Effects of healthy aging on the regional cerebral metabolic rate of glucose assessed with statistical parametric mapping
Abstract
The aging process is thought to result in changes in synaptic activity reflecting both functional and structural cell derangement. However, previous PET reports on age-related changes in resting brain glucose utilization (CMRglc) have been discrepant, presumably because of methodological as well as subject screening differences. In contrast to other studies, which used a region of interest approach, the objective of the present work was to determine, by means of the SPM software, the changes in regional CMRglc as a function of age in 24 optimally healthy, unmedicated volunteers of ages from 20 to 67 years. Global CMRglc showed a significant decline with age (approximately 6% per decade, P < 0.05), which concerned all the voxels studied save for most of the occipital cortex and part of the cerebellum. The most significant effects (P < 0.001) concerned the association neocortex in perisylvian temporoparietal and anterior temporal areas, the insula, the inferior and posterior-lateral frontal regions, the anterior cingulate cortex, the head of caudate nucleus, and the anterior thalamus, in a bilateral and essentially symmetrical fashion. The high posterior parietal cortex was not sampled in this study. This distribution of changes in CMRglc with age may differ from that seen in Alzheimer' disease, where the earliest metabolic reduction has been shown to affect the posterior cingulate cortex.
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Most previous studies have reported decreased activity in frontal areas and the anterior cingulate gyrus with age.
“Most previous studies have reported decreased activity in frontal areas and the anterior cingulate gyrus with age, using SPECT [44], [ 15 O]H2O-PET [5,12,42,48,54] or 18 FDG-PET [28,32,49,58,86,87,89].”
From Voxel-based mapping of brain gray matter volume and glucose metabolism profiles in normal aging (2009) · cites this paper as [58]
This reveals a major difference between Alzheimer's disease and normal aging.
“once again revealing a major difference between this neurodegenerative disease and normal aging [58,86].”
From Voxel-based mapping of brain gray matter volume and glucose metabolism profiles in normal aging (2009) · cites this paper as [58]
Less metabolic decrease was found within the inferior temporal (fusiform cortex) and occipital areas (calcarine area and lingual gyrus), consistent with the literature.
“Consistent with the literature, less metabolic decrease was found within the inferior temporal (fusiform cortex) and occipital areas (calcarine area and lingual gyrus) [32,49,58,86].”
From Voxel-based mapping of brain gray matter volume and glucose metabolism profiles in normal aging (2009) · cites this paper as [58]
Cites
Co-Planar Stereotaxic Atlas of the Human Brain
Talairach, J., & Tournoux, P. (1988) · Medical Entomology and Zoology · Cited by 11,798 · see citing works
Talairach, J., Tournoux, P., & Rayport, M. (1988) · Thieme eBooks · Cited by 5,058 · see citing works
Berti, A. (1992) · Neuropsychologia · doi:10.1016/0028-3932(92)90076-x · Cited by 4,190 · see citing works
Phelps, M. E., Huang, S. C., Hoffman, E. J., Selin, C. E., Sokoloff, L., & Kuhl, D. E. (1979) · Annals of Neurology · doi:10.1002/ana.410060502 · Cited by 2,417 · see citing works
Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease
Minoshima, S., Giordani, B., Berent, S., Frey, K. A., Foster, N. L., & Kuhl, D. E. (1997) · Annals of Neurology · doi:10.1002/ana.410420114 · Cited by 1,802 · see citing works
Aging, energy, and oxidative stress in neurodegenerative diseases
Beal, M. F. (1995) · Annals of Neurology · doi:10.1002/ana.410380304 · Cited by 1,434 · see citing works
Reiman, E. M., Caselli, R. J., Yun, L. S., Chen, K., Bandy, D., Minoshima, S., Thibodeau, S. N., & Osborne, D. (1996) · New England Journal of Medicine · doi:10.1056/nejm199603213341202 · Cited by 1,366 · see citing works
Life and Death of Neurons in the Aging Brain
Morrison, J. H., & Hof, P. R. (1997) · Science · doi:10.1126/science.278.5337.412 · Cited by 1,344 · see citing works
Beal, M. F. (1992) · Annals of Neurology · doi:10.1002/ana.410310202 · Cited by 956 · see citing works
The Relationship between Global and Local Changes in PET Scans
Friston, K. J., Frith, C., Liddle, P. F., Dolan, R. J., Lammertsma, A. A., & Frackowiak, R. S. J. (1990) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1990.88 · Cited by 858 · see citing works
Horton, A. M., & Moses, J. A. (1996) · Archives of Clinical Neuropsychology · doi:10.1093/arclin/11.8.713 · Cited by 765 · see citing works
Neocortical cell counts in normal human adult aging
Terry, R. D., DeTeresa, R. M., & Hansen, L. A. (1987) · Annals of Neurology · doi:10.1002/ana.410210603 · Cited by 686 · see citing works
Small, G. W. (1995) · JAMA: The Journal of the American Medical Association · doi:10.1001/jama.1995.03520360056039 · Cited by 604 · see citing works
A Stereotactic Method of Anatomical Localization for Positron Emission Tomography
Fox, P. T., Perlmutter, J. S., & Raichle, M. E. (1985) · Journal of Computer Assisted Tomography · doi:10.1097/00004728-198501000-00025 · Cited by 576 · see citing works
Murphy, D., Decarli, C., Mcintosh, A. R., Daly, E., Mentis, M., Pietrini, P., Szczepanik, J., Schapiro, M., Grady, C., Horwitz, B., et al. (1996) · Archives of General Psychiatry · doi:10.1001/archpsyc.1996.01830070031007 · Cited by 552 · see citing works
DeCarli, C., Murphy, D. G. M., Tranh, M., Grady, C. L., Haxby, J. V., Gillette, J. A., Salerno, J. A., Gonzales-Aviles, A., Honvitz, B., Rapoport, S. I., et al. (1995) · Neurology · doi:10.1212/wnl.45.11.2077 · Cited by 531 · see citing works
Quantitative cerebral anatomy of the aging human brain
Coffey, C. E., Wilkinson, W. E., Parashos, L., Soady, S. A. R., Sullivan, R. J., Patterson, L. J., Figiel, G. S., Webb, M. C., Spritzer, C. E., & Djang, W. T. (1992) · Neurology · doi:10.1212/wnl.42.3.527 · Cited by 480 · see citing works
Quantitative synaptic alterations in the human neocortex during normal aging
Masliah, E., Mallory, M. E., Hansen, L. A., DeTeresa, R. M., & Terry, R. D. (1993) · Neurology · doi:10.1212/wnl.43.1_part_1.192 · Cited by 408 · see citing works
Decreases in regional cerebral blood flow with normal aging
Martin, A. J., Friston, K. J., Colebatch, J. G., & Frackowiak, R. S. J. (1991) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1991.121 · Cited by 393 · see citing works
Visualisation and quantification of rates of atrophy in Alzheimer's disease
Fox, N. C., Freeborough, P. A., & Rossor, M. N. (1996) · The Lancet · doi:10.1016/s0140-6736(96)05228-2 · Cited by 378 · see citing works
Sex Differences in Regional Cerebral Glucose Metabolism During a Resting State
Gur, R. C., Mozley, L. H., Mozley, P. D., Resnick, S. M., Karp, J. S., Alavi, A. A., Arnold, S. E., & Gur, R. E. (1995) · Science · doi:10.1126/science.7824953 · Cited by 340 · see citing works
Kuhl, D. E., Metter, E. J., Riege, W. H., & Phelps, M. E. (1982) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1982.15 · Cited by 338 · see citing works
Localisation in PET Images: Direct Fitting of the Intercommissural (AC—PC) Line
Friston, K. J., Passingham, R. E., Nutt, J. G., Heather, J. D., Sawle, G. V., & Frackowiak, R. S. J. (1989) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1989.97 · Cited by 302 · see citing works
Regional Cerebral Oxygen Consumption, Blood Flow, and Blood Volume in Healthy Human Aging
Marchal, G., Rioux, P. P., Petit-Taboué, M.-C., Sette, G., Travère, J.-M., Poec, C. L., Courtheoux, P., Derlon, J.-M., & Baron, J. (1992) · Archives of Neurology · doi:10.1001/archneur.1992.00530340029014 · Cited by 271 · see citing works
Self-citationCommentary and Opinion: II. Statistical Parametric Mapping: Ontology and Current Issues
Friston, K. J. (1995) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1995.45 · Cited by 268 · see citing works
Human brain glucose utilization and cognitive function in relation to age
Duara, R., PhD, C. G., PhD, J. H., Ingvar, D. H., Sokoloff, L., Margolin, R. A., PhD, R. G. M., Cutler, N. R., & Рапопорт, С. И. (1984) · Annals of Neurology · doi:10.1002/ana.410160613 · Cited by 262 · see citing works
The metabolic topography of normal aging
Moeller, J. R., Ishikawa, T., Dhawan, V., Spetsieris, P., Mandel, F., Alexander, G. E., Grady, C., Pietrini, P., & Eidelberg, D. (1996) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199605000-00005 · Cited by 254 · see citing works
Creasey, H. M., & Rapoport, S. I. (1985) · Annals of Neurology · doi:10.1002/ana.410170103 · Cited by 250 · see citing works
Thalamic stimulation and suppression of parkinsonian tremor
Deiber, M., Pollak, P., Passingham, R. E., Landais, P., Gervason, C., Cinotti, L., Friston, K. J., Frackowiak, R. S. J., Mauguı̀ere, F., & Benabid, A. L. (1993) · Brain · doi:10.1093/brain/116.1.267 · Cited by 204 · see citing works
Topography of Brain Atrophy During Normal Aging and Alzheimer's Disease
Double, K. L., Halliday, G. M., Kril, J. J., Harasty, J., Cullen, K. M., Brooks, W. S., Creasey, H. M., & Broe, G. A. (1996) · Neurobiology of Aging · doi:10.1016/0197-4580(96)00005-x · Cited by 196 · see citing works
Effects of Exercise on Body Composition and Functional Capacity of the Elderly
Schwartz, R. S., & Evans, W. J. (1995) · The Journals of Gerontology Series A · doi:10.1093/gerona/50a.special_issue.147 · Cited by 169 · see citing works
Yoshii, F., Barker, W. W., Chang, J. Y., Loewenstein, D., Apicella, A., Smith, D. D., Boothe, T. E., Ginsberg, M. D., Pascal, S., & Duara, R. (1988) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1988.112 · Cited by 168 · see citing works
Cerebral glucose metabolic rates in normal human females versus normal males
Baxter, L. R., Mazziotta, J. C., Phelps, M. E., Selin, C. E., Guzé, B. H., & Fairbanks, L. A. (1987) · Psychiatry Research · doi:10.1016/0165-1781(87)90028-x · Cited by 165 · see citing works
Liu, X., Erikson, C., & Brun, A. E. (1996) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000106867 · Cited by 152 · see citing works
Tanna, N. K., Kohn, M., Horwich, D., Jolles, P. R., Zimmerman, R. A., Alves, W. M., & Alavi, A. (1991) · Radiology · doi:10.1148/radiology.178.1.1984290 · Cited by 148 · see citing works
Gender-related differences in regional cerebral glucose metabolism in normal volunteers
Andreason, P., Zametkin, A. J., Guo, A. C., Baldwin, P., & Cohen, R. M. (1994) · Psychiatry Research · doi:10.1016/0165-1781(94)90037-x · Cited by 140 · see citing works
Labbé, C., Froment, J. C., Kennedy, A. M., Ashburner, J., & Cinotti, L. (1996) · Alzheimer Disease & Associated Disorders · doi:10.1097/00002093-199601030-00005 · Cited by 99 · see citing works
Regional Correction of Positron Emission Tomography Data for the Effects of Cerebral Atrophy
Videen, T. O., Perlmutter, J. S., Mintun, M. A., & Raichle, M. E. (1988) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1988.113 · Cited by 98 · see citing works
Positron Emission Tomography and Computed Tomography Assessments of the Aging Human Brain
de Leon, M. J., GEORGE, A. E., Ferris, S. H., Christman, D. R., Fowler, J. S., Gentes, C. I., Brodie, J. D., Reisberg, ., & Wolf, A. P. (1984) · Journal of Computer Assisted Tomography · doi:10.1097/00004728-198402000-00017 · Cited by 97 · see citing works
Penniello, M., Lambert, J., Eustache, F., et al. (1995) · Brain · doi:10.1093/brain/118.3.697 · Cited by 96 · see citing works
Healthy aging, memory subsystems and regional cerebral oxygen consumption
Eustache, F., Rioux, P. P., Desgranges, B., Marchal, G., Petit-Taboué, M.-C., Dary, M., Lechevalier, B., & Baron, J. (1995) · Neuropsychologia · doi:10.1016/0028-3932(95)00021-t · Cited by 91 · see citing works
Self-citationde Leon, M. J., George, A. E., Tomanelli, J., Christman, D., Kluger, A., Miller, J., Ferris, S. H., Fowler, J., Brodie, J. D., van Gelder, P., et al. (1987) · Neurobiology of Aging · doi:10.1016/0197-4580(87)90070-4 · Cited by 79 · see citing works
Giannakopoulos, P., Hof, P. R., Giannakopoulos, A.-S., Herrmann, F. R., Michel, J.-P., & Bouras, C. (1995) · Archives of Neurology · doi:10.1001/archneur.1995.00540360028012 · Cited by 78 · see citing works
McGeer, E. G., Peppard, R. P., McGeer, P. L., Tuokko, H., Crockett, D., Parks, R., Akiyama, H., Calne, D. B., Beattie, B. L., & Harrop, R. (1990) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/s0317167100029930 · Cited by 76 · see citing works
Nehlig, A., Porrino, L. J., Crane, A. M., & Sokoloff, L. (1985) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1985.54 · Cited by 60 · see citing works
Miura, S., Schapiro, M. B., Grady, C. L., Kumar, A., Salerno, J. A., Kozachuk, W. E., Wagner, E., Рапопорт, С. И., & Horwitz, B. (1990) · Journal of Neuroscience Research · doi:10.1002/jnr.490270410 · Cited by 55 · see citing works
Relation of measured brain glucose utilisation and cerebral atrophy in man.
Schlageter, N. L., Horwitz, B., Creasey, H. M., Carson, R. E., Duara, R., BERG, G. W., & Рапопорт, С. И. (1987) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.50.6.779 · Cited by 52 · see citing works
Salmon, É., Maquet, P., Sadzot, B., et al. (1991) · PubMed · Cited by 50 · see citing works
Gender differences in cerebellar metabolism: test-retest reproducibility
Volkow, N. D., Wang, G. J., Fowler, J. S., et al. (1997) · American Journal of Psychiatry · doi:10.1176/ajp.154.1.119 · Cited by 50 · see citing works
Brain Metabolic Function in Older Men With Chronic Essential Hypertension
Salerno, J. A., Grady, C., Mentis, M. J., et al. (1995) · The Journals of Gerontology Series A · doi:10.1093/gerona/50a.3.m147 · Cited by 35 · see citing works
Positron Emission Tomography in Familial Alzheimer Disease
Kennedy, A. M., Rossor, M. N., & Frackowiak, R. S. J. (1995) · Alzheimer Disease & Associated Disorders · doi:10.1097/00002093-199505000-00005 · Cited by 29 · see citing works
Changes in cerebral glucose metabolism with normal aging
Blesa, R., Mohr, E., Miletich, R. S., RANDOLPH, C. C., Hildebrand, K., Sampson, M., & Chase, T. N. (1997) · European Journal of Neurology · doi:10.1111/j.1468-1331.1997.tb00294.x · Cited by 27 · see citing works
Cortical mapping of Alzheimer pathology in brains of aged non-demented subjects.
Vermersch, P., David, J., Frigard, B., Fallet-Bianco, C., Wattez, A., Petit, H., & Delacourte, A. (1995) · Progress in Neuro-psychopharmacology and Biological Psychiatry · doi:10.1016/0278-5846(95)00195-6 · Cited by 26 · see citing works
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“…1959; Kennedy and Sokoloff, 1957; Kinnala et al., 1996; Kuhl et al., 1982; Leenders et al., 1990; Pantano et al., 1984; Perlmutter et al., 1987; Petit-Taboué et al., 1998; 50 Cell Metabolism 19, 49–57, January 7, 2014 ª2014 Elsevier Inc. Scheinberg et al., 1953; Takahashi et al., 1999; Yoxall…”
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Calautti, C., Serrati, C., & Baron, J.-C. (2001) · Stroke · doi:10.1161/01.str.32.1.139 · Cited by 164 · see citing works
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- Authors
- Petit-Taboué, M. C., Landeau, B., Desson, J. F., Desgranges, B., & Baron, J. C.
- Affiliations
- Inserm (FR)
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 1998-04
- Volume
- 7
- Issue
- 3
- Pages
- 176-184
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W2025767657
- Cited by
- 221
- References
- 53
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 6 · 2023: 4 · 2022: 9 · 2021: 9 · 2020: 6 · 2019: 10 · 2018: 9 · 2017: 12 · 2016: 9 · 2015: 6 · 2014: 8 · 2013: 6 · 2012: 8
- FWCI
- 7.21
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Keywords
- healthy aging, regional cerebral glucose metabolism, cerebral metabolic rate of glucose, brain aging, association cortex, anterior cingulate cortex, insula, frontal cortex, thalamus, caudate nucleus, occipital cortex, cerebellum, Alzheimer's disease comparison
- MeSH terms
- Adult, Aged, Aging, Blood Glucose, Brain, Brain Mapping, Cerebral Cortex, Dominance, Cerebral, Energy Metabolism, Female, Humans, Image Processing, Computer-Assisted, Male, Mathematical Computing, Middle Aged, Software, Tomography, Emission-Computed, Fluorodeoxyglucose F18
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