Advertisement

Brain Structure and Function

, Volume 219, Issue 6, pp 2029–2049 | Cite as

Gray-matter macrostructure in cognitively healthy older persons: associations with age and cognition

  • Debra A. FleischmanEmail author
  • Sue Leurgans
  • Konstantinos Arfanakis
  • Zoe Arvanitakis
  • Lisa L. Barnes
  • Patricia A. Boyle
  • S. Duke Han
  • David A. Bennett
Original Article

Abstract

A deeper understanding of brain macrostructure and its associations with cognition in persons who are considered cognitively healthy is critical to the early detection of persons at risk of developing dementia. Few studies have examined the associations of all three gray-matter macrostructural brain indices (volume, thickness, surface area) with age and cognition, in the same persons who are over the age of 65 and do not have cognitive impairment. We performed automated morphometric reconstruction of total gray matter, cortical gray matter, subcortical gray matter and 84 individual regions in 186 persons (60 % over the age of 80) without cognitive impairment. Morphometric measures were scaled and expressed as difference per decade of age and an adjusted score was created to identify those regions in which there was greater atrophy per decade of age compared to cortical or subcortical brain averages. The results showed that there is substantial total volume loss and cortical thinning in cognitively healthy older persons. Thinning was more widespread than volume loss, but volume loss, particularly in temporoparietal and hippocampal regions, was more strongly associated with cognition.

Keywords

Aging Cognition MRI morphometry Volume Thickness Surface area 

Notes

Acknowledgments

This work was supported by National Institute on Aging grants R01AG17917, R01AG40039, R01AG34374 and K23AG40625, and by National Institute of Minority Health and Health Disparities grant P20MD6886 to Rush University Medical Center, the Illinois Department of Public Health, the Rush Translational Science Consortium and the Marsha K Dowd Philanthropic Fund. We are indebted to the altruism of the participants of the Rush Memory and Aging Project. We thank Lei Yu, Ph.D. for a critical reading of the statistical methods, Woojeong Bang, M.S. for statistical analyses and Niranjini Rajendran, M.S. for post-processing.

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Allen JS, Bruss J, Brown CK, Damasio H (2005) Normal neuroanatomical variation due to age: the major lobes and a parcellation of the temporal region. Neurobiol Aging 26:1245–1260PubMedCrossRefGoogle Scholar
  2. Bakkour A, Morris JC, Dickerson BC (2009) The cortical signature of prodromal AD: regional thinning predicts mild AD dementia. Neurology 72:1048–1055PubMedCentralPubMedCrossRefGoogle Scholar
  3. Barta P, Dazzan P (2003) Hemispheric surface area: sex, laterality and age effects. Cereb Cortex 13:364–370PubMedCrossRefGoogle Scholar
  4. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188CrossRefGoogle Scholar
  5. Bennett DA, Schneider JA, Buchman AS, Barnes LL, Boyle PA, Wilson RS (2012a) Overview and findings from the Rush Memory and Aging Project. Curr Alzheimer Res 9:646–663PubMedCentralPubMedCrossRefGoogle Scholar
  6. Bennett DA, Wilson RS, Boyle PA, Buchman AS, Schneider JA (2012b) Relation of neuropathology to cognition in persons without cognitive impairment. Ann Neurol 72:599–609PubMedCentralPubMedCrossRefGoogle Scholar
  7. Brickman AM, Habeck C, Zarahn E, Flynn J, Stern Y (2007) Structural MRI covariance patterns associated with normal aging and neuropsychological functioning. Neurobiol Aging 28:284–295PubMedCrossRefGoogle Scholar
  8. Buckner RL (2004) Memory and executive function in aging and AD: multiple factors that cause decline and reserve factors that compensate. Neuron 44:195–208PubMedCrossRefGoogle Scholar
  9. Burgmans S, van Boxtel MP, Vuurman EF, Smeets F, Gronenschild EH, Uylings HB, Jolles J (2009) The prevalence of cortical gray matter atrophy may be overestimated in the healthy brain. Neuropsychology 23:541–550PubMedCrossRefGoogle Scholar
  10. Chetelat G, Baron JC (2003) Early diagnosis of Alzheimer’s disease: contribution of structural neuroimaging. NeuroImage 18:525–541PubMedCrossRefGoogle Scholar
  11. Christensen H, McKinnon AJ, Korten AE, Jorm AF, Henderson AS, Jacomb P (1999) An analysis of diversity in the cognitive performance of elderly community dwellers: individual differences in change scores as a function of age. Psychol Aging 14:365–379PubMedCrossRefGoogle Scholar
  12. Cummings JL, Doody R, Clark C (2007) Disease-modifying therapies for Alzheimer’s disease: challenges to early intervention. Neurology 69:1622–1634PubMedCrossRefGoogle Scholar
  13. DeCarli C, Massaro J, Harvey D, Hald J, Tullberg M, Au R, Wolf PA (2005) Measures of brain morphology and infarction in the Framingham Heart Study: establishing what is normal. Neurobiol Aging 26:491–510PubMedCrossRefGoogle Scholar
  14. Den Heijer T, Geerlings MI, Hoebeek FE, Hofman A, Koudstaal PJ, Breteler MM (2006) Use of hippocampal and amygdalar volumes on magnetic resonance imaging to predict dementia in cognitive intact elderly people. Arch Gen Psychiatry 63:57–62CrossRefGoogle Scholar
  15. Destrieux C, Fischl B, Dale A, Halgren E (2010) Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 53:1–15PubMedCentralPubMedCrossRefGoogle Scholar
  16. Dickerson BC, Goncharova I, Sullivan MP, Forchetti C, Wilson RS, Bennett DA, Beckett LA, deToledo-Morrell L (2001) MRI-derived entorhinal and hippocampal atrophy in incipient and very mild Alzheimer's disease. Neurobiol Aging 22:747–754Google Scholar
  17. Dickerson BC, Wolk DA, The Alzheimer’s Disease Neuroimaging Initiative (2012) MRI cortical thickness biomarker predicts AD-like CSF and cognitive decline in normal adults. Neurology 78:84–90Google Scholar
  18. Dickerson BC, Bakkour A, Salat DH, Feczko E, Pacheco J, Greve DN, Grodstein F, Wright CI, Blacker D, Rosas HD, Sperling RA, Atri A, Growdon JH, Hyman BT, Morris JC, Fischl B, Buckner RL (2009a) The cortical signature of Alzheimer’s disease: regionally specific cortical thinning relates to symptom severity in very mild to mild AD dementia and is detectable in asymptomatic amyloid-positive individual. Cereb Cortex 19:497–510PubMedCentralPubMedCrossRefGoogle Scholar
  19. Dickerson BC, Feczko E, Augustinack JC, Pacheco J, Morris JC, Fischl B, Buckner RL (2009b) Differential effects of aging and Alzheimer’s disease on medial temporal lobe cortical thickness and surface area. Neurobiol Aging 30:432–440PubMedCentralPubMedCrossRefGoogle Scholar
  20. Dickerson BC, Stoub TR, Shah RC, Sperling RA, Killiany RJ, Albert MS, Hyman BT, Blacker D, deToledo-Morrell L (2011) Alzheimer-signature MRI biomarker predicts AD dementia in cognitively normal adults. Neurology 76:1395–1402PubMedCentralPubMedCrossRefGoogle Scholar
  21. Driscoll I, Davatzikos C, An Y, Wu X, Shen D, Kraut M, Resnick SM (2009) Longitudinal pattern of regional brain volume change differentiates normal aging from MCI. Neurology 72:1906–1913PubMedCentralPubMedCrossRefGoogle Scholar
  22. Du AT, Schuff N, Chao LL, Kornak J, Jagust WJ, Kramer JH, Reed BR, Miller BL, Norman D, Chui HC, Weiner MW (2006) Age effects on atrophy rates of entorhinal cortex and hippocampus. Neurobiol Aging 27:733–740PubMedCentralPubMedCrossRefGoogle Scholar
  23. Ecker C, Stahl D, Daly E, Johnston P, Thomson A, Murphy DGM (2009) Is there a common underlying mechanism for age-related decline in cortical thickness? NeuroReport 20:1155–1160PubMedCrossRefGoogle Scholar
  24. Finkel D, Reynolds CA, McArdle JJ, Pederson NL (2007) Age changes in processing speed as a leading indicator of cognitive aging. Psychol Aging 22:558–568PubMedCrossRefGoogle Scholar
  25. Fjell AM, Walhovd KB (2010) Structural brain changes in aging: courses, causes and cognitive consequences. Rev Neurosci 21:187–221PubMedCrossRefGoogle Scholar
  26. Fjell AM, Westlye LT, Amlien I, Espeseth T, Reinvang I, Raz N, Agartz I, Salat DH, Greve DN, Fischl B, Dale AM, Walhovd KB (2009a) High consistency of regional cortical thinning in aging across multiple samples. Cereb Cortex 19:2001–2012PubMedCentralPubMedCrossRefGoogle Scholar
  27. Fjell AM, Walhovd KB, Fennema-Notestine C, McEvoy LK, Hagler DJ, Holland D, Brewer JB, Dale AM (2009b) One-year brain atrophy evident in healthy aging. J Neurosci 29:15223–15231PubMedCentralPubMedCrossRefGoogle Scholar
  28. Fjell AM, Amlien IK, Westlye LT, Stenset V, Fladby T, Skinningsrud A, Eilsertsen DE, Bjornerud A, Walhovd KB (2010a) CSF biomarker pathology correlates with a medial temporo-parietal network affected by very mild to moderate Alzheimer’s disease but not a fronto-striatal network affected by healthy aging. NeuroImage 49:1820–1830PubMedCrossRefGoogle Scholar
  29. Fjell AM, Westlye LT, Espeseth T, Reinvang I, Walhovd KB, Dale AM, Holland D (2010b) Cortical gray matter atrophy in healthy aging cannot be explained by undetected incipient cognitive disorders: a comment on Burgmans (2009). Neuropsychology 24:258–266PubMedCentralPubMedCrossRefGoogle Scholar
  30. Fleischman DA, Arfanakis KA, Kelly JF, Rajendran N, Buchman AS, Morris MC, Barnes LL, Bennett DA (2010) Regional brain cortical thinning and systemic inflammation in older persons without dementia. JAGS 58:1823–1825CrossRefGoogle Scholar
  31. Fortea J, Sala-Llonch R, Bartres-Faz D, Bosch B, Llado A, Bargallo N, Molinuevo JL, Sanchez-Valle R (2010) Increased cortical thickness and caudate volume precede atrophy in PSEN1 mutation carriers. J Alzheimer’s Dis 22:909–922Google Scholar
  32. Fotenos AF, Mintun MA, Snyder AZ, Morris JC, Buckner RL (2008) Brain volume decline in aging: evidence for a relation between socioeconomic status, preclinical Alzheimer disease, and reserve. Arch Neurol 65:113–120PubMedCrossRefGoogle Scholar
  33. Golomb J, De Leon MJ, Kluger A, George AE, Tarshish C, Ferris SH (1993) Hippocampal atrophy in normal aging: an association with recent memory impairment. Arch Neurol 50:967–973PubMedCrossRefGoogle Scholar
  34. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) A voxel-based morphometric study of ageing in 464 normal adult human brains. NeuroImage 14:21–36PubMedCrossRefGoogle Scholar
  35. Hackert VH, den Heijer T, Oudkerk M, Koudstaal PJ, Hofman A, Breteler MM (2002) Hippocampal head size associated with verbal memory performance in nondemented elderly. Neuroimage 17:1365–1372PubMedCrossRefGoogle Scholar
  36. Harris JA, Petersen RS, Diamond ME (2001) The cortical distribution of sensory mechanisms. Neuron 30:315–318PubMedCrossRefGoogle Scholar
  37. Head D, Snyder AZ, Girton E, Morris JC, Buckner RL (2005) Frontal-hippocampal double dissociation between normal aging and Alzheimer’s disease. Cereb Cortex 15:732–739PubMedCrossRefGoogle Scholar
  38. Head D, Rodrigue KM, Kennedy KM, Raz N (2008) Neuroanatomical and cognitive mediators of age-related differences in episodic memory. Neuropsychology 22:491–507PubMedCentralPubMedCrossRefGoogle Scholar
  39. Hedden T, Gabrieli JDE (2004) Insights into the ageing mind: a view from cognitive neuroscience. Nat Neurosci Rev 5:87–97CrossRefGoogle Scholar
  40. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  41. Hutton C, Draganski B, Ashburner J, Weiskopf N (2009) A comparison between voxel-based cortical thickness and voxel-based morphometry in normal aging. NeuroImage 48:371–380PubMedCentralPubMedCrossRefGoogle Scholar
  42. Iacono D, O’Brien R, Resnick SM, Zonderman AB, Pletnikova O, Rudow G, An Y, West MJ, Crain B, Troncoso JC (2008) Neuronal hypertrophy in asymptomatic Alzheimer disease. J Neuropathol Exp Neurol 67:578–589PubMedCentralPubMedCrossRefGoogle Scholar
  43. Jack CR Jr, Petersen RC, Xu YC, Waring SC, O’Brien PC, Tangalos EG, Smith GE, Ivnik RJ, Kokmen E (1997) Medial temporal atrophy on MRI in normal aging and very mild Alzheimer’s disease. Neurology 49:786–794PubMedCentralPubMedCrossRefGoogle Scholar
  44. Jee GC, Dooling EC, Gilles FH (1977) Gyral development of the human brain. Ann Neurol 1:86–93CrossRefGoogle Scholar
  45. Jernigan TL, Archibald SL, Fennema-Notestine C, Gamst AC, Stout JC, Bonner J, Hesselink JR (2001) Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol Aging 22:581–594PubMedCrossRefGoogle Scholar
  46. Kalpouzos G, Chetelat G, Baron JC, Landeau B, Mevel K, Godeau C, Barre L, Constans JM, Viader F, Eustache F, Desgranges B (2009) Voxel-based mapping of brain gray matter volume and glucose metabolism profiles in normal aging. Neurobiol Aging 30:112–124PubMedCrossRefGoogle Scholar
  47. Kaye JA, Swihart T, Howieson D, Dame A, Moore MM, Karnos T, Camicioli R, Ball M, Oken B, Sexton G (1997) Volume loss of the hippocampus and temporal lobe in healthy elderly persons destined to develop dementia. Neurology 48:1297–1304PubMedCrossRefGoogle Scholar
  48. Kochunov P, Robin DA, Royall DR, Coyle T, Lancaster J, Kochunov V, Schlosser AE, Fox PT (2009) Can structural MRI indices of cerebral integrity track cognitive trends in executive control function during normal maturation and adulthood? Hum Brain Mapp 30:2581–2594PubMedCentralPubMedCrossRefGoogle Scholar
  49. Kramer JH, Mungas D, Reed BR, Wetzel ME, Burnett MM, Miller BL, Weiner MW, Chui HC (2007) Longitudinal MRI and cognitive change in healthy elderly. Neuropsychology 21:412–418PubMedCentralPubMedCrossRefGoogle Scholar
  50. Lee GJ, Po HL, Medina LD, Rodriguez-Agudelo Y, Melchor S, Coppola G, Braskie MN, Hua X, Apostolova LG, Leow AD, Thompson PM, Ringman JM (2012) Regional brain volume differences in symptomatic and presymptomatic carriers of familial Alzheimer’s disease mutations. J Neurol Neurosurg Psychiatry 84:154–162PubMedCentralPubMedCrossRefGoogle Scholar
  51. 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 26:900–911PubMedCrossRefGoogle Scholar
  52. Lemaitre H, Goldman AL, Sambataro F, Verchinski BA, Meyer-Lindenberg A, Weinberger, Mattay VS (2012) Normal age-related brain morphometric changes: nonuniformity across cortical thickness, surface area and gray matter volume? Neurobiol Aging 33:e1–e9 Epub 2010 Aug 23PubMedCrossRefGoogle Scholar
  53. MacPherson SE, Phillips LH, Della Sala S (2002) Age, executive function and social decision making: a dorsolateral prefrontal theory of cognitive aging. Psychol Aging 17:598–609PubMedCrossRefGoogle Scholar
  54. Magnotta VA, Andreasen NC, Schultz SK, Harris G, Cizadlo T, Heckel D, Nopoulos P, Flaum M (1999) Quantitative in vivo measurement of gyrification in the human brain: changes associated with aging. Cereb Cortex 9:151–160PubMedCrossRefGoogle Scholar
  55. Mu Q, Xie J, Wen Z, Weng Y, Shuyun Z (1999) A quantitative MR study of the hippocampal formation, the amygdala, and the temporal horn of the lateral ventricle in healthy subjects 40 to 90 years of age. AJNR 20:207–211PubMedGoogle Scholar
  56. Murphy EA, Holland D, Donohue M, McEvoy LK, Hagler DJ Jr, Dale AM, Brewer JB, The Alzheimer’s Disease Neuroimaging Initiative (2010) Six-month atrophy in MTL structures is associated with subsequent memory decline in elderly controls. NeuroImage 53:1310–1317PubMedCentralPubMedCrossRefGoogle Scholar
  57. Panizzon MS, Fennema-Notestine C, Eyler LT, Jernigan TL, Prom-Wormley E, Neale M, Jacobson K, Lyons MJ, Grant MD, Franz CE, Xian H, Tsuang M, Fischl B, Seidman L, Dale A, Kremen WS (2009) Distinct genetic influences on cortical surface area and cortical thickness. Cereb Cortex 19:2728–2735PubMedCentralPubMedCrossRefGoogle Scholar
  58. Prull MW, Gabrieli JDE, Bunge SM (2000) Age-related changes in memory: a cognitive neuroscience perspective. In: Craik FIM, TA Salthouse (eds) Handbook of aging and cognition, vol 2. Erlbaum, Mahweh, pp 91–153Google Scholar
  59. Raji CA, Lopez L, Kuller LH, Carmichael OT, Becker JT (2009) Age, Alzheimer disease, and brain structure. Neurology 73:1899–1905PubMedCentralPubMedCrossRefGoogle Scholar
  60. Raz N (1996) Neuroanatomy of the aging brain: Evidence from structural MRI. In: Bigler ED (ed) Neuroimaging II: clinical applications. Plenum, New York, pp 153–182CrossRefGoogle Scholar
  61. Raz N (2001) Ageing and the Brain. Encyclopedia of Life Sciences, LondonGoogle Scholar
  62. Raz N, Rodrigue KM (2006) Differential aging of the brain: patterns, cognitive correlates and modifiers. Neurosci Biobehav Rev 30:730–748PubMedCrossRefGoogle Scholar
  63. Raz N, Gunning FM, Head D, Dupuis JH, McQuain J, Briggs SD, Loken WJ, Thornton AE, Acker JD (1997) Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cereb Cortex 7:268–282PubMedCrossRefGoogle Scholar
  64. Raz N, Gunning-Dixon FM, Head DP, Dupuis JH, Acker JD (1998) Neuroanatomical correlates of cognitive aging: evidence from structural magnetic resonance imaging. Neuropsychology 12:95–114PubMedCrossRefGoogle Scholar
  65. Raz N, Rodrigue KM, Kennedy KM, Head D, Gunning-Dixon F, Acker JD (2003) Differential aging of the human striatum: longitudinal evidence. Am J Neuroradiol 24:1849–1856PubMedGoogle Scholar
  66. Raz N, Lindenberger U, Rodrigue KM, Kennedy M, Head D, Williamson A, Dahle C, Gerstorf D, Acker JD (2005) Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 15:1676–1689PubMedCrossRefGoogle Scholar
  67. Raz N, Lindenberger U (2011) Only time will tell: Cross-sectional studies offer no solution to the age-brain-cognition triangle: Comment on Salthouse (2011). Psychol Bull 137:790–795Google Scholar
  68. Resnick SM, Goldszal AF, Davatzikos C, Golski S, Kraut MA, Metter EJ, Bryan RN, Zonderman AB (2000) One-year age changes in MRI brain volumes in older adults. Cereb Cortex 10:464–472PubMedCrossRefGoogle Scholar
  69. Resnick SM, Pham DL, Kraut MA, Zonderman AB, Davatzikos C (2003) Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J Neurosci 23:3295–3301PubMedGoogle Scholar
  70. Rettmann ME, Kraut MA, Prince JL, Resnick SM (2006) Cross-sectional and longitudinal analyses of anatomical sulcal changes associated with aging. Cereb Cortex 16:1584–1594PubMedCrossRefGoogle Scholar
  71. Riudavets MA, Iacono D, Resnick SM, O’Brien R, Zonderman AB, Martin LJ, Rudow G, Pletnikova O, Troncoso JC (2007) Resistance to Alzheimer’s pathology is associated with nuclear hypertrophy in neurons. Neurobiol Aging 28:1484–1492PubMedCentralPubMedCrossRefGoogle Scholar
  72. Rusinek H, De Santi S, Frid D, Tsui W-H, Tarshish CY, Convit A, de Leon MJ (2003) Regional brain atrophy rate predicts future cognitive decline: 6-year longitudinal MR imaging study of normal aging. Radiology 229:691–696PubMedCrossRefGoogle Scholar
  73. Salat DH, Buckner RL, Snyder AZ, Greve DN, Desikan RS, Busa E, Morris JC, Dale AM, Fischl B (2004) Thinning of the cerebral cortex in aging. Cereb Cortex 14:721–730PubMedCrossRefGoogle Scholar
  74. Salthouse TA (2000) Aging and measures of processing speed. Biol Psychiatry 54:35–54CrossRefGoogle Scholar
  75. Salthouse TA (2010) Major issues in cognitive aging. Oxford University Press, New YorkGoogle Scholar
  76. Salthouse TA (2011) Neuroanatomical substrates of age-related cognitive decline. Psychol Bull 137:753–784PubMedCentralPubMedCrossRefGoogle Scholar
  77. SAS Institute Inc. SAS.STAT ® 9.3 User’s Guide (2012) SAS Institute Inc. Cary NCGoogle Scholar
  78. Scahill RI, Fros C, Jenkins R, Whitwell JL, Rossor MN, Fox NC (2003) A longitudinal study of brain volume changes in normal aging using serial registered magnetc resonance imaging. Arch Neurol 60:989–994PubMedCrossRefGoogle Scholar
  79. Schmidt R, Ropele S, Enzinger C, Petrovic K, Smith S, Schmidt H, Matthews PM, Fazekas F (2005) White matter lesion progression, brain atrophy, and cognitive decline: The Austrian Stroke Prevention Study. Ann Neurol 58:610–616PubMedCrossRefGoogle Scholar
  80. Schretlen D, Pearlson GD, Anthony JC, Aylward EH, Augustine AM, Davis A, Barta P (2000) Elucidating the contributions of processing speed, executive ability, and frontal lobe volume to normal age-related differences in fluid intelligence. J Int Neuropsychol Soc 6:52–61PubMedGoogle Scholar
  81. Sloane PD, Zimmerman S, Suchindran C, Reed P, Wang L, Boustani M, Sudha S (2002) The public health impact of Alzheimer's disease, 2000-2050: potential implication of treatment advances. Ann Rev Public Health 23:213–231Google Scholar
  82. Smith CD, Chebrolu H, Wekstein DR, Schmitt FA, Jicha GA, Cooper G, Markesbery WR (2007) Brain structural alterations before mild cognitive impairment. Neurology 68:1268–1273PubMedCrossRefGoogle Scholar
  83. Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, Iwatsubo T, Jack CR Jr, Kaye J, Montine TJ, Park DC, Reiman EM, Rowe CC, Siemers E, Stern Y, Yaffe K, Carrillo MC, Thies B, Morrison-Bogorad M, Wagster MV, Phelps CH (2011) Toward defining the preclinical stages of Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7:280–292PubMedCentralPubMedCrossRefGoogle Scholar
  84. Su L, Wang L, Chen F, Shen H, Li B, Hu D (2012) Sparse representation of brain aging: extracting covariance patterns from structural MRI. PLoS ONE 7:e36147PubMedCentralPubMedCrossRefGoogle Scholar
  85. Sullivan EV, Deshmukh A, Desmond JE, Lim KO, Pfefferbaum A (2000) Cerebellar volume decline in normal aging, alcoholism, and Korsakoff’s syndrome: relation to ataxia. Neuropsychology 14:341–352PubMedCrossRefGoogle Scholar
  86. Sullivan EV, Rosenbloom M, Serventi KL, Pfefferbaum A (2004) Effects of age and sex on the volumes of thalamus, pons and cortex. Neurobiol Aging 25:185–192PubMedCrossRefGoogle Scholar
  87. Thambisetty M, Wan J, Carass A, An Y, Prince JL, Resnick SM (2010) Longitudinal changes in cortical thickness associated with normal aging. NeuroImage 52:1215–1223PubMedCentralPubMedCrossRefGoogle Scholar
  88. Tisserand DJ, Visser PJ, van Boxtel MPJ, Jolles J (2000) The relation between global and limbic brain volumes on MRI and cognitive performance in healthy individuals across the age range. Neurobiol Aging 21:569–576PubMedCrossRefGoogle Scholar
  89. Tisserand DJ, Pruessner JC, Sanz Arigita EJ, van Boxtel MP, Evans AC, Jolles J, Uylings HB (2002) Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approach and voxel-based morphometry. Neuroimage 17:657–669PubMedCrossRefGoogle Scholar
  90. Tisserand DJ, van Boxtel MPJ, Pruessner JC, Hofman P, Evans AC, Jolles J (2004) A voxel-based morphometric study to determine individual differences in gray matter density associated with age and cognitive change over time. Cereb Cortex 14:966–973PubMedCrossRefGoogle Scholar
  91. Tupler LA, Krishnan KRR, Greenberg DL, Marcovina SM, Payne ME, MacFall JR, Charles HC, Doraiswamy PM (2007) Predicting memory decline in normal elderly: genetics MRI and cognitive reserve. Neurobiol Aging 28:1644–1656PubMedCrossRefGoogle Scholar
  92. Van Der Werf YD, Tisserand DJ, Visser PJ, Hofman PA, Vuurman E, Uylings HB, Jolles J (2001) Thalamic volume predicts performance on tests of cognitive speed and decreases in healthy aging. A magnetic resonance imaging-based volumetric analysis. Brain Res Cogn Brain Res 11:377–385CrossRefGoogle Scholar
  93. Van Petten C (2004) Relationship between hippocampal volume and memory ability in healthy individual across the lifespan: review and meta-analysis. Neuropsychologia 42:1394–1413PubMedCrossRefGoogle Scholar
  94. Walhovd KB, Fjell AM, Reinvang I, Lundervold A, Dale AM, Eilertsen DE, Quinn BT, Salat D, Makris N, Fischl B (2005) Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol Aging 26:1261–1270PubMedCrossRefGoogle Scholar
  95. Walhovd KB, Westlye LT, Amlien I, Espesth T, Reinvang I, Raz N, Agartz I, Salat DH, Greve DN, Fischl B, Dale AM, Fjell AM (2011) Consistent neuroanatomical age-related volume differences across multiple samples. Neurobiol Ag 32:916–932CrossRefGoogle Scholar
  96. Wheeler ME, Petersen SE, Buckner RL (2000) Memory’s echo: vivid remembering reactivates sensory-specific cortex. Proc Natl Acad Sci 97:11125–11129PubMedCentralPubMedCrossRefGoogle Scholar
  97. Wilson RS, Beckett LA, Barnes LL, Schneider JA, Bach J, Evans DA, Bennett DA (2002) Individual differences in rates of change in cognitive abilities of older persons. Psychol Aging 17:179–193PubMedCrossRefGoogle Scholar
  98. Zimmerman ME, Paul RH, Tate DF, Cohen RA, Williams LM, Whitford TJ (2006) The relationship between frontal gray matter volume and cognition varies across the healthy adult lifespan. Am J Geriatr Psychiatry 14:823–833PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Debra A. Fleischman
    • 1
    • 2
    • 3
    Email author
  • Sue Leurgans
    • 1
    • 2
    • 4
  • Konstantinos Arfanakis
    • 1
    • 5
    • 6
  • Zoe Arvanitakis
    • 1
    • 2
  • Lisa L. Barnes
    • 1
    • 2
    • 3
  • Patricia A. Boyle
    • 1
    • 3
  • S. Duke Han
    • 1
    • 3
    • 7
  • David A. Bennett
    • 1
    • 2
  1. 1.Rush Alzheimer’s Disease CenterRush University Medical CenterChicagoUSA
  2. 2.Neurological SciencesRush University Medical CenterChicagoUSA
  3. 3.Behavioral SciencesRush University Medical CenterChicagoUSA
  4. 4.Preventive MedicineRush University Medical CenterChicagoUSA
  5. 5.Diagnostic Radiology and Nuclear MedicineRush University Medical CenterChicagoUSA
  6. 6.Department of Biomedical EngineeringIllinois Institute of TechnologyChicagoUSA
  7. 7.VA Long Beach Healthcare System Long BeachLong BeachUSA

Personalised recommendations