Age-related differences in the structural complexity of subcortical and ventricular structures

Neurobiology of Aging

Volumn 50, Issue , 2017, Pages 87-95

  Madan, Christopher R ^a   Kensinger, Elizabeth A ^a  

^a BOSTON COLLEGE   (United States)

Author keywords

Age; Atrophy; Brain morphometry; Fractal dimensionality; Hippocampus; Putamen; Thalamus; Ventricles

Indexed keywords

ADULT; AGE; AGED; AMYGDALA; ARTICLE; BRAIN SIZE; BRAIN VENTRICLE; CAUDATE NUCLEUS; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; GLOBUS PALLIDUS; HIPPOCAMPUS; HUMAN; IMAGE RECONSTRUCTION; IMAGE SEGMENTATION; LIFESPAN; MALE; NEUROIMAGING; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PUTAMEN; SUBCORTEX; THALAMUS; VOXEL BASED MORPHOMETRY; ADOLESCENT; AGING; BRAIN CORTEX; INFORMATION PROCESSING; MIDDLE AGED; PATHOLOGY; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; CAUDATE NUCLEUS; CEREBRAL CORTEX; CEREBRAL VENTRICLES; DATASETS AS TOPIC; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MIDDLE AGED; PUTAMEN; THALAMUS; YOUNG ADULT;

EID: 85002781513     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2016.10.023     Document Type: Article

References (86)

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. Neurobiol. Aging 26 (2005), 1245–1260.
2. Apostolova, L.G., Green, A.E., Babakchanian, S., Hwang, K.S., Chou, Y.-Y., Toga, A.W., Thompson, P.M., Hippocampal atrophy and ventricular enlargement in normal aging, mild cognitive impairment (MCI), and Alzheimer disease. Alzheimer Dis. Assoc. Disord. 26 (2012), 17–27.
3. Barron, S.A., Jacobs, L., Kinkel, W.R., Changes in size of normal lateral ventricles during aging determined by computerized tomography. Neurology 26 (1976), 1011–1013.
4. Buckner, R.L., Head, D., Parker, J., Fotenos, A.F., Marcus, D., Morris, J.C., Snyder, A.Z., A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage 23 (2004), 724–738.
5. Burnham, K.E., Anderson, D.R., Model Selection and Multimodel Inference. second ed., 2002, Springer-Verlag, New York.
6. Burnham, K.P., Anderson, D.R., Multimodel inference: understanding AIC and BIC in model selection. Sociol. Methods Res. 33 (2004), 261–304.
7. Caserta, F., Eldred, W.D., Fernandez, E., Hausman, R.E., Stanford, L.R., Bulderev, S.V., Schwarzer, S., Stanley, H.E., Determination of fractal dimension of physiologically characterized neurons in two and three dimensions. J. Neurosci. Methods 56 (1995), 133–144.
8. Chung, M.K., Nacewicz, B.M., Wang, S., Dalton, K.M., Pollak, S., Davidson, R.J., Amygdala surface modeling with weighted spherical harmonics. Lect. Notes Comput. Sci. 5128 (2008), 177–184.
9. Chung, M.K., Worsley, K.J., Nacewicz, B.M., Dalton, K.M., Davidson, R.J., General multivariate linear modeling of surface shapes using SurfStat. Neuroimage 53 (2010), 491–505.
10. Creasey, H., Rapoport, S.I., The aging human brain. Ann. Neurol. 17 (1985), 2–10.
11. Di Ieva, A., Esteban, F.J., Grizzi, F., Klonowski, W., Martin-Landrove, M., Fractals in the neurosciences, Part II: clinical applications and future perspectives. Neuroscientist 21 (2015), 30–43.
12. Di Ieva, A., Grizzi, F., Jelinek, H., Pellionisz, A.J., Losa, G.A., Fractals in the neurosciences, Part I: general principles and basic neurosciences. Neuroscientist 20 (2013), 403–417.
13. Drayer, B.P., Imaging of the aging brain. Part I. Normal findings. Radiology 166 (1988), 785–796.
14. Fischl, B., FreeSurfer. Neuroimage 62 (2012), 774–781.
15. Fischl, B., Dale, A.M., Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 11050–11055.
16. Fischl, B., Salat, D.H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., van der Kouwe, A., Killiany, R., Kennedy, D., Klaveness, S., Montillo, A., Makris, N., Rosen, B., Dale, A.M., Whole brain segmentation: automated labelling of neuroanatomical structures in the human brain. Neuron 33 (2002), 341–355.
17. Fischl, B., Salat, D.H., van der Kouwe, A.J.W., Makris, N., Ségonne, F., Quinn, B.T., Dale, A.M., Sequence-independent segmentation of magnetic resonance images. Neuroimage 23 (2004), S69–S84.
18. Fischl, B., Sereno, M.I., Dale, A.M., Cortical surface-based analysis. Neuroimage 9 (1999), 195–207.
19. Fjell, A.M., Westlye, L.T., Amlien, I., Espeseth, T., Reinvang, I., Raz, N., Agartz, I., Salat, D.H., Greve, D.N., Fischl, B., Dale, A.M., Walhovd, K.B., High consistency of regional cortical thinning in aging across multiple samples. Cereb. Cortex 19 (2009), 2001–2012.
20. Free, S.L., Sisodiya, S.M., Cook, M.J., Fish, D.R., Shorvon, S.D., Three-dimensional fractal analysis of the white matter surface from magnetic resonance images of the human brain. Cereb. Cortex 6 (1996), 830–836.
21. Goodro, M., Sameti, M., Patenaude, B., Fein, G., Age effect on subcortical structures in healthy adults. Psychiatry Res. 203 (2012), 38–45.
22. Greenberg, D.L., Messer, D.F., Payne, M.E., MacFall, J.R., Provenzale, J.M., Steffens, D.C., Krishnan, R.R., Aging, gender, and the elderly adult brain: an examination of analytical strategies. Neurobiol. Aging 29 (2008), 290–302.
23. Gunning-Dixon, F.M., Head, D., McQuain, J., Acker, J.D., Raz, N., Differential aging of the human striatum: a prospective MR imaging study. Am. J. Neuroradiol. 19 (1998), 1501–1507.
24. Ha, T.H., Yoon, U., Lee, K.J., Shin, Y.W., Lee, J.-M., Kim, I.Y., Ha, K.S., Kim, S.I., Kwon, J.S., Fractal dimension of cerebral cortical surface in schizophrenia and obsessive–compulsive disorder. Neurosci. Lett. 384 (2005), 172–176.
25. Hogstrom, L.J., Westlye, L.T., Walhovd, K.B., Fjell, A.M., The structure of the cerebral cortex across adult life: age-related patterns of surface area, thickness, and gyrification. Cereb. Cortex 23 (2013), 2521–2530.
26. Hofman, M.A., The fractal geometry of convoluted brains. J. Hirnforsch. 32 (1991), 103–111.
27. Hrybouski, S., Aghamohammadi-Sereshki, A., Madan, C.R., Shafer, A.T., Baron, C.A., Seres, P., Beaulieu, C., Olsen, F., Malykhin, N.V., Amygdala subnuclei response and connectivity during emotional processing. Neuroimage 133 (2016), 98–110.
28. Im, K., Lee, J.-M., Yoon, U., Shin, Y.-W., Hong, S.B., Kim, I.Y., Kwon, J.S., Kim, S.I., Fractal dimension in human cortical surface: multiple regression analysis with cortical thickness, sulcal depth, and folding area. Hum. Brain Mapp. 27 (2006), 994–1003.
29. Inano, S., Takao, H., Hayashi, N., Yoshioka, N., Mori, H., Kunimatsu, A., Abe, O., Ohtomo, K., Effects of age and gender on neuroanatomical volumes. J. Magn. Reson. Imaging 37 (2013), 1072–1076.
30. Jernigan, T.L., Archibald, S.L., Fennema-Notestine, C., Gamst, A.C., Stout, J.C., Bonner, J., Hesselink, J.R., Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol. Aging 22 (2001), 581–594.
31. Jovicich, J., Czanner, S., Han, X., Salat, D.H., van der Kouwe, A.J.W., Quinn, B., Pacheco, J., Albert, M., Killany, R., Blacker, D., Maguire, P., Rosas, D., Makris, N., Gollub, R., Dale, A.M., Dickerson, B.C., Fischl, B., MRI-derived measurements of human subcortical, ventricular and intracranial brain volumes: reliability effects of scan sessions, acquisition sequences, data analyses, scanner upgrade, scanner vendors and field strengths. Neuroimage 46 (2009), 177–192.
32. Kaye, J.A., DeCarli, C., Luxenberg, J.S., Rapoport, S.I., The significance of age-related enlargement of the cerebral ventricles in healthy men and women measured by quantitative computed X-ray tomography. J. Am. Geriatr. Soc. 40 (1992), 225–231.
33. Keller, S.S., Gerdes, J.S., Mohammadi, S., Kellinghaus, C., Kugel, H., Deppe, K., Ringelstein, E.B., Evers, S., Schwindt, W., Deppe, M., Volume estimation of the thalamus using FreeSurfer and stereology: consistency between methods. Neuroinformatics 10 (2012), 341–350.
34. Kemper, T.L., Neuroanatomical and neuropathological changes during aging and dementia. Albert, M.L., Knoefel, J.E., (eds.) Clinical Neurology of Aging, second ed., 1994, Oxford University Press, New York, 3–67.
35. King, R.D., Brown, B., Hwang, M., Jeon, T., George, A.T., Fractal dimension analysis of the cortical ribbon in mild Alzheimer's disease. Neuroimage 53 (2010), 471–479.
36. King, R.D., George, A.T., Jeon, T., Hynan, L.S., Youn, T.S., Kennedy, D.N., Dickerson, B., Characterization of atrophic changes in the cerebral cortex using fractal dimensional analysis. Brain Imaging Behav. 3 (2009), 154–166.
37. Kiselev, V.G., Hahn, K.R., Auer, D.P., Is the brain cortex a fractal?. Neuroimage 20 (2003), 1765–1774.
38. Kochunov, P., Thompson, P.M., Coyle, T.R., Lancaster, J.L., Kochunov, V., Royall, D., Mangin, J.-F., Rivière, D., Fox, P.T., Relationship among neuroimaging indices of cerebral health during normal aging. Hum. Brain Mapp. 29 (2008), 36–45.
39. La Joie, R., Fouquet, M., Mézenge, F., Landeau, B., Villain, N., Mevel, K., Pélerin, A., Eustache, F., Desgranges, B., Chételat, G., Differential effect of age on hippocampal subfields assessed using a new high-resolution 3T MR sequence. Neuroimage 53 (2010), 506–514.
40. Lehmann, M., Douiri, A., Kim, L.G., Modat, M., Chan, D., Ourselin, S., Barnes, J., Fox, N.C., Atrophy patterns in Alzheimer's disease and semantic dementia: a comparison of FreeSurfer and manual volumetric measurements. Neuroimage 49 (2010), 2264–2274.
41. LeMay, M., Radiologic changes of the aging brain and skull. Am. J. Roentgenol. 143 (1984), 383–389.
42. Long, X., Liao, W., Jiang, C., Liang, D., Qiu, B., Zhang, L., Healthy aging: an automatic analysis of global and regional morphological alterations of human brain. Acad. Radiol. 19 (2012), 785–793.
43. Madan, C.R., Creating 3D visualizations of MRI data: a brief guide. F1000Res., 4, 2015, 466.
44. Madan, C.R., Kensinger, E.A., Cortical complexity as a measure of age-related brain atrophy. Neuroimage 134 (2016), 617–629.
45. Mandelbrot, B.B., How long is the coast of Britain? Statistical self-similarity and fractional dimension. Science 156 (1967), 636–638.
46. Mandelbrot, B.B., The Fractal Geometry of Nature. 1982, W.H. Freeman, San Francisco.
47. Marcus, D.S., Wang, T.H., Parker, J., Csernansky, J.G., Morris, J.C., Buckner, R.L., Open Access Series of Imaging Studies (OASIS): cross-sectional MRI Data in young, middle aged, nondemented, and demented older adults. J. Cogn. Neurosci. 19 (2007), 1498–1507.
48. McKay, D.R., Knowles, E.E.M., Winkler, A.A.M., Sprooten, E., Kochunov, P., Olvera, R.L., Curran, J.E., Kent, J.W. Jr, Carless, M.A., Göring, H.H., Dyer, T.D., Duggirala, R., Almasy, L., Fox, P.T., Blangero, J., Glahn, D.C., Influence of age, sex and genetic factors on the human brain. Brain Imaging Behav. 8 (2014), 143–152.
49. Mulder, E.R., de Jong, R.A., Knol, D.L., van Schijndel, R.A., Cover, K.S., Visser, P.J., Barkhof, F., Vrenken, H., Alzheimer's Disease Neuroimaging Initiative. Hippocampal volume change measurement: quantitative assessment of the reproducibility of expert manual outlining and the automated methods FreeSurfer and FIRST. Neuroimage 92 (2014), 169–181.
50. Mustafa, N., Ahearn, T.S., Waiter, G.D., Murray, A.D., Whalley, L.J., Staff, R.T., Brain structural complexity and life course cognitive change. Neuroimage 61 (2012), 694–701.
51. Narr, K.L., Bilder, R.M., Kim, S., Thompson, P.M., Szeszko, P., Robinson, D., Luders, E., Toga, A.W., Abnormal gyral complexity in first-episode schizophrenia. Biol. Psychiatry 55 (2004), 859–867.
52. Nenadic, I., Yotter, R.A., Sauer, H., Gaser, C., Cortical surface complexity in frontal and temporal areas varies across subgroups of schizophrenia. Hum. Brain Mapp. 35 (2014), 1691–1699.
53. Nestor, S.M., Rupsingh, R., Borrie, M., Smith, M., Accomazzi, V., Wells, J.L., Fogarty, J., Bartha, R., Ventricular enlargement as a possible measure of Alzheimer's disease progression validated using the Alzheimer's disease neuroimaging initiative database. Brain 131 (2008), 2443–2454.
54. Palombo, D.J., Amaral, R.S.C., Olsen, R.K., Muller, D.J., Todd, R.M., Anderson, A.K., Levine, B., KIBRA polymorphism is associated with individual differences in Hippocampal subregions: evidence from anatomical segmentation using high-resolution MRI. J. Neurosci. 33 (2013), 13088–13093.
55. Pardoe H, R., Pell, G.S., Abbott, D.F., Jackson, G.D., Hippocampal volume assessment in temporal lobe epilepsy: How good is automated segmentation?. Epilepsia 50 (2009), 2586–2592.
56. Pienaar, R., Fischl, B., Caviness, V., Makris, N., Grant, P.E., A methodology for analyzing curvature in the developing brain from preterm to adult. Int. J. Imaging Syst. Technol. 18 (2008), 42–68.
57. Potvin, O., Mouiha, A., Dieumegarde, L., Duchesne, S., Normative data for subcortical regional volumes over the lifetime of the adult human brain. Neuroimage 137 (2016), 9–20.
58. Qiu, A., Zhong, J., Graham, S., Chia, M.Y., Sim, K., Combined analyses of thalamic volume, shape and white matter integrity in first-episode schizophrenia. Neuroimage 47 (2009), 1163–1171.
59. Raz, N., Lindenberger, U., Rodrigue, K.M., Kennedy, K.M., Head, D., Williamson, A., Dahle, C., Gerstorf, D., Acker, J.D., Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex 15 (2005), 1676–1689.
60. Raz, N., Rodrigue, K.M., Differential aging of the brain: patterns, cognitive correlates and modifiers. Neurosci. Biobehav. Rev. 30 (2006), 730–748.
61. Raz, N., Rodrigue, K.M., Head, D., Kennedy, K.M., Acker, J.D., Differential aging of the medial temporal lobe: a study of a five-year change. Neurology 62 (2004), 433–438.
62. Reagh, Z.M., Yassa, M.A., Object and spatial mnemonic interference differentially engage lateral and medial entorhinal cortex in humans. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), E4264–E4273.
63. Reuter, M., Wolter, F.-E., Peinecke, N., Laplace–Beltrami spectra as “Shape-DNA” of surfaces and solids. Comput. Aided Des. 38 (2006), 342–366.
64. Salat, D.H., Buckner, R.L., Snyder, A.Z., Greve, D.N., Desikan, R.S., Busa, E., Morris, J.C., Dale, A.M., Fischl, B., Thinning of the cerebral cortex in aging. Cereb. Cortex 14 (2004), 721–730.
65. Sandu, A.-L., Rasmussen, I.-A., Lundervold, A., Kreuder, F., Neckelmann, G., Hugdahl, K., Specht, K., Fractal dimension analysis of MR images reveals grey matter structure irregularities in schizophrenia. Comput. Med. Imaging Graph. 32 (2008), 150–158.
66. Sandu, A.-L., Staff, R.T., McNeil, C.J., Mustafa, N., Ahearn, T., Whalley, L.J., Murray, A.D., Structural brain complexity and cognitive decline in late life: a longitudinal study in the Aberdeen 1936 Birth Cohort. Neuroimage 100 (2014), 558–563.
67. Sargolzaei, S., Sargolzaei, A., Cabrerizo, M., Chen, G., Goryawala, M., Pinzon-Ardila, A., Gonzalez-Arias, S.M., Adjouadi, M., Estimating intracranial volume in brain research: an evaluation of methods. Neuroinformatics 13 (2015), 427–441.
68. Seo, S., Chung, M.K., Laplace-Beltrami eigenfunction expansion of cortical manifolds. IEEE Int. Symp. Biomed. Imaging 2011 (2011), 372–375.
69. Smith, M.J., Wang, L., Cronenwett, W., Goldman, M.B., Mamah, D., Barch, D.M., Csernansky, J.G., Alcohol use disorders contribute to hippocampal and subcortical shape differences in schizophrenia. Schizophr. Res. 131 (2011), 174–183.
70. Tae, W.S., Kim, S.S., Lee, K.U., Nam, E.-C., Kim, K.W., Validation of hippocampal volumes measured using a manual method and two automated methods (FreeSurfer and IBASPM) in chronic major depressive disorder. Neuroradiology 50 (2008), 569–581.
71. Tamnes, C.K., Walhovd, K.B., Dale, A.M., Østby, Y., Grydeland, H., Richardson, G., Westlye, L.T., Roddey, J.C., Hagler, D.J. Jr, Due-Tønnessen, P., Holland, D., Fjell, A.M., Alzheimer's Disease Neuroimaging Initiative. Brain development and aging: overlapping and unique patterns of change. Neuroimage 68 (2013), 63–74.
72. Tang, X., Holland, D., Dale, A.M., Younes, L., Miller, M.I., Shape abnormalities of subcortical and ventricular structures in mild cognitive impairment and Alzheimer's disease: detecting, quantifying, and predicting. Hum. Brain Mapp. 35 (2014), 3701–3725.
73. Thompson, P., Moussai, J., Zohoori, A., Khan, A.A., Mega, M.S., Cummings, J.L., Toga, A.W., Cortical variability and asymmetry in normal aging and Alzheimer's disease. Cereb. Cortex 8 (1998), 492–509.
74. Thompson, P.M., Schwartz, C., Lin, R.T., Khan, A.A., Toga, A.W., Three-dimensional statistical analysis of sulcal variability in the human brain. J. Neurosci. 16 (1996), 4261–4274.
75. Toro, R., Poline, J.-B., Huguet, G., Loth, E., Frouin, V., Banaschewski, T., Barker, G.J., Bokde, A., Büchel, C., Carvalho, F.M., Conrod, P., Fauth-Bühler, M., Flor, H., Gallinat, J., Garavan, H., Gowland, P., Heinz, A., Ittermann, B., Lawrence, C., Lemaître, H., Mann, K., Nees, F., Paus, T., Pausova, Z., Rietschel, M., Robbins, T., Smolka, M.N., Ströhle, A., Schumann, G., Bourgeron, T., IMAGEN Consortium. Genomic architecture of human neuroanatomical diversity. Mol. Psychiatry 20 (2014), 1011–1016.
76. van der Kouwe, A.J.W., Benner, T., Salat, D.H., Fischl, B., Brain morphometry with multiecho MPRAGE. Neuroimage 40 (2008), 559–569.
77. Wachinger, C., Golland, P., Kremen, W., Fischl, B., Reuter, M., BrainPrint: a discriminative characterization of brain morphology. Neuroimage 109 (2015), 232–248.
78. 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. Neurobiol. Aging 26 (2005), 1261–1270.
79. Walhovd, K.B., Westlye, L.T., Amlien, I., Espeseth, T., Reinvang, I., Raz, N., Agartz, I., Salat, D.H., Greve, D.N., Fischl, B., Dale, A.M., Fjell, A.M., Consistent neuroanatomical age-related volume differences across multiple samples. Neurobiol. Aging 32 (2011), 916–932.
80. Wenger, E., Mårtensson, J., Noack, H., Bodammer, N.C., Kühn, S., Schaefer, S., Heinze, H.J., Düzel, E., Bäckman, L., Lindenberger, U., Lövdén, M., Comparing manual and automatic segmentation of hippocampal volumes: reliability and validity issues in younger and older brains. Hum. Brain Mapp. 35 (2014), 4236–4248.
81. Wonderlick, J.S., Ziegler, D.A., Hosseini-Varnamkhasti, P., Locascio, J.J., Bakkour, A., van der Kouwe, A., Triantafyllou, C., Corkin, S., Dickerson, B.C., Reliability of MRI-derived cortical and subcortical morphometric measures: effects of pulse sequence, voxel geometry, and parallel imaging. Neuroimage 44 (2009), 1324–1333.
82. Yang, Z., Wen, W., Jiang, J., Crawford, J.D., Reppermund, S., Levitan, C., Slavin, M.J., Kochan, N.A., Richmond, R.L., Brodaty, H., Trollor, J.N., Sachdev, P.S., Age-associated differences on structural brain MRI in nondemented individuals from 71 to 103 years. Neurobiol. Aging 40 (2016), 86–97.
83. Yotter, R.A., Nenadic, I., Ziegler, G., Thompson, P.M., Gaser, C., Local cortical surface complexity maps from spherical harmonic reconstructions. Neuroimage 56 (2011), 961–973.
84. Yun, H.J., Im, K., Yang, Jin-Ju, Yoon, U., Lee, J.-M., Automated sulcal depth measurement on cortical surface reflecting geometrical properties of sulci. PLoS One, 8, 2013, e55977.
85. Yushkevich, P.A., Pluta, J.B., Wang, H., Xie, L., Ding, S.-L., Gertje, E.C., Mancuso, L., Kliot, D., Das, S.R., Wolk, D.A., Automated volumetry and regional thickness analysis of hippocampal subfields and medial temporal cortical structures in mild cognitive impairment. Hum. Brain Mapp. 36 (2015), 258–287.
86. Zhao, G., Denisova, K., Sehatpour, P., Long, J., Gui, W., Qiao, J., Javitt, D.C., Wang, Z., Fractal dimension analysis of subcortical gray matter structures in Schizophrenia. PLoS One, 11, 2016, e0155415.