Comparison of impaired subcortico-frontal metabolic networks in normal aging, subcortico-frontal dementia, and cortical frontal dementia
Open accessAbstract
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.
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Decomposition of metabolic brain clusters in the frontal variant of frontotemporal dementia
Salmon, É., Kerrouche, N., Herholz, K., Perani, D., Holthoff‐Detto, V., Beuthien‐Baumann, B., Degueldre, C., Lemaire, C. F., Luxen, A., Baron, J., et al. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.10.016 · Cited by 44 · see citing works
“Previous imaging studies essentially emphasized a mean decrease of activity (or volume) in large portions of the frontal lobes in groups of FTD patients compared to reference populations (Boccardi et al., 2003; Garraux et al., 1999; Ishii et al., 1998; McMillan et al., 2004; Rosen et al., 2002a).”
InfluentialSelf-citationKlein, R. C., de Jong, B. M., de Vries, J. J., & Leenders, K. L. (2005) · Movement Disorders · doi:10.1002/mds.20493 · Cited by 41 · see citing works
Mihara, M., Hattori, N., Abe, K., et al. (2006) · Neuroreport · doi:10.1097/01.wnr.0000203353.52622.05 · Cited by 41 · see citing works
“This technique has been used for evaluating neurodegenerative dementias [1–3], which include various pathological entities such as Alzheimer’s disease (AD), frontotemporal dementia (FTD), corticobasal degeneration (CBD), progressive supranuclear palsy (PSP), dementia with Lewy bodies (DLB) and other disorders.”
ResultInfluentialIlieva, I. P., Alexopoulos, G. S., Dubin, M. J., Morimoto, S. S., Victoria, L. W., & Gunning, F. M. (2018) · The American Journal of Geriatric Psychiatry · doi:10.1016/j.jagp.2017.09.002 · Cited by 38 · see citing works
Importance of partial-volume correction in brain PET studies.
Fazio, F., & Perani, D. (2000) · PubMed · Cited by 39 · see citing works
EEG Microstate Analysis in Patients with Disorders of Consciousness and Its Clinical Significance
Toplutaş, E., Aydın, F., & Hanoğlu, L. (2023) · Brain Topography · doi:10.1007/s10548-023-00939-y · Cited by 38 · see citing works
Varrone, A., Pagani, M., Salvatore, E., Salmaso, D., Sansone, V., Amboni, M., Nobili, F. M., Michele, G. D., Filla, A., Barone, P., et al. (2007) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-006-0344-7 · Cited by 35 · see citing works
“This could have been due to a lower sensitivity of rCBF SPECT compared with FDG-PET, but also to the sample size.”
BackgroundResultInfluentialKo, J. H., Katako, A., Aljuaid, M., Goertzen, A. L., Borys, A., Hobson, D. E., Kim, S., & Lee, C. S. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2017.08.020 · Cited by 33 · see citing works
“This is in line with previous reports on frontal hypo-metabolism in normal aging (Curiati et al., 2011; Garraux et al., 1999; Kakimoto et al., 2016; Moeller et al., 1996; Nugent t al., 2014).”
BackgroundResultMedial temporal lobe metabolic impairment in dementia associated with motor neuron disease
Garraux, G., Salmon, É., Degueldre, C., et al. (1999) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(99)00188-4 · Cited by 33 · see citing works
Self-citationPoljansky, S., Ibach, B., Hirschberger, B., Männer, P., Klünemann, H. H., Hajak, G., & Marienhagen, J. (2011) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-010-0184-0 · Cited by 30 · see citing works
Chen, P. L., & Machado, L. (2016) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2016.02.010 · Cited by 27 · see citing works
Salmon, É. (2007) · Journal of Neural Transmission · doi:10.1007/s00702-007-0636-5 · Cited by 27 · see citing works
“ers such as Garraux et al. (1999) and Salmon et al. (2003) have found a decrease in activity in the medial prefrontal, cingulate, orbitofrontal and anterior temporal cortices,”
BackgroundSelf-citationImagerie cérébrale du vieillissement normal : contraste avec la maladie d’Alzheimer
Desgranges, B., Kalpouzos, G., & Eustache, F. (2008) · Revue Neurologique · doi:10.1016/s0035-3787(08)73299-5 · Cited by 22 · see citing works
Nugent, S., Castellano, C., Bocti, C., Dionne, I. J., Fülöp, T., & Cunnane, S. C. (2015) · Biogerontology · doi:10.1007/s10522-015-9595-7 · Cited by 20 · see citing works
“…suggest that the most consistent finding for CMRg during normal aging is glucose hypometabolism in the frontal cortex (Kalpouzos et al. 2009; Zuendorf et al. 2003; Herholz et al. 2002; Garraux et al. 1999; Petit-Taboue et al. 1998; Moeller et al. 1996; De Santi et al. 1995; Nugent et al. 2014a, b).”
BackgroundThe Relationship Between Atrophy and Hypometabolism: Is It Regionally Dependent in Dementias?
Rodríguez‐Oroz, M., Gago, B., Clavero, P., Delgado‐Alvarado, M., García‐García, D., & Jiménez‐Urbieta, H. (2015) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-015-0562-0 · Cited by 21 · see citing works
Influence of blood viscosity to cerebral blood flow in older humans compared to young subjects
Galduróz, J. C. F., Bueno, O. F. A., Yamaga, L. I., et al. (2011) · Clinical Neurophysiology · doi:10.1016/j.clinph.2011.05.025 · Cited by 19 · see citing works
“Several reports have also pointed out that cerebral perfusion decreases with age, mainly in the left hemisphere (Catafau et al., 1996; Garraux et al., 1999; Pagani et al., 2002; Herholz et al., 2002).”
BackgroundFrontal hypometabolism in the diagnosis of progressive supranuclear palsy clinical variants
Black, J. A., Pham, N. T. T., Ali, F., et al. (2024) · Journal of Neurology · doi:10.1007/s00415-024-12350-z · Cited by 18 · see citing works
“While one might expect prefrontal hypometabolism in PSP-F, given the clinical overlap with bvFTD [4], this was not the case.”
Functional brain imaging applications to differential diagnosis in the dementias
Salmon, É. (2002) · Current Opinion in Neurology · doi:10.1097/00019052-200208000-00006 · Cited by 18 · see citing works
Self-citationValotassiou, V. J., Papatriantafyllou, J. D., Sifakis, N., Tzavara, C. K., Tsougos, I., Kapsalaki, E. Z., Hadjigeorgiou, G. M., & Georgoulias, P. (2012) · Nuclear Medicine Communications · doi:10.1097/mnm.0b013e3283599983 · Cited by 16 · see citing works
Age related preservation and loss in optimized brain SPECT
Barnden, L. R., Behin-Ain, S., Kwiatek, R., Casse, R., & Yelland, L. (2005) · Nuclear Medicine Communications · doi:10.1097/00006231-200506000-00004 · Cited by 16 · see citing works
Frontotemporal dementia: clinical, neuroimaging, and molecular biological findings in 6 patients
Jauß, M., Herholz, K., Kracht, L. W., et al. (2001) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s004060170031 · Cited by 16 · see citing works
“gated 15 FTD patients in a SPECT study [18] and 6 FTD patients in a PET study, respectively [ 4 ].”
MethodGarraux, G., Bahri, M. A., Lemaire, C. F., Degueldre, C., Salmon, É., & Kaschten, B. (2011) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2011.41 · Cited by 15 · see citing works
“…of resting-state cerebral FDG uptake were all obtained at the Cyclotron Research Centre, University Campus of Sart Tilman, Belgium, with eyes closed on a SIEMENS CTI 951 R 16/31 tomograph (CTI, Knoxville, TN, USA) in two-dimensional mode, after fasting for at least 12 hours (Garraux et al, 1999).”
MethodSelf-citationPositron Emission Tomography for Brain Research
Mishina, M. (2008) · Journal of Nippon Medical School · doi:10.1272/jnms.75.68 · Cited by 14 · see citing works
Brainstem and cerebellar radiological findings in progressive supranuclear palsy
Spiegel, C., Marotta, C., Bertram, K., Vivash, L. E., & Harding, I. H. (2024) · Brain Communications · doi:10.1093/braincomms/fcaf051 · Cited by 13 · see citing works
Hellwig, S., Domschke, K., & Meyer, P. T. (2019) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000706 · Cited by 11 · see citing works
Frontotemporal lobar degeneration: clinical and pathologic overview
Rabinovici, G. D., Rascovsky, K., & Miller, B. L. (2008) · Handbook of clinical neurology · doi:10.1016/s0072-9752(07)01233-x · Cited by 11 · see citing works
López-Grueso, R., Borrás, C., Gambini, J., & Viña, J. (2010) · Revista Española de Geriatría y Gerontología · doi:10.1016/j.regg.2009.12.005 · Cited by 10 · see citing works
Sierra, B., Cruz, I., & Froufe, M. (2009) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 7 · see citing works
Experimental gerontology in Belgium: from model organisms to age-related pathologies
Toussaint, O., Baret, P. V., Brion, J., Cras, P. P., Collette, F., Deyn, P. P. D., Geenen, V. G., Kienlen‐Campard, P., Labeur, C., Legros, J., et al. (2000) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00177-7 · Cited by 7 · see citing works
“Cerebral glucose uptake in normal ageing was confirmed to be essentially decreased in several frontal regions, when compared to young subjects (Garraux et al., 1999).”
ResultSelf-citationCerebral aging: neuropsychological, neuroradiological, and neurometabolic correlates.
STARKSTEIN, S. E., & Kremer, J. L. (2001) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2001.3.3/sestarkstein · Cited by 6 · see citing works
Emotion Recognition and Aging of the Social Brain
Ruffman, T. K., & Sutcliffe, R. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108552684.023 · Cited by 5 · see citing works
Falasco, G., Damián, A., Urrutia, L., Niell, N., Lago, G., Bérgamo, Y., Chrem, P., Quagliata, A., Bentancourt, C., Calandri, I. L., et al. (2021) · Current Alzheimer Research · doi:10.2174/1567205018666211116095035 · Cited by 5 · see citing works
The Frontotemporal Dementia Syndromes
Mendez, M. F. (2010) · Wiley eBooks · doi:10.1002/9780470669600.ch57 · Cited by 5 · see citing works
Does age affect medial prefrontal functions? A behavioral investigation.
Iveson, M. H., Sala, S. D., & MacPherson, S. E. (2019) · Psychology & Neuroscience · doi:10.1037/pne0000194 · Cited by 2 · see citing works
“, 2017), and metabolic impairment (Garraux et al., 1999; Hazlett et al., 2010) within the DLPFC and the MPFC.”
15 Differential Diagnosis of Dementia Using Functional Neuroimaging
Salmon, É., Collette, F., & Garraux, G. (2009) · doi:10.1093/acprof:oso/9780195328875.003.0015 · Cited by 3 · see citing works
Self-citationAge-Related Glucose Metabolism in FDG-PET Brain Studies
Seifar, F., Hajibonabi, F., Parnianfard, N., Ranjkesh, M., Valikhani, E., & Yazdchi, M. R. (2018) · Translational Neuroscience Research and Reviews · doi:10.36959/817/520 · Cited by 3 · see citing works
La Paralysie Supranucléaire Progressive
Dujardin, K., & Defebvre, L. (2007) · Elsevier eBooks · doi:10.1016/b978-2-294-08039-5.50005-8 · Cited by 3 · see citing works
18F-FDG PET/CT Indications, Pitfalls and Limitations in Brain Imaging
Vöö, S. A., & Bomanji, J. B. (2019) · Springer eBooks · doi:10.1007/978-3-030-01523-7_9 · Cited by 2 · see citing works
Advances in early diagnosis and differentiation of the dementias
Thompson, S., Nestor, P. J., & Hodges, J. R. (2003) · Cambridge University Press eBooks · doi:10.1017/cbo9780511550072.014 · Cited by 1 · see citing works
Nuclear Imaging in Frontotemporal Dementia
Reesink, F. E., Stormezand, G. N., Dierckx, R. A. J. O., & Deyn, P. P. D. (2014) · Springer eBooks · doi:10.1007/978-3-642-54307-4_15 · Cited by 2 · see citing works
Nuclear Imaging in Frontotemporal Dementia
Reesink, F. E., Stormezand, G. N., Dierckx, R. A. J. O., & Deyn, P. P. D. (2020) · Springer eBooks · doi:10.1007/978-3-030-53168-3_15 · Cited by 1 · see citing works
The role of tau and neuroinflammation in Progressive Supranuclear Palsy and Alzheimer's Disease
Rodríguez, P. V. (2019) · Apollo (University of Cambridge) · doi:10.17863/cam.45106 · Cited by 1 · see citing works
Les troubles cognitifs associés au vieillissement normal
Collette, F., Salmon, É., & Audiffren, M. F. (2012) · Presses universitaires de Rennes eBooks · doi:10.4000/books.pur.61156
Self-citation
- Authors
- Garraux, G., Salmon, E., Degueldre, C., Lemaire, C., Laureys, S., & Franck, G.
- Affiliations
- University of Liège (BE)
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 1999-08
- Volume
- 10
- Issue
- 2
- Pages
- 149-162
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W2149544109
- Cited by
- 109
- References
- 0
- Citations by year
- 2026: 1 · 2024: 2 · 2023: 1 · 2021: 2 · 2020: 3 · 2019: 5 · 2018: 2 · 2017: 3 · 2016: 4 · 2015: 2 · 2014: 4 · 2013: 2 · 2012: 7
- FWCI
- 4.96
- Type
- journal article
- Language
- en
- Open access
- green
- orbi.uliege.be
- Licence
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- ORBi (University of Liège) (submittedVersion, other-oa)
- 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 › Neurology › Parkinson's Disease Mechanisms and Treatments
- Keywords
- subcortical dementia, progressive supranuclear palsy, frontotemporal dementia, normal aging, glucose hypometabolism, medial prefrontal cortex, anterior cingulate cortex, dorsolateral prefrontal cortex, striatum, cerebellum, globus pallidus, temporal lobe
- MeSH terms
- Adult, Aged, Blood Glucose, Brain, Brain Mapping, Cerebellum, Dementia, Dominance, Cerebral, Energy Metabolism, Female, Frontal Lobe, Globus Pallidus, Humans, Image Processing, Computer-Assisted, Male, Mesencephalon, Middle Aged, Nerve Net, Reference Values, Supranuclear Palsy, Progressive, Tegmentum Mesencephali, Temporal Lobe, Tomography, Emission-Computed
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