[en] BACKGROUND: Alzheimer's disease (AD) is characterized by an involvement of brain dopamine (DA) circuitry, the presence of which has been associated with emergence of both neuropsychiatric symptoms and cognitive deficits. OBJECTIVE: In order to investigate whether and how the DA pathways are involved in the pathophysiology of AD, we assessed by in vivo neuroimaging the structural and metabolic alterations of subcortical and cortical DA pathways and targets. METHODS: We included 54 healthy control participants, 53 amyloid-positive subjects with mild cognitive impairment due to AD (MCI-AD), and 60 amyloid-positive patients with probable dementia due to AD (ADD), all with structural 3T MRI and 18F-FDG-PET scans. We assessed MRI-based gray matter reductions in the MCI-AD and ADD groups within an anatomical a priori-defined Nigrostriatal and Mesocorticolimbic DA pathways, followed by 18F-FDG-PET metabolic connectivity analyses to evaluate network-level metabolic connectivity changes. RESULTS: We found significant tissue loss in the Mesocorticolimbic over the Nigrostriatal pathway. Atrophy was evident in the ventral striatum, orbitofrontal cortex, and medial temporal lobe structures, and already plateaued in the MCI-AD stage. Degree of atrophy in Mesocorticolimbic regions positively correlated with the severity of depression, anxiety, and apathy in MCI-AD and ADD subgroups. Additionally, we observed significant alterations of metabolic connectivity between the ventral striatum and fronto-cingulate regions in ADD, but not in MCI-AD. There were no metabolic connectivity changes within the Nigrostriatal pathway. CONCLUSION: Our cross-sectional data support a clinically-meaningful, yet stage-dependent, involvement of the Mesocorticolimbic system in AD. Longitudinal and clinical correlation studies are needed to further establish the relevance of DA system involvement in AD.
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Bibliography
Jack CRJ, Bennett DA, Blennow K, Carrillo MC, Dunn B, Haeberlein SB, Holtzman DM, JagustW, Jessen F, Karlawish J, Liu E, Molinuevo JL, Montine T, Phelps C, Rankin KP, Rowe CC, Scheltens P, Siemers E, Snyder HM, Sperling R, Contributors (2018)NIA-AAResearch Framework: Toward a biological definition of Alzheimer's disease. Alzheimers Dement 14, 535-562.
Trillo L, Das D, Hsieh W, Medina B, Moghadam S, Lin B, Dang V, Sanchez MM, De Miguel Z, Ashford JW (2013) Ascending monoaminergic systems alterations in Alzheimer's disease. Translating basic science into clinical care. Neurosci Biobehav Rev 37, 1363-1379.
Gibb WR, Mountjoy CQ, Mann DM, Lees AJ (1989) The substantia nigra and ventral tegmental area in Alzheimer's disease and Down's syndrome. J Neurol Neurosurg Psychiatry 52, 193-200.
Storga D, Vrecko K, Birkmayer JGD, Reibnegger G (1996) Monoaminergic neurotransmitters, their precursors and metabolites in brains of Alzheimer patients. Neurosci Lett 203, 29-32.
Rinne JO, Säkö E, Paljärvi L, Mölsä PK, Rinne UK (1986) Brain dopamine D-1 receptors in senile dementia. J Neurol Sci 73, 219-230.
Allard P, Alafuzoff I, Carlsson A, Eriksson K, Ericson E, Gottfries C-G, Marcusson JO (1990) Loss of dopamine uptake sites labeled with [3H] GBR-12935 in Alzheimer's disease. Eur Neurol 30, 181-185.
Murray AM, Weihmueller FB, Marshall JF, Hurtig HI, Gottleib GL, Joyce JN (1995) Damage to dopamine systems differs between Parkinson's disease and Alzheimer's disease with parkinsonism. Ann Neurol 37, 300-312.
Joyce JN, Smutzer G, Whitty CJ, Myers A, Bannon MJ (1997) Differential modification of dopamine transporter and tyrosine hydroxylase mRNAs in midbrain of subjects with Parkinson's, Alzheimer's with parkinsonism, and Alzheimer's disease. Mov Disord 12, 885-897.
D'Amelio M, Puglisi-Allegra S, Mercuri N (2018) The role of dopaminergic midbrain in Alzheimer's disease: Translating basic science into clinical practice. Pharmacol Res 130, 414-419.
Nobili A, Latagliata EC, Viscomi MT, Cavallucci V, Cutuli D, Giacovazzo G, Krashia P, Rizzo FR, Marino R, Federici M, De Bartolo P, Aversa D, Dell'Acqua MC, Cordella A, Sancandi M, Keller F, Petrosini L, Puglisi-Allegra S, Mercuri NB, Coccurello R, Berretta N, D'Amelio M (2017) Dopamine neuronal loss contributes to memory and reward dysfunction in a model of Alzheimer's disease. NatCommun 8, 14727.
Bjorklund A, Dunnett SB (2007) Dopamine neuron systems in the brain: An update. Trends Neurosci 30, 194-202.
Le Moal M, Simon H (1991) Mesocorticolimbic dopaminergic network: Functional and regulatory roles. Physiol Rev 71, 155-234.
Chau BKH, Jarvis H, Law C-K, Chong TT-J (2018) Dopamine and reward: A view from the prefrontal cortex. Behav Pharmacol 29, 569-583.
Oades RD, Halliday GM (1987) Ventral tegmental (A10) system: Neurobiology. 1. Anatomy and connectivity. Brain Res Rev 12, 117-165.
Ntamati NR, Lüscher C (2016) VTA projection neurons releasing GABA and glutamate in the dentate gyrus. Eneuro 3, ENEURO. 0137-16. 2016.
Lanari A, Amenta F, Silvestrelli G, Tomassoni D, Parnetti L (2006) Neurotransmitter deficits in behavioural and psychological symptoms of Alzheimer's disease. Mech Ageing Dev 127, 158-165.
Mitchell RA, Herrmann N, Lanctôt KL (2011) The role of dopamine in symptoms and treatment of apathy in Alzheimer's disease. CNS Neurosci Ther 17, 411-427.
De Marco M, Venneri A (2018) Volume and connectivity of the ventral tegmental area are linked to neurocognitive signatures of Alzheimer's disease in humans. J Alzheimers Dis 63, 1-14.
Serra L, D'Amelio M, Di Domenico C, Dipasquale O, Marra C, Mercuri NB, Caltagirone C, CercignaniM, Bozzali M (2018) In vivo mapping of brainstem nuclei functional connectivity disruption in Alzheimer's disease. Neurobiol Aging 72, 72-82.
Sala A, Perani D (2019) Brain molecular connectivity in neurodegenerative diseases: Recent advances and new perspectives using positron emission tomography. Front Neurosci 13, 617.
Riedl V, Utz L, Castrillón G, Grimmer T, Rauschecker JP, Ploner M, Friston KJ, Drzezga A, Sorg C (2016) Metabolic connectivity mapping reveals effective connectivity in the resting human brain. Proc Natl Acad SciUS A 113, 428-433.
Perani D (2014) FDG-PET and amyloid-PET imaging: The diverging paths. Curr Opin Neurol 27, 405-413.
Holtbernd F, Ma Y, Peng S, Schwartz F, Timmermann L, Kracht L, Fink GR, Tang CC, Eidelberg D, Eggers C (2015) Dopaminergic correlates of metabolic network activity in Parkinson's disease. Hum Brain Mapp 36, 3575-3585.
Sala A, Caminiti SP, Presotto L, Premi E, Pilotto A, Cosseddu M, Paghera B, Borroni B (2017) Altered brain metabolic connectivity at multiscale level in early Parkinson's disease. Sci Rep 7, 4256.
Caminiti SP, Tettamanti M, Sala A, Presotto L, Iannaccone S, Cappa SF, Magnani G, Perani D (2017) Metabolic con nectomics targeting brain pathology in dementia with Lewy bodies. J Cereb Blood Flow Metab 37, 1311-1325.
McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer's disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34, 939-944.
Beach TG, Monsell SE, Phillips LE, Kukull W (2012) Accuracy of the clinical diagnosis of Alzheimer disease at National Institute on Aging Alzheimer Disease Centers, 2005-2010. J Neuropathol Exp Neurol 71, 266-273.
Clark CM, Schneider JA, Bedell BJ, Beach TG, Bilker WB, Mintun MA, Pontecorvo MJ, Hefti F, Carpenter AP, Flitter ML, Krautkramer MJ, Kung HF, Coleman RE, Doraiswamy PM, Fleisher AS, Sabbagh MN, Sadowsky CH, Reiman PEM, Zehntner SP, Skovronsky DM; AV45-A07Study Group (2011) Use of florbetapir-PET for imaging amyloid pathology. JAMA 305, 275-283.
McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack Jr CR, Kawas CH, Klunk WE, Koroshetz WJ, Manly JJ, Mayeux R (2011) The diagnosis of dementia due to Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 7, 263-269.
Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, Gamst A, Holtzman DM, Jagust WJ, Petersen RC, Snyder PJ, Carrillo MC, Thies B, PhelpsCH(2011) The diagnosis of mild cognitive impairment due to Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 7, 270-279.
Joshi AD, Pontecorvo MJ, Clark CM, Carpenter AP, Jennings DL, Sadowsky CH, Adler LP, Kovnat KD, Seibyl JP, Arora A, Saha K, Burns JD, Lowrey MJ, Mintun MA, Skovronsky DM (2012) Performance characteristics of amyloid PET with florbetapir F 18 in patients with Alzheimer's disease and cognitively normal subjects. J Nucl Med 53, 378-384.
Perani D, Della Rosa PA, Cerami C, Gallivanone F, Fallanca F, Vanoli EG, Panzacchi A, Nobili F, Pappatà S, Marcone A, GaribottoV, Castiglioni I, Magnani G, Cappa SF, Gianolli L (2014) Validation of an optimized SPM procedure for FDGPET in dementia diagnosis in a clinical setting. Neuroimage Clin 6, 445-54.
Caminiti SP, Alongi P, Majno L, Volontè MA, Cerami C, Gianolli L, Comi G, Perani D (2017) Evaluation of an optimized [18F]fluoro-deoxy-glucose positron emission tomography voxel-wise method to early support differential diagnosis in atypical Parkinsonian disorders. Eur J Neurol 24, 687-e26.
Cerami C, Dodich A, Greco L, Iannaccone S, Magnani G, Marcone A, Pelagallo E, Santangelo R, Cappa SF, Perani D (2016) The role of single-subject brain metabolic patterns in the early differential diagnosis of primary progressive aphasias and in prediction of progression to dementia. J Alzheimers Dis 55, 183-197.
Perani D, Cerami C, Caminiti SP, Santangelo R, Coppi E, Ferrari L, Pinto P, Passerini G, Falini A, Iannaccone S, Cappa SF, Comi G, Gianolli L, Magnani G (2016) Crossvalidation of biomarkers for the early differential diagnosis and prognosis of dementia in a clinical setting. Eur J Nucl Med Mol Imaging 43, 499-508.
Caminiti SP, Sala A, Iaccarino L, Beretta L, Pilotto A, Gianolli L, Iannaccone S, Magnani G, Padovani A, Ferini-Strambi L, Perani D (2019) Brain glucose metabolism in Lewy body dementia: Implications for diagnostic criteria. Alzheimers Res Ther 11, 20.
Cerami C, Della Rosa PA, Magnani G, Santangelo R, Marcone A, Cappa SF, Perani D (2015) Brain metabolic maps in mild cognitive impairment predict heterogeneity of progression to dementia. Neuroimage Clin 7, 187-194.
Iaccarino L, Sala A, Perani D (2019) Predicting long-term clinical stability in amyloid-positive subjects by FDG-PET. Ann Clin Transl Neurol 6, 1113-1120.
Frisoni GB, Bocchetta M, Chételat G, Rabinovici GD, De Leon MJ, Kaye J, ReimanEM, Scheltens P, Barkhof F, Black SE, Brooks DJ, Carrillo MC, Fox NC, Herholz K, Nordberg A, Jack CR, Jagust WJ, Johnson KA, Rowe CC, Sperling RA, Thies W, Wahlund LO, Weiner MW, Pasqualetti P, DeCarli C (2013) Imaging markers for Alzheimer disease: Which vs how. Neurology 81, 487-500.
Nelson PT, Dickson DW, Trojanowski JQ, Jack CR, Boyle PA, Arfanakis K, Rademakers R, Alafuzoff I, Attems J, Brayne C, Coyle-Gilchrist ITS, Chui HC, Fardo DW, Flanagan ME, Halliday G, Hokkanen SRK, Hunter S, Jicha GA, Katsumata Y, Kawas CH, Keene CD, Kovacs GG, Kukull WA, Levey AI, Makkinejad N, Montine TJ, Murayama S, Murray ME, Nag S, Rissman RA, SeeleyWW, Sperling RA, White CL, Yu L, Schneider JA (2019) Limbic-predominant age-related TDP-43 encephalopathy (LATE): Consensus working group report. Brain 142, 1503-1527.
Cerami C, Dodich A, Iannaccone S, Magnani G, Santangelo R, Presotto L, Marcone A, Gianolli L, Cappa SF, Perani D (2018) A biomarker study in long-lasting amnestic mild cognitive impairment. Alzheimer Res Ther 10, 42.
Iaccarino L, Sala A, Caminiti SP, Perani D (2017) The emerging role of PET imaging in dementia. F1000Research 6, 1830.
Teng EL, Chui HC (1987) The Modified Mini-Mental State (3MS) examination. J Clin Psychiatry 48, 314-318.
Morris JC (1993) The Clinical Dementia Rating (CDR): Current version and scoring rules. Neurology 43, 2412-2414.
Cummings JL, Mega M, Gray K, Rosenberg-Thompson S, Carusi DA, Gornbein J (1994) The Neuropsychiatric Inventory: Comprehensive assessment of psychopathology in dementia. Neurology 44, 2308.
La Joie R, Perrotin A, Barré L, Hommet C, Mézenge F, Ibazizene M, Camus V, Abbas A, Landeau B, Guilloteau D, de La Sayette V, Eustache F, Desgranges B, Chételat G (2012) Region-specific hierarchy between atrophy, hypometabolism, and 2-amyloid (A) load in Alzheimer's disease dementia. J Neurosci 32, 16265-16273.
Ossenkoppele R, Cohn-Sheehy BI, La Joie R, Vogel JW, Möller C, Lehmann M, van Berckel BNM, Seeley WW, Pijnenburg YA, Gorno-Tempini ML (2015) Atrophy patterns in early clinical stages across distinct phenotypes of Alzheimer's disease. Hum Brain Mapp 36, 4421-4437.
Tziortzi AC, Haber SN, Searle GE, Tsoumpas C, Long CJ, Shotbolt P, Douaud G, Jbabdi S, Behrens TEJ, Rabiner EA, Jenkinson M, Gunn RN (2013) Connectivity-based functional analysis of dopamine release in the striatum using diffusion-weightedMRIand positron emission tomography. Cereb Cortex 24, 1165-1177.
Lai CKY (2014) The merits and problems of Neuropsychiatric Inventory as an assessment tool in people with dementia and other neurological disorders. Clin Interv Aging 9, 1051.
FristonK(2002) Beyond phrenology: What can neuroimaging tell us about distributed circuitry? Annu Rev Neurosci 25, 221-250.
Presotto L, BallariniT, Caminiti SP, BettinardiV, Gianolli L, PeraniD(2017)Validation of 18F-FDG-PET single-subject optimized SPM procedure with different PET scanners. Neuroinformatics 15, 151-163.
Gallivanone F, Della Rosa PA, Perani D, Gilardi MC, Castiglioni I (2017) The impact of different 18FDG PET healthy subject scans for comparison with single patient in SPM analysis. Q J Nucl Med Mol Imaging 61, 115-132.
Dukart J, Mueller K, Horstmann A, Vogt B, Frisch S, Barthel H, Becker G, Muller HE, Villringer A, Sabri O, Schroeter ML (2010) Differential effects of global and cerebellar normalization on detection and differentiation of dementia in FDG-PET studies. Neuroimage 49, 1490-1495.
Zheng L, Vinters H V, Mack WJ, Weiner MW, Chui HC, project IVD program (2016) Differential effects of ischemic vascular disease and Alzheimer's disease on brain atrophy and cognition. J Cereb Blood Flow Metab 36, 204-215.
McKee AC, Stein TD, Kiernan PT, Alvarez VE (2015) The neuropathology of chronic traumatic encephalopathy. Brain Pathol 25, 350-364.
Giorgio A, Santelli L, Tomassini V, Bosnell R, Smith S, De Stefano N, Johansen-Berg H (2010) Age-related changes in grey and white matter structure throughout adulthood. Neuroimage 51, 943-951.
Smiley JF, Mesulam M-M (1999) Cholinergic neurons of the nucleus basalis of Meynert receive cholinergic, catecholaminergic and GABAergic synapses: An electron microscopic investigation in the monkey. Neuroscience 88, 241-255.
Yeomans JS (1995) Role of tegmental cholinergic neurons in dopaminergic activation, antimuscarinic psychosis and schizophrenia. Neuropsychopharmacology 12, 3.
Yeomans J, Baptista M (1997) Both nicotinic and muscarinic receptors in ventral tegmental area contribute to brain-stimulation reward. Pharmacol Biochem Behav 57, 915-921.
Shi F, Liu B, Zhou Y, Yu C, Jiang T (2009) Hippocampal volume and asymmetry in mild cognitive impairment and Alzheimer's disease: Metap-analyses of MRI studies. Hippocampus 19, 1055-1064.
Pini L, Pievani M, Bocchetta M, Altomare D, Bosco P, Cavedo E, Galluzzi S, Marizzoni M, Frisoni GB (2016) Brain atrophy in Alzheimer's disease and aging. Ageing Res Rev 30, 25-48.
Kempadoo KA, Mosharov E V., Choi SJ, Sulzer D, Kandel ER (2016) Dopamine release from the locus coeruleus to the dorsal hippocampus promotes spatial learning and memory. Proc Natl Acad Sci U S A 113, 14835-14840.
Takeuchi T, Duszkiewicz AJ, Sonneborn A, Spooner PA, Yamasaki M, Watanabe M, Smith CC, Fernández G, Deisseroth K, Greene RW, Morris RGM (2016) Locus coeruleus and dopaminergic consolidation of everyday memory. Nature 537, 357-362.
Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Tredici K (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112, 389-404.
Theofilas P, Ehrenberg AJ, Dunlop S, Di Lorenzo Alho AT, Nguy A, Leite REP, Rodriguez RD, Mejia MB, Suemoto CK, Ferretti-Rebustini REDL, Polichiso L, Nascimento CF, Seeley WW, Nitrini R, Pasqualucci CA, Jacob Filho W, Rueb U, Neuhaus J, Heinsen H, Grinberg LT (2017) Locus coeruleus volume and cell population changes during Alzheimer's disease progression: A stereological study in human postmortem brains with potential implication for early-stage biomarker discovery. Alzheimers Dement 13, 236-246.
Devoto P, FloreG(2006) On the origin of cortical dopamine: Is it a co-transmitter in noradrenergic neurons? Curr Neuropharmacol 4, 115-125.
Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82, 239-259.
Martorana A, Koch G (2014) Is dopamine involved in Alzheimer's disease? Front Aging Neurosci 6, 252.
McNamara CG, Tejero-Cantero á, Trouche S, Campo-Urriza N, Dupret D (2014) Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence. Nat Neurosci 17, 1658.
Broussard JI, Yang K, Levine AT, Tsetsenis T, Jenson D, Cao F, Garcia I, Arenkiel BR, Zhou F-M, De BiasiM(2016) Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the hippocampus. Cell Rep 14, 1930-1939.
Lisman JE, Grace AA (2005) The hippocampal-VTA loop: Controlling the entry of information into long-term memory. Neuron 46, 703-713.
Rossato JI, Radiske A, Kohler CA, Gonzalez C, Bevilaqua LR, Medina JH, Cammarota M (2013) Consolidation of object recognition memory requires simultaneous activation of dopamine D1/D5 receptors in the amygdala and medial prefrontal cortex but not in the hippocampus. Neurobiol Learn Mem 106, 66-70.
Ambreé O, Richter H, Sachser N, Lewejohann L, Dere E, de Souza Silva MA, Herring A, Keyvani K, PaulusW, Schäbitz W-R (2009) Levodopa ameliorates learning and memory deficits in a murine model of Alzheimer's disease. Neurobiol Aging 30, 1192-1204.
Guzmán-Ramos K, Moreno-Castilla P, Castro-Cruz M, McGaugh JL, Martínez-Coria H, LaFerla FM, Bermúdez-Rattoni F (2012) Restoration of dopamine release deficits during object recognition memory acquisition attenuates cognitive impairment in a triple transgenic mice model of Alzheimer's disease. Learn Mem 19, 453-460.
Lee GJ, Lu PH, Hua X, Lee S, Wu S, Nguyen K, Teng E, Leow AD, Jack Jr CR, Toga AW (2012) Depressive symptoms in mild cognitive impairment predict greater atrophy in Alzheimer's disease-related regions. Biol Psychiatry 71, 814-821.
Mega MS, Lee L, Dinov ID, Mishkin F, Toga AW, Cummings JL (2000) Cerebral correlates of psychotic symptoms in Alzheimer's disease. J Neurol Neurosurg Psychiatry 69, 167-171.
Bruen PD, McGeown WJ, Shanks MF, Venneri A (2008) Neuroanatomical correlates of neuropsychiatric symptoms in Alzheimer's disease. Brain 131, 2455-2463.
de Jong LW, Ferrarini L, van der Grond J, Milles JR, Reiber JHC, Westendorp RGJ, Bollen ELEM, Middelkoop HAM, van BuchemMA(2011) Shape abnormalities of the striatum in Alzheimer's disease. J Alzheimers Dis 23, 49-59.
Liu Y, Paajanen T, Zhang Y, Westman E, Wahlund L-O, Simmons A, Tunnard C, Sobow T, Mecocci P, Tsolaki M (2010) Analysis of regional MRI volumes and thicknesses as predictors of conversion from mild cognitive impairment to Alzheimer's disease. Neurobiol Aging 31, 1375-1385.
Yi H-A, Möller C, Dieleman N, Bouwman FH, Barkhof F, Scheltens P, van der Flier WM, Vrenken H (2016) Relation between subcortical grey matter atrophy and conversion from mild cognitive impairment to Alzheimer's disease. J Neurol Neurosurg Psychiatry 87, 425-432.
Lyketsos CG, Carrillo MC, Ryan JM, Khachaturian AS, Trzepacz P, Amatniek J, Cedarbaum J, Brashear R, Miller DS (2011) Neuropsychiatric symptoms in Alzheimer's disease. Alzheimers Dement 7, 532-539.
Geda YE, Roberts RO, Mielke MM, Knopman DS, Christianson TJH, Pankratz VS, Boeve BF, Sochor O, Tangalos EG, Petersen RC (2014) Baseline neuropsychiatric symptoms and the risk of incident mild cognitive impairment: A population-based study. Am J Psychiatry 171, 572-581.
Monastero R, Mangialasche F, Camarda C, Ercolani S, Camarda R (2009) A systematic review of neuropsychiatric symptoms in mild cognitive impairment. J Alzheimers Dis 18, 11-30.
Peters ME, Rosenberg PB, SteinbergM, NortonMC, Welsh-Bohmer KA, Hayden KM, Breitner J, Tschanz JT, Lyketsos CG, Investigators CC (2013) Neuropsychiatric symptoms as risk factors for progression from CIND to dementia: The Cache County Study. Am J Geriatr Psychiatry 21, 1116-1124.
Ballarini T, Iaccarino L, Magnani G, Ayakta N, Miller BL, Jagust WJ, Gorno-tempini ML, Rabinovici GD, Perani D, Francisco S (2016) Neuropsychiatric subsyndromes and brain metabolic network dysfunctions in early onset Alzheimer's disease. Hum Brain Mapp 37, 4234-4247.
Morbelli S, Drzezga A, Perneczky R, Frisoni GB, Caroli A, van Berckel BNM, Ossenkoppele R, Guedj E, Didic M, Brugnolo A, Sambuceti G, Pagani M, Salmon E, Nobili F (2012) Resting metabolic connectivity in prodromal Alzheimer's disease. A European Alzheimer Disease Consortium (EADC) project. Neurobiol Aging 33, 2533-2550.
Herholz K, Haense C, Gerhard A, Jones M, Anton-Rodriguez J, Segobin S, Snowden JS, Thompson JC, Kobylecki C (2017) Metabolic regional and network changes in Alzheimer's disease subtypes. J Cereb Blood Flow Metab 38, 1796-1806.
Morbelli S, Perneczky R, Drzezga A, Frisoni GB, Caroli A, van Berckel BNM, Ossenkoppele R, Guedj E, Didic M, Brugnolo A, Naseri M, Sambuceti G, Pagani M, Nobili F (2013) Metabolic networks underlying cognitive reserve in prodromal Alzheimer disease: A European Alzheimer disease consortium project. J Nucl Med 54, 894-902.
Malpetti M, Ballarini T, Presotto L, Garibotto V, Tettamanti M, Perani D (2017) Gender differences in healthy aging and Alzheimer's dementia: A 18F-FDG-PET study of brain and cognitive reserve. Hum Brain Mapp 38, 4212-4227.
Perani D, Farsad M, Ballarini T, Lubian F, Malpetti M, Fracchetti A (2017) The impact of bilingualism on brain reserve and metabolic connectivity in Alzheimer's dementia. Proc Natl Acad Sci U S A 114, 1690-1695.
Malpetti M, Sala A, Vanoli EG, Gianolli L, Luzi L, PeraniD (2018) Unfavourable gender effect of high body mass index on brain metabolism and connectivity. Sci Rep 8, 12584.
Pagani MM, Giuliani A, Öberg J, De Carli F, Morbelli S, Girtler N, Bongioanni F, Arnaldi D, Accardo J, Bauckneht M, Chincarini A, Sambuceti G, Jonsson C, Nobili F (2017) Progressive disgregation of brain networking from normal aging to Alzheimer's disease. Independent component analysis on FDG-PET data. J Nucl Med 58, 1132-1139.
Yakushev I, Drzezga A, Habeck C (2017) Metabolic connectivity: Methods and applications. Curr Opin Neurol 30, 677-685.
Verger A, Horowitz T, Chawki MB, Eusebio A, Bordonne M, Azulay J-P, Girard N, Guedj E (2020) From metabolic connectivity to molecular connectivity: Application to dopaminergic pathways. Eur J Nucl Med Mol Imaging 47, 413-424.
Rodriguez-OrozMC, Gago B, Clavero P, Delgado-Alvarado M, Garcia-Garcia D, Jimenez-Urbieta H (2015) The relationship between atrophy and hypometabolism: Is it regionally dependent in dementias? Curr Neurol Neurosci Rep 15, 44.
Xia M, Wang J, He Y (2013) BrainNet Viewer: A network visualization tool for human brain connectomics. PLoS One 8, e68910.
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