review of twin and family studies on neuroanatomic phenotypes and typical neurodevelopment. Twin Research and Human Genetics 2007, 10:683-694.
72. Singer J.J., MacGregor A.J., Cherkas L.F., Spector T.D. Genetic influences on cognitive function using The Cambridge Neuropsychological Test Automated Battery. Intelligence 2006, 34:421-428.
73. Sowell E.R., Peterson B.S., Thompson P.M., Welcome S.E., Henkenius A.L., Toga A.W. Mapping cortical change across the human life span. Nature Neuroscience 2003, 6:309-315.
74. Sullivan E.V., Pfefferbaum A., Adalsteinsson E., Swan G.E., Carmelli D. Differential rates of regional brain change in callosal and ventricular size: a 4-year longitudinal MRI study of elderly men. Cerebral Cortex 2002, 12:438-445.
75. Sullivan E.V., Pfefferbaum A., Swan G.E., Carmelli D. Heritability of hippocampal size in elderly twin men: equivalent influence from genes and environment. Hippocampus 2001, 11:754-762.
76. Taki Y., Kinomura S., Sato K., Goto R., Kawashima R., Fukuda H. A longitudinal study of gray matter volume decline with age and modifying factors. Neurobiology of Aging 2011, 32:907-915.
77. Thompson P.M., Cannon T.D., Narr K.L., van Erp T., Poutanen V.P., Huttunen M., Lönnqvist J., Standertskjöld Nordenstam C.-G., Kaprio J., Khaledy M., Dail R., Zoumalan C.I., Toga A.W. Genetic influences on brain structure. Nature Neuroscience 2001, 4:1253-1258.
78. Toga A.W., Thompson P.M. Genetics of brain structure and intelligence. Annual Review of Neuroscience 2005, 28:1-23.
79. Trzaskowski M., Yang J., Visscher P.M., Plomin R. DNA evidence for strong genetic stability and increasing heritability of intelligence from age 7 to 12. Molecular Psychiatry 2013, 10.1038/mp.2012.191.
80. Ungerleider L.G., Doyon J., Karni A. Imaging brain plasticity during motor skill learning. Neurobiology of Learning and Memory 2002, 78:553-564.
81. van Leeuwen M., Peper J.S., van den Berg S.M., Brouwer R.M., Hulshoff Pol H.E., Kahn R.S., Boomsma D.I. A genetic analysis of brain volumes and IQ in children. Intelligence 2009, 37:181-191.
82. van Soelen I.L.C., Brouwer R.M., van Baal G.C.M., Schnack H.G., Peper J.S., Chen L., Kahn R.S., Boomsma D.I., Pol H.E.H. Heritability of volumetric brain changes and height in children entering puberty. Human Brain Mapping 2013, 34:713-725.
83. Walhovd K.B., Fjell A.M., Reinvang I., Lundervold A., Dale A.M., Eilertsen D.E., Quinn B.T., Salat D., Makris N., Fischl B. Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiology of Aging 2005, 26:1261-1270.
84. Wallace D.C., Melov S. Radicals r'aging. Nature Genetics 1998, 19:105-106.
85. Wallace G., Lee N., Prom-Wormley E., Medland S., Lenroot R., Clasen L., Schmitt J., Neale M., Giedd J. A bivariate twin study of regional brain volumes and verbal and nonverbal intellectual skills during childhood and adolescence. Behavior Genetics 2010, 40:125-134.
86. Wallace G.L., Schmitt J.E., Lenroot R., Viding E., Ordaz S., Rosenthal M.A., Molloy E.A., Clasen L.S., Kendler K.S., Neale M.C., Giedd J.N. A pediatric twin study of brain morphometry. Journal of Child Psychology and Psychiatry 2006, 47:987-993.
87. Winkler A.M., Kochunov P., Blangero J., Almasy L., Zilles K., Fox P.T., Duggirala R., Glahn D.C. Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. NeuroImage 2010, 53:1135-1146.
88. Wright I.C., Sham P., Murray R.M., Weinberger D.R., Bullmore E.T. Genetic contributions to regional variability in human brain structure: methods and preliminary results. NeuroImage 2002, 17:256-271.
89. Yau-Huei W., Ching-You L., Hsin-Chen L., Cheng-Yoong P., Yi-Shing M. Oxidative damage and mutation to mitochondrial DNA and age-dependent decline of mitochondrial respiratory functiona. Annals of the New York Academy of Sciences 1998, 854:155-170.
90. Yoon U., Fahim C., Perusse D., Evans A.C. Lateralized genetic and environmental influences on human brain morphology of 8-year-old twins. NeuroImage 2010, 53:1117-1125.
91. Yoon U., Perusse D., Lee J.-M., Evans A.C. Genetic and environmental influences on structural variability of the brain in pediatric twin: deformation based morphometry. Neuroscience Letters 2011, 493:8-13.
92. Hulshoff Pol H.E., Schnack H.G., Posthuma D., Mandl R.C.W., Baare W.F., van Oel C., van Haren N.E., Collins D.L., Evans A.C., Amunts K., Burgel U., Zilles K., de Geus E., Boomsma D.I., Kahn R.S. Genetic Contributions to Human Brain Morphology and Intelligence. Journal of Neuroscience 2006, 26:10235-10242.
93. Panizzon M.S., Hauger R.L., Eaves L.J., Chen C.H., Dale A.M., Eyler L.T., Fischl B., Fennema-Notestine C., Franz C.E., Grant M.D., Jacobson K.C., Jak A.J., Lyons M.J., Mendoza S.P., Neale M.C., Prom-Wormley E., Seidman L.J., Tsuang M.T., Xian H., Kremen W.S. Genetic influences on hippocampal volume differ as a function of testosterone level in middle-aged men. NeuroImage 2012, 59:9.
94. Pfefferbaum A., Sullivan E.V., Carmelli D. Genetic regulation of regional microstructure of the corpus callosum in late life. NeuroReport 2001, 12:1677-1681.
95. Scamvougeras A., Kigar D.L., Jones D., Weinberger D.R., Witelson S.F. Size of the human corpus callosum is genetically determined: an MRI study in mono and dizygotic twins. Neuroscience Letters 2003, 338:91-94.