Normal aging; Progressive supranuclear palsy; Frontotemporal dementia; PET; (18)FDG
Abstract :
[en] Normal aging, progressive supranuclear palsy (PSP), and frontotemporal dementia (FTD) are characterized by different degrees of decline in frontal lobe functions. We used (18)FDG-PET and statistical parametric mapping (SPM96) to compare relative subcorticofrontal metabolic impairment at rest in 21 healthy elderly subjects (HES), 20 PSP patients, and 6 FTD patients. When HES were compared to 22 healthy young subjects, widespread decrease in metabolism was observed in bilateral medial prefrontal areas including anterior cingulate cortices, in dorsolateral prefrontal areas, in left lateral premotor area, in Broca's area, and in left insula. In PSP compared to the 43 healthy subjects (HS), we observed subcorticofrontal metabolic impairment including both motor and cognitive neural networks. Impairment of functional connections between midbrain tegmentum and cerebellar, temporal and pallidal regions was demonstrated in PSP as compared to HS. When comparing FTD to HS, glucose uptake was primarily reduced in dorsolateral and ventrolateral prefrontal cortices and in frontopolar and anterior cingulate regions. There was also bilateral anterior temporal, right inferior parietal, and bilateral striatal hypometabolism. Finally, FTD showed more severe striatofrontal metabolic impairment than PSP, while mesencephalothalamic involvement was only observed in PSP. Our data suggest that subcorticofrontal metabolic impairment is distributed in distinct subcorticocortical networks in normal aging, PSP, and FTD. Subcorticofrontal dementia in PSP is related to hypometabolism in discrete frontal areas, which are probably disconnected from certain subcortical structures. The concept of subcortical dementia is reinforced by our data, which show disrupted functional connections between mesencephalon and cerebellar cortex, inferior and medial temporal regions, and pallidum.
Research center :
GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège
Disciplines :
Neurology Neurosciences & behavior
Author, co-author :
Garraux, Gaëtan ; Université de Liège - ULiège > Centre de Recherches du cyclotron et Département des sciences cliniques > Neurologie
Salmon, Eric ; Université de Liège - ULiège > Centre de Recherches du cyclotron et Département des sciences cliniques > Neurologie
Degueldre, Christian ; Université de Liège - ULiège > Centre de recherches du cyclotron
Lemaire, Christian ; Université de Liège - ULiège > Centre de recherches du cyclotron
Laureys, Steven ; Université de Liège - ULiège > Centre de Recherches du cyclotron et Département des sciences cliniques > Neurologie
Franck, Georges ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie
Language :
English
Title :
Comparison of impaired subcortico-frontal metabolic networks in normal aging, subcortico-frontal dementia, and cortical frontal demential
Publication date :
August 1999
Journal title :
NeuroImage
ISSN :
1053-8119
eISSN :
1095-9572
Publisher :
Academic Press Inc Elsevier Science, San Diego, United States - California
Absher, J. R., and Cummings, J. L. 1995. Neurobehavioural examination of frontal lobe functions. Aphasiology 9:181-192.
Albert, M. L., Feldman, R. G., and Willis, A. L. 1974. The "subcortical dementia" of progressive supranuclear palsy. J. Neurol. Neurosurg. Psychiatry 37:121-130.
Alexander, G. E., DeLong, M. R., and Strick, P. L. 1986. Parallel organization of functionally segregated circuits liking basal ganglia and cortex. Annu. Rev. Neurosci. 9:357-381.
Bak, T. H., and Hodges, J. R. 1998. The neuropsychology of progressive supranuclear palsy. Neurocase 4:89-94.
Berg, L. 1984. Clinical dementia rating. Br. J Psychiatry 145:339.
Blesa, R., Mohr, E., Miletich, R. S., Randolph, C., Hildebrand, K., Sampson, M., and Chase, N. T. 1997. Changes in cerebral glucose metabolism with normal aging. Eur. Neurol. 4:8-14.
Blin, J., Baron, J.-C., Dubois, B., Pillon, B., Cambon, H., Cambier, J., and Agid, Y. 1990. Positron emission tomography study in progressive supranuclear palsy. Brain hypometabolic pattern and clinicometabolic correlations. Arch. Neurol. 47:747-752.
Chase, N. T., Burrows, G. H., and Mohr, E. 1987. Cortical glucose utilization patterns in primary degenerative dementias of the anterior and posterior type. Arch. Gerontol. Geriatr. 6:289-297.
Collins, S. J., Ahlskog, J. E., Parisi, J. E., and Maraganore, D. M. 1995. Progressive supranuclear palsy: Neuropathologically based diagnostic clinical criteria. J. Neurol. Neurosurg. Psychiatry 58:167-173.
Craik, F. I. M., Anderson, N. D., Kerr, S. A., and Li, K. Z. H. 1995. Memory changes in normal ageing. In Handbook of Memory Disorders (A. D. Baddeley, B. A. Wilson, and F. N. Watts, Eds.), pp. 211-241. Wiley, Chichester.
D'Antona, R., Baron, J.-C., Samson, Y., Serdaru, M., Viader, F., Agid, Y., and Cambier, J. 1985. Subcortical dementia. Frontal cortex hypometabolism detected by positron tomography in patients with progressive supranuclear palsy. Brain 108:785-799.
D'Esposito, M., Detre, J. A., Alsop, D. C., Shin, R. K., Atlas, S., and Grossman, M. 1995. The neural basis of the central executive system of working memory. Nature 378:279-281.
Daigneault, S., and Braun, C. M. J. 1993. Working memory and the self-ordered pointing task: Further evidence of early prefrontal decline in normal aging. J. Clin. Exp. Neuropsy. 15:881-895.
Daniel, S. E., de Bruin, V. M. S., and Lees, A. J. 1995. The clinical and pathological spectrum of Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy): A reappraisal. Brain 118:759-770.
Dauth, G. W., Gilman, S., Frey, K. A., and Penney, J. B. 1985. Basal ganglia glucose utilization after recent precentral ablation in the monkey. Ann. Neurol. 17:431-438.
de Leon, M. J., George, A. E., Tomanelli, J., Christman, D., Kluger, A., Miller, J., Ferris, S. H., Fowler, J., Brodie, J. D., and Van Gelder, P. 1987. Positron emission tomography studies of normal aging: A replication of PET III and 18-FDG using PET VI and 11-CDG. Neurobiol. Aging 8:319-323.
Defebvre, L., Lecouffe, P., Destée, A., Houdart, P., and Steinling, M. 1995. Tomographic measurements of regional cerebral blood flow in progressive supranuclear palsy and Parkinson's disease. Acta Neurol. Scand. 92:235-241.
Degueldre, C., and Quaglia, L. 1992. Performance evaluation of a new whole-body positron emission tomograph: The ECAT 951/31 R. Proc. Int. Conf. IEEE 14:1831-1833.
Deuel, R. K., and Collins, R. C. 1984. The functional anatomy of frontal lobe neglect in the monkey: Behavioral and quantitative 2-deoxyglucose studies. Ann. Neurol. 15:521-529.
Dubois, B., Deweer, B., and Pillon, B. 1996. The cognitive syndrome of progressive supranuclear palsy. In Advances in Neurology (L. Battistin, G. Scarlato, T. Caraceni, and S. Ruggieri, Eds.), pp. 399-403. Lippincott-Raven, Philadelphia.
Foster, N. L., Gilman, S., Berent, S., Morin, E. M., Brown, M. B., and Koeppe, R. A. 1988. Cerebral hypometabolism in progressive supranuclear palsy studied with positron emission tomography. Ann. Neurol. 24:399-406.
Friedland, R. P., Koss, E., Lerner, A., Hereda, P., Ellis, W., Dronkers, N., Ober, B. A., and Jagust, W. J. 1993. Functional imaging, the frontal lobes, and dementia. Dementia 4:192-203.
Friston, K. J. 1997a. Analysing brain images: Principles and overview. In Human Brain Function (R. S. J. Frackowiak, K. J. Friston, C. D. Frith, R. J. Dolan, and J. C. Mazziotta, Eds.), pp. 25-42. Academic Press, San Diego.
Friston, K. J., Buechel, C., Fink, G. R., Morris, J., Rolls, E., and Dolan, R. J. 1997b. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6:218-229.
Fukushima-Kudo, J., Fukushima, K., and Tashiro, K. 1987. Rigidity and dorsiflexion of the neck in progressive supranuclear palsy and the interstitial nucleus of cajal. J. Neurol. Neurosurg. Psychiatry 50:1197-1203.
Gibson, P. H. 1983. EM study of the number of cortical synapses in the brains of ageing people and people with Alzheimer-type dementia. Acta Neuropathol. (Berlin). 62:127-133.
Goffinet, A. M., De Volder, A. G., Gillain, C., Rectem, D., Bol, A., Michel, C., Cogneau, M., Labar, D., and Laterre, C. 1989. Positron emission tomography demonstrate frontal lobe hypometabolism in progressive supranuclear palsy. Ann. Neurol. 25:131-139.
Grafman, J., Litvan, I., Gomez, C., and Chase, N. T. 1990. Frontal lobe function in progressive supranuclear palsy. Arch. Neurol. 47:553-558.
Gur, R. C., Gur, R. E., Obrist, W. D., Skolnick, B. E., and Reivich, M. 1987. Age and regional cerebral blood flow at rest and during cognitive activity. Arch. Gen. Psychiatry 44:617-621.
Gustafson, L. 1987. Frontal lobe degeneration of non-Alzheimer type. II. Clinical picture and differential diagnosis. Arch. Gerontol. Geriatr. 6:209-223.
Higuchi, Y., Iwaki, T., and Tateishi, J. 1995. Neurodegeneration in the limbic and paralimbic system in progressive supranuclear palsy. Neuropath. Appl. Neurobiol. 21:246-254.
Hoffman, E. J., Huang, S. C., and Phelps, M. E. 1979. Quantitation in positron emission tomography: 1. Effect of object size. J. Comput. Assist. Tomogr. 3:299-308.
Hughes, C. P., Berg, L., Danziger, W. L., Coben, L. A., and Martin, R. L. 1982. A new clinical scale for the staging of dementia. Br. J. Psychiatry 140:566-572.
Huttenlocher, P. R. 1979. Synaptic density in human frontal cortex-Developmental changes and effects of aging. Brain Res. 163:195-205.
Ishii, K., Sakamoto, S., Sasaki, M., Kitagati, H., Yamaji, S., Hashimoto, M., Imamura, T., Shimomura, T., Hirono, N., and Mori, E. 1998. Cerebral glucose metabolism in patients with frontotemporal dementia. J. Nucl. Med. 39:1875-1878.
Jackson, M., and Lowe, J. 1996. The new neuropathology of degenerative frontotemporal dementias. Acta Neuropathol. 91:127-134.
Johnson, K. A., Sperling, R. A., Holman, B. L., Nagel, J. S., and Growdon, J. H. 1992. Cerebral perfusion in progressive supra-nuclear palsy. J. Nucl. Med. 33:704-709.
Kamo, H., McGeer, P. L., Harrop, R., McGeer, E. G., Calne, D. B., Martin, W. R. W., and Pate, B. D. 1987. Positron emission tomography and histopathology in Pick's disease. Neurology 37:439-445.
Karbe, H., Grond, M., Huber, M., Herholz, K., Kessler, J., and Heiss, W. D. 1992. Subcortical damage and cortical dysfunction in progressive supranuclear palsy demonstrated by positron emission tomography. J. Neurol. 239:98-102.
Kuhl, D. E., Metter, E. J., Riege, W. H., and Phelps, M. E. 1982. Effects of human aging on patterns of local cerebral glucose utilization determined by the [ 18F] fluorodeoxyglucose method. J. Cereb. Blood Flow Metab. 2:163-171.
Kumar, A., Schapiro, M. B., Haxby, J. V., Grady, C. L., and Friedland, R. P. 1990. Cerebral metabolic and cognitive studies in dementia with frontal lobe behavioral features. J. Psychiatr. Res. 24:97-109.
Labbé, C., Froment, J. C., Kennedy, A., Ashburner, J., and Cinotti, L. 1996. Positron emission tomography metabolic data corrected for cortical atrophy using magnetic resonance imaging. Alzheimer Dis. Assoc. Disord. 10:141-170.
Leenders, K. L., Frackowiak, R. S. J., and Lees, A. J. 1988. Steele-Richardson-Olszewski syndrome. Brain energy metabolism, blood flow and fluorodopa uptake measured by positron emission tomography. Brain 111:615-630.
Leenders, K. L., Perani, D., Lammerstma, A. A., Heather, J. D., Buckingham, P., Healy, M. J. R., Gibbs, J. M., Wise, R. S. J., Hatazawa, J., Herold, S., Beaney, R. P., Brooks, D. J., Spinks, T., Rhodes, C., Frackowiak, R. S. J., and Jones, T. 1990. Cerebral blood flow, blood volume, and oxygen utilization. Normal values and effect of age. Brain 113:27-47.
Litvan, I., Agid, Y., Calne, D., Campbell, G., Dubois, B., Duvoisin, R. C., Goetz, C. G., Golbe, L. I., Grafman, J., Growdon, J. H., Hallett, M., Jankovic, J., Quinn, N., Tolosa, E., and Zee, D. S. 1996a. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): Report of the NINDS-SPSP international workshop. Neurology 47: 1-9.
Litvan, I., Agid, Y., Jankovic, J., Goetz, C. G., Brandel, J. P., Lai, E. C., Wenning, G. K., D'Olhaberriague, L., Verny, M., Chaudhuri, K. R., McKee, A., Jellinger, K., Barkto, J.-J., Mangone, C. A., and Pearce, R. K. B. 1996b. Accuracy of clinical criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome). Neurology 46:922-930.
Mann, D. M. A., South, P. W., Snowden, J. S., and Neary, D. 1993. Dementia of frontal lobe type: Neuropathology and immunohistochemistry J. Neurol. Neurosurg. Psychiatry 56:605-614.
Martin, A. J., Friston, K. J., Colebatch, J. G., and Frackowiak, R. S. J. 1991. Decreases in regional cerebral blood flow with normal aging. J. Cereb. Blood Flow Metab. 11:684-689.
Masliah, E., Mallory, M., Hansen, L., DeTeresa, R., and Terry, R. D. 1993. Quantitative synaptic alterations in the human neocortex during normal aging. Neurology 43:192-197.
Miller, B. L., Cummings, J. L., Villanueva-Meyer, J., Boone, K., Mehringer, C. M., Lesser, I. M., and Mena, I. 1991. Frontal lobe degeneration: Clinical, neuropsychological, and SPECT characteristics. Neurology 41:1374-1382.
Mittenberg, W., Seidenberg, M., O'leary, D. S., and DiGiulio, D. V. 1989. Changes in cerebral functioning associated with normal aging. J. Clin. Exp. Neuropsy. 11:918-932.
Moeller, J. R., Ishikawa, T., Dhawan, V., Spetsieris, P., Mandel, F., Alexander, G. E., Grady, C., Pietrini, P., and Eidelberg, D. 1996. The metabolic topography of normal aging. J. Cereb. Blood Flow Metab. 16:385-398.
Morris, J. C. 1993. The clinical dementia rating (CDR): Current version and scoring rules. Neurology 43:2412-2414.
Neary, D., Snowden, J. S., Shields, R. A., Burjan, A. W. I., Northen, B., Macdermott, N., Prescott, M. C., and Testa, H. J. 1987. Single photon emission tomography using 99mTc-HM-PAO in the investigation of dementia. J. Neurol. Neurosurg. Psychiatry 50:1101-1109.
Neary, D., Snowden, J. S., and Goulding, P. 1988. Dementia of frontal lobe type. J. Neurol. Neurosurg. Psychiatry 51:353-361.
Parkinson, S. R. 1982. Performance deficits in short-term memory tasks: A comparison of amnesic korsakoff patients and the aged. In Human Memory and Amnesia (L. S. Cermak, Eds.), pp. 77-96. Erlbaum, Hillsdale.
Paulesu, E., Frith, C. D., and Frackowiak, R. S. J. 1993. The neural correlates of the verbal component of working memory. Nature 362:342-345.
Petit-Taboué, M.-C., Landeau, B., Desson, J.-F., Desgranges, B., and Baron, J.-C. 1998. Effects of healthy aging on the regional cerebral metabolic rate of glucose assessed with statistical parametric mapping. Neuroimage 7:176-184.
Petrides, M., Alivisatos, B., and Evans, A. C. 1995. Functional activation of the human ventrolateral frontal cortex during mnemonic retrieval of verbal information. Proc. Natl. Acad. Sci. USA 92:5803-5807.
Risberg, J. 1987. Frontal lobe degeneration of non-Alzheimer type. III. Regional cerebral blood flow. Arch. Gerontol. Geriatr. 6:225-233.
Rottach, K. G., Riley, D. E., DiScenna, A. O., Zivotofsky, A. Z., and Leigh, R. J. 1996. Dynamic properties of horizontal and vertical eye movements in parkinsonian syndromes. Ann. Neurol. 39:368-377.
Salmon, E., and Franck, G. 1989. Positron emission tomography study in Alzheimer's disease and Pick's disease. Arch. Gerontol. Geriatr Suppl. 1:241-247.
Salmon, E., Maquet, P., Sadzot, B., Degueldre, C., Lemaire, C., and Franck, G. 1991. Decrease of frontal metabolism demonstrated by positron emission tomography in a population of healthy elderly volunteers. Acta Neurol. Belg. 91:288-295.
Salmon, E., Van der Linden, M., Collette, F., Delfiore, G., Maquet, P., Degueldre, C., Luxen, A., and Franck, G. 1996. Regional brain activity during working memory tasks. Brain 119:1617-1625.
Salmon, E., Van der Linden, M., and Franck, G. 1997. Anterior cingulate and motor network metabolic impairment in progressive supranuclear palsy. Neuroimage 5:173-178.
Scarnati, E., and Florio, T. 1997. The pedunculopontine nucleus and related structures. Functional organization. In The Basal Ganglia and New Surgical Approaches for Parkinson's Disease (J. A. Obeso, M. J. DeLong, C. Ohye, and C. D. Marsden, Eds.), pp. 97-110. Lippincott-Raven, Philadelphia.
Shallice, T., Fletcher, P., Frith, C. D., Grasby, P., Frackowiak, R. S. J., and Dolan, R. J. 1994. Brain regions associated with acquisition and retrieval of verbal episodic memory. Nature 368:633-635.
Signorini, M., Paulesu, E., Friston, K. J., Perani, D., Colleluori, A., Lucignani, G., Grassi, F., Bettinardi, V., Frackowiak, R. S. J., and Fazio, F. 1999. Rapid assessment of regional cerebral metabolic abnormalities in single subjects with quantitative and nonquantitative [ 18F] FDG PET: A clinical validation of statistical parametric mapping. Neuroimage 9:63-80.
Starkstein, S. E., Migliorelli, R., Tesón, A., Sabe, L., Vásquez, S., Turjanski, M., Robinson, R. G., and Leiguarda, R. 1994. Specificity of changes in cerebral blood flow in patients with frontal lobe dementia. J. Neurol. Neurosurg. Psychiatry 57:790-796.
Steele, J. C., Richardson, J. C., and Olszewski, J. 1964. Progressive supranuclear palsy. Arch. Neurol. 10:333-359.
Talairach, J., and Tournoux, P. 1988. A Co-planar Stereotaxic Atlas of The Human Brain. Thieme, Stuttgart.
The Lund and Manchester Groups. 1994. Clinical and neuropathological criteria for frontotemporal dementia. J. Neurol. Neurosurg. Psychiatry 57:416-418.
Verny, M., Duyckaerts, C., Agid, Y., and Hauw, J.-J. 1996. The significance of cortical pathology in progressive supranuclear palsy. Clinico-pathological data in 10 cases. Brain 119:1123-1136.
Wakabayashi, K., Hansen, L. A., Vincent, I., Mallory, M., and Masliah, E. 1997. Neurofibrillary tangles in the dentate granule cells of patients with Alzheimer's disease, lewy body disease and progressive supranuclear palsy. Acta Neuropathol. 93:7-12.
Waldemar, G., Hasselbach, S. G., Andersen, A. R., Delecluse, F., Petersen, P., Johnsen, A., and Paulson, O. B. 1991. 99mTc-d,1-Hmpao and SPECT of the brain in normal aging. J. Cereb. Blood Flow Metab. 11:508-521.
Wingfield, A., Stine, A. L., Lahar, C. J., and Aberdeen, J. S. 1988. Does the capacity of working memory change with age? Exp. Aging Res. 14:103-107.
