Neurobiology of Aging
Volume 30, Issue 1 , Pages 112-124 , January 2009

Voxel-based mapping of brain gray matter volume and glucose metabolism profiles in normal aging

  • Grégoria Kalpouzos

      Affiliations

    • Inserm-EPHE-Université de Caen/Basse-Normandie, Unité de Recherche E0218, GIP Cyceron, Caen, France
    • ,
  • Gaël Chételat

      Affiliations

    • Inserm-EPHE-Université de Caen/Basse-Normandie, Unité de Recherche E0218, GIP Cyceron, Caen, France
    • ,
  • Jean-Claude Baron

      Affiliations

    • Inserm, U 320, GIP Cyceron, Caen, France
    • University of Cambridge, Department of Neurology, Cambridge, UK
    • ,
  • Brigitte Landeau

      Affiliations

    • Inserm-EPHE-Université de Caen/Basse-Normandie, Unité de Recherche E0218, GIP Cyceron, Caen, France
    • ,
  • Katell Mevel

      Affiliations

    • Inserm-EPHE-Université de Caen/Basse-Normandie, Unité de Recherche E0218, GIP Cyceron, Caen, France
    • ,
  • Christine Godeau

      Affiliations

    • Inserm, U 320, GIP Cyceron, Caen, France
    • ,
  • Louisa Barré

      Affiliations

    • UMR CEA 2, FRE CNRS 2698, GIP Cyceron, Caen, France
    • ,
  • Jean-Marc Constans

      Affiliations

    • CHU Côte de Nacre, Unité de neuroradiologie, Caen, France
    • ,
  • Fausto Viader

      Affiliations

    • Inserm-EPHE-Université de Caen/Basse-Normandie, Unité de Recherche E0218, GIP Cyceron, Caen, France
    • CHU Côte de Nacre, Service de neurologie Vastel, Caen, France
    • ,
  • Francis Eustache

      Affiliations

    • Inserm-EPHE-Université de Caen/Basse-Normandie, Unité de Recherche E0218, GIP Cyceron, Caen, France
    • ,
  • Béatrice Desgranges

      Affiliations

    • Inserm-EPHE-Université de Caen/Basse-Normandie, Unité de Recherche E0218, GIP Cyceron, Caen, France
    • Corresponding Author InformationCorresponding author at: Inserm-EPHE-Université de Caen/Basse-Normandie, Unité de Recherche E0218, Laboratoire de Neuropsychologie, CHU Côte de Nacre, 14033 Caen Cedex, France. Tel.: +33 2 31 06 51 95; fax: +33 2 31 06 51 98.

Received 3 August 2006 ,Revised 4 May 2007 ,Accepted 21 May 2007.

References 

  1. Abe O, Yamasue H, Aoki S, Suga M, Yamada H, Kasai K, et al. Aging in the CNS: comparison of gray/white matter volume and diffusion tensor data. Neurobiol. Aging. 2006;(Ahead of print)
  2. Allen JS, Bruss J, Brown CK, Damasio H. Normal neuroanatomical variation due to age: the major lobes and a parcellation of the temporal region. Neurobiol. Aging. 2005;26:1245–1260
  3. Baron JC, Godeau C. Human aging. In:  Mazziotta JC,  Toga A editor. Brain Mapping: The Systems. San Diego: Academic Press; 2000;p. 591–604
  4. Baron JC, Chételat G, Desgranges B, Perchey G, Landeau B, de la Sayette V, et al. In vivo mapping of gray matter loss with voxel-based morphometry in mild Alzheimer's disease. Neuroimage. 2001;14:298–309
  5. Beason-Held LL, Kraut MA, Resnick SM. I: Longitudinal changes in aging brain function. Neurobiol. Aging. 2008;29:483–496
  6. Beason-Held LL, Kraut MA, Resnick SM. II: Temporal patterns of longitudinal change in aging brain function. Neurobiol. Aging. 2008;29:497–513
  7. Bernard F, Desgranges B, Eustache F, Baron JC. Neural correlates of age-related verbal episodic memory decline: a PET study with combined subtraction/correlation analysis. Neurobiol. Aging. 2006;(Ahead of print)
  8. Bigler ED, Blatter DD, Anderson CV, Johnson SC, Gale SD, Hopkins RO, et al. Hippocampal volume in normal aging and traumatic brain injury. Am. J. Neuroradiol. 1997;18:11–23
  9. Buckner RL. Memory and executive function in aging and AD: multiple factors that cause decline and reserve factors that compensate. Neuron. 2004;44:195–208
  10. Cabeza R. Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol. Aging. 2002;17:85–100
  11. Cabeza R, Nyberg L. Imaging cognition II: an empirical review of 275 PET and fMRI studies. J. Cogn. Neurosci. 2000;12:1–47
  12. Calautti C, Serrati C, Baron JC. Effects of age on brain activation during auditory-cued thumb-to-index opposition. Stroke. 2001;32:139–146
  13. Cardebat D, Doyon B, Puel M, Goulet P, Joanette Y. Evocation lexicale formelle et sémantique chez des sujets normaux: performances et dynamiques de production en fonction du sexe, de l’âge et du niveau d’étude. Acta Neurol. Belg. 1990;90:207–217
  14. Chételat G, Desgranges B, de la Sayette V, Viader F, Eustache F, Baron JC. Mapping gray matter loss with voxel-based morphometry in mild cognitive impairment. Neuroreport. 2002;13:1939–1943
  15. Chételat G, Desgranges B, de la Sayette V, Viader F, Berkouk K, Landeau B, et al. Dissociating atrophy and hypometabolism impact on episodic memory in mild cognitive impairment. Brain. 2003;126:1955–1967
  16. Chugani HT. A critical period of brain development: studies of cerebral glucose utilization with PET. Prev. Med. 1998;27:184–188
  17. Cohen RM, Szczepanik J, McManus M, Mirza N, Putnam K, Levy J, et al. Hippocampal atrophy in the healthy is initially linear and independent of age. Neurobiol. Aging. 2006;27:1385–1394
  18. Collignon A, Maes F, Delaere D, Vandermeulen D, Suetens P, Marchal G. Automated multi-modality image registration based on information theory. In: Bizais , Barillot , Di Paola  editor. Information Processing in Medical Imaging. Dordrecht, The Netherlands: Kluwer Academic Publishers; 1995;p. 263–274
  19. Delacourte A, David JP, Sergeant N, Buée L, Wattez A, Vermersch P, et al. The biochemical pathway of neurofibrillary degeneration in aging and Alzheimer's disease. Neurology. 1999;52:1156–1165
  20. Desgranges B, Baron JC, Eustache F. The functional neuroanatomy of episodic memory: the role of the frontal lobes, the hippocampal formation, and other areas. Neuroimage. 1998;8:198–213
  21. Desgranges B, Baron JC, Lalevée C, Giffard B, Viader F, de la Sayette V, et al. The neural substrates of episodic memory impairment in Alzheimer's disease as revealed by FDG-PET: relationship to degree of deterioration. Brain. 2002;125:1116–1124
  22. Desgranges B, Baron JC, Giffard B, Chételat G, Lalevée C, Viader F, et al. The neural basis of intrusions in free recall and cued recall: a PET study in Alzheimer's disease. Neuroimage. 2002;17:1658–1664
  23. Dickerson BC, Salat DH, Greve DN, Chua EF, Rand-Giovannetti E, Rentz DM, et al. Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology. 2005;65:404–411
  24. Driscoll I, Hamilton DA, Petropoulos H, Yeo RA, Brooks WM, Baumgartner RN, et al. The aging hippocampus: cognitive, biochemical and structural findings. Cereb. Cortex. 2003;13:1344–1351
  25. Eustache F, Desgranges B, Lalevée C. L’évaluation clinique de la mémoire. Revue Neurologique (Paris). 1998;154:18–32
  26. Eustache F, Desgranges B, Giffard B, de la Sayette V, Baron JC. Entorhinal cortex disruption causes memory deficit in early Alzheimer's disease as shown by PET. Neuroreport. 2001;12:683–685
  27. Fotenos AF, Snyder AZ, Girton LE, Morris JC, Buckner RL. Normative estimates of cross-sectional and longitudinal brain volume decline in aging and AD. Neurology. 2005;64:1032–1039
  28. Garraux G, Salmon E, Degueldre C, Lemaire C, Laureys S, Franck G. Comparison of impaired subcortico-frontal metabolic networks in normal aging, subcortico-frontal dementia, and cortical frontal dementia. Neuroimage. 1999;10:149–162
  29. Good CD, Johnsrude IS, Ashburner J, Henson RNA, Friston KJ, Frackowiak RSJ. A voxel-based morphometric study of aging in 465 normal adult human brains. Neuroimage. 2001;14:21–36
  30. Grady CL. Functional brain imaging and age-related changes in cognition. Biol. Psychol. 2000;54:259–281
  31. Grieve SM, Clark CR, Williams LM, Peduto AJ, Gordon E. Preservation of limbic and paralimbic structures in aging. Hum. Brain Mapp. 2005;25:391–401
  32. Herholz K, et al. Discrimination between Alzheimer dementia and controls by automated analysis of multicenter FDG PET. Neuroimage. 2002;17:302–316
  33. Ibanez V, Pietrini P, Furey ML, Alexander GE, Millet P, Bokde ALW, et al. Resting state glucose metabolism is not reduced in normotensive healthy men during aging, after correction for brain atrophy. Brain Res. Bull. 2004;63:147–154
  34. Jernigan TL, Archibald SL, Fennema-Notestine C, Gamst AC, Stout JC, Bonner J, et al. Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol. Aging. 2001;22:581–594
  35. Jernigan TL, Gamst AC. Changes in volume with age-consistency and interpretation of observed effects. Neurobiol. Aging. 2005;26:1271–1274
  36. Kantarci K, Jack CR. Neuroimaging in Alzheimer disease: an evidence-based review. Neuroimaging Clin. N. Am. 2003;13:197–209
  37. Lehmbeck JT, Brassen S, Weber-Fahr W, Braus DF. Combining voxel-based morphometry and diffusion tensor imaging to detect age-related brain changes. Neuroreport. 2006;17:467–470
  38. Lemaître H, Crivello F, Grassiot B, Alpérovitch A, Tzourio C, Mazoyer B. Age- and sex-related effects on the neuroanatomy of healthy elderly. Neuroimage. 2005;26:900–911
  39. Lepage M, Habib R, Tulving E, Hippocampal . PET activations of memory encoding and retrieval: the HIPER model. Hippocampus. 1998;8:313–322
  40. Liu RSN, Lemieux L, Bell GS, Sisodiya SM, Shorvon SD, Sander JWAS, et al. A longitudinal study of brain morphometrics using quantitative magnetic resonance imaging and difference image analysis. Neuroimage. 2003;20:22–33
  41. Lupien SJ, Evans A, Lord C, Miles J, Pruessner M, Pike B, et al. Hippocampal volume is as variable in young as in older adults: implications for the notion of hippocampal atrophy in humans. Neuroimage. 2007;34:479–485
  42. Martin AJ, Friston KJ, Colebatch JG, Frackowiak RSJ. Decreases in regional cerebral blood flow with normal aging. J. Cereb. Blood Flow Metab. 1991;11:684–689
  43. Matsuda H, Kitayama N, Ohnishi T, Asada T, Nakano S, Sakamoto S, et al. Longitudinal evaluation of both morphologic and functional changes in the same individuals with Alzheimer's disease. J. Nucl. Med. 2002;43:304–311
  44. Matsuda H, Ohnishi T, Asada T, Li Z, Kanetaka H, Imabayashi E, et al. Correction for partial-volume effects on brain perfusion SPECT in healthy men. J. Nucl. Med. 2003;44:1243–1252
  45. Mattis S. Mental status examination for organic mental syndrome in the elderly patient. In:  Bellack L,  Karasu TB editor. Mental Status Examination for Organic Mental Syndrome in the Elderly Patients. New York: Grune & Stratton; 1976;p. 77–101
  46. Meguro K, Constans JM, Courtheoux P, Theron J, Viader F, Yamadori A. Atrophy of the corpus callosum correlates with white matter lesions in patients with cerebral ischaemia. Neuroradiology. 2000;42:416–419
  47. Meltzer CC, Becker JT, Price JC, Moses-Kolko E. Positron emission tomography imaging of the aging brain. Neuroimaging Clin. N. Am. 2003;13:759–767
  48. Meltzer CC, Cantwell MN, Greer PJ, Ben-Eliezer D, Smith G, Frank G, et al. Does cerebral blood flow decline in healthy aging? A PET study with partial-volume correction. J. Nucl. Med. 2000;41:1842–1848
  49. Moeller JR, Ishikawa T, Dhawan V, Spetsieris P, Mandel F, Alexander GE, et al. The metabolic topography of normal aging. J. Cereb. Blood Flow Metab. 1996;16:385–398
  50. Morcom A, Good C, Frackowiak R, Rugg M. Age effects on the neural correlates of successful memory encoding. Brain. 2003;126:213–229
  51. Mosconi L, Tsui WH, De Santi S, Li J, Rusinek H, Convit A, et al. Reduced hippocampal metabolism in MCI and AD: automated FDG-PET image analysis. Neurology. 2005;64:1860–1867
  52. Müller-Gärtner HW, Links JM, Prince JL, Bryan RN, McVeigh E, Leal JP, et al. Measurement of radiotracer concentration in brain gray matter using positron emission tomography: MRI-based correction for partial volume effects. J. Cereb. Blood Flow Metab. 1992;12:571–583
  53. Nestor PJ, Fryer TD, Ikeda M, Hodges JR. Retrosplenial cortex (BA29/30) hypometabolism in mild cognitive impairment (prodromal Alzheimer's disease). Eur. J. Neurosci. 2003;18:1–5
  54. Pantano P, Baron JC, Lebrun-Grandie P, Duquesnoy N, Bousser MG, Comar D. Regional cerebral blood flow and oxygen consumption in human aging. Stroke. 1984;15:635–641
  55. Pariente J, Cole S, Henson R, Clare L, Kennedy A, Rossor M, et al. Alzheimer's patients engage an alternative network during a memory task. Ann. Neurol. 2005;58:870–879
  56. Park DC, Gutchess AH. Aging, cognition, and culture: a neuroscientific perspective. Neurosci. Biobehav. Rev. 2002;26:859–867
  57. Persson J, Nyberg L. Altered brain activity in healthy seniors: what does it mean?. Prog. Brain Res. 2006;157:45–56
  58. Petit-Taboué MC, Landeau B, Desson JF, Desgranges B, Baron JC. Effects of healthy aging on the regional cerebral metabolic rate of glucose assessed with statistical parametric mapping. Neuroimage. 1998;7:176–184
  59. Pfefferbaum A, Sullivan EV, Rosenbloom MJ, Mathalon DH, Lim KO. A controlled study of cortical gray matter and ventricular changes in alcoholic men over a 5-year interval. Arch. Gen. Psychiatry. 1998;55:905–912
  60. Prayer D, Kasprian G, Krampl E, Ulm B, Witzani L, Prayer L, et al. MRI of normal fetal brain development. Eur. J. Radiol. 2006;57:199–216
  61. Quarantelli M, Berkouk K, Prinster A, Landeau B, Svarer C, Balkay L, et al. Integrated software for the analysis of brain PET/SPECT studies with partial-volume-effect correction. J. Nucl. Med. 2004;45:192–201
  62. Rados M, Judas M, Kostovic I. In vitro MRI of brain development. Eur. J. Radiol. 2006;57:187–198
  63. Raz N. Ageing and the brain. Encyclopedia of Life Sciences. London: Nature Publishing Group; 2001;
  64. Raz N. Aging of the brain and its impact on cognitive performance: integration of structural and functional findings. In:  Craik FIM,  Salthouse TA editor. Handbook of Aging and Cognition—II. Mahwah, NJ: Erlbaum; 2000;p. 1–90
  65. Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, Williamson A, et al. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex. 2005;15:1676–1689
  66. Raz N, Gunning-Dixon F, Head D, Rodrigue KM, Williamson A, Acker JD. Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume. Neurobiol. Aging. 2004;25:377–396
  67. Raz N, Rodrigue KM, Head D, Kennedy KM, Acker JD. Differential aging of the medial temporal lobe: a study of a five-year change. Neurology. 2004;62:433–438
  68. Raz N, Gunning FM, Head D, Dupuis JH, McQuain J, Briggs SD, et al. Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cereb. Cortex. 1997;7:268–282
  69. Resnick SM, Pham DL, Kraut MA, Zonderman AB, Davatzikos C. Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J. Neurosci. 2003;23:3295–3301
  70. Resnick SM, Goldszal AF, Davatzikos C, Golski S, Kraut MA, Metter EJ, et al. One-year age changes in MRI brain volumes in older adults. Cereb. Cortex. 2000;10:464–472
  71. Rettmann ME, Kraut MA, Prince JL, Resnick SM. Cross-sectional and longitudinal analyses of anatomical sulcal changes associated with aging. Cereb. Cortex. 2006;16:1584–1594
  72. Rousset OG, Ma Y, Evans AC. Correction for partial volume effects in PET: principle and validation. J. Nucl. Med. 1998;39:904–911
  73. Rousset OG, Ma Y, Wong DF, Evans AC. Pixel- versus region-based partial volume correction in PET. In:  Carson RE,  Herscovitch P,  Daube-Witherspoon M editor. Quantitative Functional Brain Imaging with Positron Emission Tomography. San Diego, CA: Academic Press; 1998;p. 67–75
  74. Rousset O, Zaidi H. Correction for partial volume effects in emission tomography. In:  Zaidi H editors. Quantitative Analysis in Nuclear Medicine Imaging. New York: Springer; 2005;p. 236–271
  75. Salat DH, Buckner RL, Snyder AZ, Greve DN, Desikan RSR, Busa E, et al. Thinning of the cerebral cortex in aging. Cereb. Cortex. 2004;14:721–730
  76. Scahill RI, Frost C, Jenkins R, Whitwell JL, Rossor MN, Fox NC. A longitudinal study of brain volume changes in normal aging using serial registered magnetic resonance imaging. Arch. Neurol. 2003;60:989–994
  77. Schacter DL, Wagner AD. Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval. Hippocampus. 1999;9:7–24
  78. Schacter DL, Savage CR, Alpert NM, Rauch SL, Albert MS. The role of hippocampus and frontal cortex in age-related memory changes: a PET study. Neuroreport. 1996;7:1165–1169
  79. Sperling RA, Bates JF, Chua EF, Cocchiarella AJ, Rentz DM, Rosen BR, et al. fMRI studies of associative encoding in young and elderly controls and mild Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry. 2003;74:44–50
  80. Sullivan EV, Marsh L, Pfefferbaum A. Preservation of hippocampal volume throughout adulthood in healthy men and women. Neurobiol. Aging. 2005;26:1093–1098
  81. Tisserand DJ, van Boxtel MPJ, Pruessner JC, Hofman P, Evans AC, Jolles J. A voxel-based morphometric study to determine individual differences in gray matter density associated with age and cognitive change over time. Cereb. Cortex. 2004;14:966–973
  82. Toga AW, Thompson PM, Sowell ER. Mapping brain maturation. Trends Neurosci. 2006;29:148–159
  83. Tulving E, Kapur S, Craik FIM, Moscovitch M, Houle S. Hemispheric encoding retrieval asymmetry in episodic memory: positron emission tomography findings. Proc. Natl. Acad. Sci. U.S.A. 1994;91:2016–2020
  84. Van Laere KJ, Dierckx RA. Brain perfusion SPECT: age- and sex-related effects correlated with voxel-based morphometric findings in healthy adults. Radiology. 2001;221:810–817
  85. Walhovd KB, Fjell AM, Reinvang I, Lundervold A, Dale AM, Eilertsen DE, et al. Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol. Aging. 2005;26:1261–1270
  86. Willis MW, Ketter TA, Kimbrell TA, George MS, Herscovitch P, Danielson AL, et al. Age, sex and laterality effects on cerebral glucose metabolism in healthy adults. Psychiatry Res. (Neuroimaging). 2002;114:23–37
  87. Yanase D, Matsunari I, Yajima K, Chen W, Fujikawa A, Nishimura S, et al. Brain FDG PET study of normal aging in Japanese: effect of atrophy correction. Eur. J. Nucl. Med. Mol. Imaging. 2005;32:794–805
  88. Zaidi H, Ruest T, Schoenahl F, Montandon ML. Links comparative assessment of statistical brain MR image segmentation algorithms and their impact on partial volume correction in PET. Neuroimage. 2006;32:1591–1607
  89. Zuendorf G, Kerrouche N, Herholz K, Baron JC. Efficient principal component analysis for multivariate 3D voxel-based mapping of brain functional imaging data sets as applied to FDG-PET and normal aging. Hum. Brain Mapp. 2003;18:13–21

PII: S0197-4580(07)00230-8

doi: 10.1016/j.neurobiolaging.2007.05.019

Neurobiology of Aging
Volume 30, Issue 1 , Pages 112-124 , January 2009

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