In vivo MRI Structural and PET Metabolic Connectivity Study of Dopamine Pathways in Alzheimer’s Disease
Abstract
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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Our data confirm the very recent clinical evidence from MCI and AD patients showing that functional, structural and metabolic changes affecting the VTA and its projection areas in the mesocorticolimbic pathway occur at the earlier stages of the disease.
“Our data confirm the very recent clinical evidence from MCI and AD patients showing that functional, structural and metabolic changes affecting the VTA and its projection areas in the mesocorticolimbic pathway occur at the earlier stages of the disease (De Marco and Ven neri, 2018; Iaccarino et al., 2020; Serra et al., 2018).”
From Nilotinib restores memory function by preventing dopaminergic neuron degeneration in a mouse model of Alzheimer’s Disease (2021) · cites this paper as Iaccarino et al., 2020
Cites
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M. (1984) · Neurology · doi:10.1212/wnl.34.7.939 · Cited by 27,915 · see citing works
McKhann, G. M., Knopman, D. S., Chertkow, H., Hyman, B. T., Jack, C. R., Kawas, C. H., Klunk, W. E., Koroshetz, W. J., Manly, J. J., Mayeux, R., et al. (2011) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2011.03.005 · Cited by 18,657 · see citing works
Neuropathological stageing of Alzheimer-related changes.
Braak, H., & Braak, E. (1991) · Acta Neuropathologica · doi:10.1007/bf00308809 · Cited by 16,123 · see citing works
NIA‐AA Research Framework: Toward a biological definition of Alzheimer's disease
Jack, C. R., Bennett, D. A., Blennow, K., Carrillo, M. C., Dunn, B., Haeberlein, S. B., Holtzman, D. M., Jagust, W., Jessen, F., Karlawish, J., et al. (2018) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2018.02.018 · Cited by 10,537 · see citing works
Albert, M. S., DeKosky, S. T., Dickson, D., Dubois, B., Feldman, H. H., Fox, N. C., Gamst, A., Holtzman, D. M., Jagust, W. J., Petersen, R. C., et al. (2011) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2011.03.008 · Cited by 10,152 · cited 3× · see citing works
“, temporal-parietal/precuneus hypometabolism) [30, 31].”
MethodResultThe Clinical Dementia Rating (CDR): Current version and scoring rules
Morris, J. C. (1993) · Neurology · doi:10.1212/wnl.43.11.2412-a · Cited by 9,882 · see citing works
The Neuropsychiatric Inventory: Comprehensive assessment of psychopathology in dementia
Cummings, J. L., Mega, M., Gray, K., Rosenberg-Thompson, S., Carusi, D. A., & Gornbein, J. (1994) · Neurology · doi:10.1212/wnl.44.12.2308 · Cited by 7,568 · see citing works
BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics
Xia, M., Wang, J., & He, Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068910 · Cited by 4,106 · see citing works
Braak, H., Alafuzoff, I., Arzberger, T., Kretzschmar, H., & Del Tredici, K. (2006) · Acta Neuropathologica · doi:10.1007/s00401-006-0127-z · Cited by 3,172 · see citing works
(1987) · PubMed · Cited by 2,657 · see citing works
The hippocampal-VTA loop: controlling the entry of information into long-term memory
Lisman, J. E., & Grace, A. A. (2005) · Neuron · doi:10.1016/j.neuron.2005.05.002 · Cited by 1,983 · see citing works
Dopamine neuron systems in the brain: An update
Björklund, A., & Dunnett, S. B. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.03.006 · Cited by 1,777 · see citing works
Limbic-predominant age-related TDP-43 encephalopathy (LATE): consensus working group report
Nelson, P. T., Dickson, D. W., Trojanowski, J. Q., Jack, C. R., Boyle, P. A., Arfanakis, K., Rademakers, R., Alafuzoff, I., Attems, J., Brayne, C., et al. (2019) · Brain · doi:10.1093/brain/awz099 · Cited by 1,547 · see citing works
Neuropsychiatric symptoms in Alzheimer's disease
Lyketsos, C. G., Carrillo, M. C., Ryan, J. M., Khachaturian, A. S., Trzepacz, P., Amatniek, J., Cedarbaum, J., Brashear, R., & Miller, D. S. (2011) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2011.05.2410 · Cited by 1,139 · see citing works
Use of Florbetapir-PET for Imaging β-Amyloid Pathology
Clark, C. M. (2011) · JAMA · doi:10.1001/jama.2010.2008 · Cited by 1,117 · see citing works
Beach, T. G., Monsell, S. E., Phillips, L. E., & Kukull, W. (2012) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e31824b211b · Cited by 1,103 · cited 1× · see citing works
“Since ADNI enrollment criteria are based on the 1984 NINCDS/ADRDA clinical criteria for AD [27], known to yield some mismatch against definite neuropathological diagnosis [28], we set additional and more stringent inclusion criteria to select our clinical sample.”
MethodMesocorticolimbic dopaminergic network: functional and regulatory roles
Moal, M. L., & Simon, H. (1991) · Physiological Reviews · doi:10.1152/physrev.1991.71.1.155 · Cited by 1,096 · see citing works
Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity
Oades, R. D., & Halliday, G. M. (1987) · Brain Research Reviews · doi:10.1016/0165-0173(87)90011-7 · Cited by 1,001 · see citing works
Brain atrophy in Alzheimer’s Disease and aging
Pini, L., Pievani, M., Bocchetta, M., Altomare, D., Bosco, P., Cavedo, E., Galluzzi, S., Marizzoni, M., & Frisoni, G. B. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.01.002 · Cited by 874 · see citing works
Locus coeruleus and dopaminergic consolidation of everyday memory
Takeuchi, T., Duszkiewicz, A. J., Sonneborn, A., Spooner, P. A., Yamasaki, M., Watanabe, M., Smith, C. C., Fernández, G., Deisseroth, K., Greene, R. W., et al. (2016) · Nature · doi:10.1038/nature19325 · Cited by 827 · see citing works
Amyloid Deposition, Hypometabolism, and Longitudinal Cognitive Decline
Landau, S. M., Mintun, M., Joshi, A. D., Koeppe, R., Petersen, R. C., Aisen, P., Weiner, M., & Jagust, W. J. (2012) · Annals of Neurology · doi:10.1002/ana.23650 · Cited by 723 · see citing works
Kempadoo, K. A., Mosharov, E. V., Choi, S. J., Sulzer, D., & Kandel, E. R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616515114 · Cited by 647 · see citing works
The Neuropathology of Chronic Traumatic Encephalopathy
McKee, A. C., Stein, T. D., Kiernan, P. T., & Alvarez, V. E. (2015) · Brain Pathology · doi:10.1111/bpa.12248 · Cited by 585 · see citing works
Neuropathologic changes in Alzheimer's disease.
Wenk, G. L. (2003) · PubMed · Cited by 554 · see citing works
Age-related changes in grey and white matter structure throughout adulthood
Giorgio, A., Santelli, L., Tomassini, V., Bosnell, R., Smith, S., De Stefano, N., & Johansen-Berg, H. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.03.004 · Cited by 532 · see citing works
Nobili, A., Latagliata, E. C., Viscomi, M. T., Cavallucci, V., Cutuli, D., Giacovazzo, G., Krashia, P., Rizzo, F. R., Marino, R., Federici, M., et al. (2017) · Nature Communications · doi:10.1038/ncomms14727 · Cited by 514 · cited 5× · see citing works
“As mentioned in the introduction, both hippocampal formation and VST are innervated by VTA dopaminergic projections, the degeneration of which has been shown to produce lower DA outflow, equally affecting the hippocampus and VST in AD transgenic animal models [11].”
BackgroundInfluentialDopaminergic neurons promote hippocampal reactivation and spatial memory persistence
McNamara, C. G., Tejero-Cantero, Á., Trouche, S., Campo-Urriza, N., & Dupret, D. (2014) · Nature Neuroscience · doi:10.1038/nn.3843 · Cited by 486 · see citing works
Shi, F., Liu, B., Zhou, Y., Yu, C., & Jiang, T. (2009) · Hippocampus · doi:10.1002/hipo.20573 · Cited by 470 · see citing works
Beyond Phrenology: What Can Neuroimaging Tell Us About Distributed Circuitry?
Friston, K. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142846 · Cited by 465 · see citing works
Theofilas, P., Ehrenberg, A. J., Dunlop, S., Di Lorenzo Alho, A. T., Nguy, A., Leite, R. E. P., Rodriguez, R. D., Mejia, M. B., Suemoto, C. K., Ferretti-Rebustini, R. E. D. L., et al. (2017) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2016.06.2362 · Cited by 416 · see citing works
Joshi, A. D., Pontecorvo, M. J., Clark, C. M., Carpenter, A. P., Jennings, D. L., Sadowsky, C., Adler, L. P., Kovnat, K. D., Seibyl, J. P., Arora, A., et al. (2012) · Journal of Nuclear Medicine · doi:10.2967/jnumed.111.090340 · Cited by 391 · see citing works
La Joie, R., Perrotin, A., Barré, L., Hommet, C., Mézenge, F., Ibazizene, M., Camus, V., Abbas, A., Landeau, B., Guilloteau, D., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.2170-12.2012 · Cited by 374 · see citing works
Neuroanatomical correlates of neuropsychiatric symptoms in Alzheimer's disease
Bruen, P. D., McGeown, W. J., Shanks, M. F., & Venneri, A. (2008) · Brain · doi:10.1093/brain/awn151 · Cited by 374 · see citing works
Geda, Y. E., Roberts, R. O., Mielke, M. M., Knopman, D. S., Christianson, T. J. H., Pankratz, V. S., Boeve, B. F., Sochor, O., Tangalos, E. G., Petersen, R. C., et al. (2014) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2014.13060821 · Cited by 338 · see citing works
Tziortzi, A. C., Haber, S. N., Searle, G. E., Tsoumpas, C., Long, C. J., Shotbolt, P., Douaud, G., Jbabdi, S., Behrens, T. E. J., Rabiner, E. A., et al. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs397 · Cited by 316 · see citing works
A Systematic Review of Neuropsychiatric Symptoms in Mild Cognitive Impairment
Monastero, R., Mangialasche, F., Camarda, C., Ercolani, S., & Camarda, R. (2009) · Journal of Alzheimer s Disease · doi:10.3233/jad-2009-1120 · Cited by 297 · see citing works
“Is dopamine involved in Alzheimer's disease?”
Martorana, A., & Koch, G. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00252 · Cited by 276 · see citing works
The impact of bilingualism on brain reserve and metabolic connectivity in Alzheimer's dementia
Perani, D., Farsad, M., Ballarini, T., Lubian, F., Malpetti, M., Fracchetti, A., Magnani, G., March, A., & Abutalebi, J. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610909114 · Cited by 266 · see citing works
Self-citationOssenkoppele, R., Cohn‐Sheehy, B. I., La Joie, R., Vogel, J. W., Möller, C., Lehmann, M., van Berckel, B. N. M., Seeley, W. W., Pijnenburg, Y. A., Gorno‐Tempini, M. L., et al. (2015) · Human Brain Mapping · doi:10.1002/hbm.22927 · Cited by 243 · cited 2× · see citing works
“To create maps of statistical deviation of brain volume from the reference control group, we estimated voxel-level atrophy W-score maps [48, 49].”
MethodImaging markers for Alzheimer disease
Frisoni, G. B., Bocchetta, M., Chételat, G., Rabinovici, G. D., de Leon, M. J., Kaye, J. A., Reiman, E. M., Scheltens, P., Barkhof, F., Black, S. E., et al. (2013) · Neurology · doi:10.1212/wnl.0b013e31829d86e8 · Cited by 224 · see citing works
Trillo, L., Das, D., Hsieh, W., Medina, B., Moghadam, S., Lin, B., Dang, V., Sanchez, M. M., Miguel, Z. D., Ashford, J. W., et al. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.05.008 · Cited by 224 · see citing works
Validation of an optimized SPM procedure for FDG-PET in dementia diagnosis in a clinical setting
Perani, D., Rosa, P. A. D., Cerami, C., Gallivanone, F., Fallanca, F., Vanoli, E. G., Panzacchi, A., Nobili, F. M., Pappatà, S., Marcone, A., et al. (2014) · NeuroImage Clinical · doi:10.1016/j.nicl.2014.10.009 · Cited by 217 · see citing works
Self-citationMonoaminergic neurotransmitters, their precursors and metabolites in brains of Alzheimer patients
Štorga-Tomić, D., Vrečko, K., Birkmayer, J. G. D., & Reibnegger, G. J. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(95)12256-7 · Cited by 209 · see citing works
Yeomans, J. S. (1995) · Neuropsychopharmacology · doi:10.1038/sj.npp.1380235 · Cited by 198 · see citing works
Cerebral correlates of psychotic symptoms in Alzheimer's disease
Mega, M. S. (2000) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.69.2.167 · Cited by 189 · see citing works
Neurotransmitter deficits in behavioural and psychological symptoms of Alzheimer's disease
Lanari, A., Amenta, F., Silvestrelli, G., Tomassoni, D., & Parnetti, L. (2005) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2005.09.016 · Cited by 180 · see citing works
Broussard, J. I., Yang, K., Levine, A. T., Tsetsenis, T., Jenson, D., Cao, F., Garcia, I., Arenkiel, B. R., Zhou, F.-M., De Biasi, M., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.070 · Cited by 180 · see citing works
Lee, G. J., Lu, P. H., Hua, X., Lee, S., Wu, S., Nguyen, K., Teng, E., Leow, A., Jack, C. R., Toga, A. W., et al. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.12.024 · Cited by 172 · see citing works
Peters, M. E., Rosenberg, P. B., Steinberg, M., Norton, M. C., Welsh-Bohmer, K. A., Hayden, K. M., Breitner, J., Tschanz, J. T., & Lyketsos, C. G. (2013) · The American Journal of Geriatric Psychiatry · doi:10.1016/j.jagp.2013.01.049 · Cited by 167 · see citing works
Metabolic connectivity: methods and applications
Yakushev, I. Y., Drzezga, A. E., & Habeck, C. G. (2017) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000494 · Cited by 152 · see citing works
The Role of Dopamine in Symptoms and Treatment of Apathy in Alzheimer's Disease
Mitchell, R., Herrmann, N., & Lanctôt, K. (2011) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2010.00161.x · Cited by 141 · see citing works
Yeomans, J. S., & Baptista, M. A. S. (1997) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(96)00467-4 · Cited by 139 · see citing works
On the Origin of Cortical Dopamine: Is it a Co-Transmitter in Noradrenergic Neurons?
Devoto, P., & Flore, G. (2006) · Current Neuropharmacology · doi:10.2174/157015906776359559 · Cited by 137 · see citing works
Lai, C. K. Y. (2014) · Clinical Interventions in Aging · doi:10.2147/cia.s63504 · Cited by 136 · see citing works
Murray, A. M., Weihmueller, F. B., Marshall, J. F., Hurtig, H. I., Gottleib, G. L., & Joyce, J. N. (1995) · Annals of Neurology · doi:10.1002/ana.410370306 · Cited by 135 · see citing works
Dukart, J., Mueller, K., Horstmann, A., Vogt, B., Frisch, S., Barthel, H., Becker, G., Möller, H. E., Villringer, A., Sabri, O., et al. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.09.017 · Cited by 134 · see citing works
Morbelli, S. D., Drzezga, A. E., Perneczky, R., Frisoni, G. B., Caroli, A., van Berckel, B. N. M., Ossenkoppele, R., Guedj, É., Didic, M., Brugnolo, A., et al. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.01.005 · Cited by 129 · see citing works
Yi, H., Möller, C., Dieleman, N., Bouwman, F. H., Barkhof, F., Scheltens, P., van der Flier, W. M., & Vrenken, H. (2015) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2014-309105 · Cited by 128 · see citing works
Brain metabolic maps in Mild Cognitive Impairment predict heterogeneity of progression to dementia
Cerami, C., Della Rosa, P. A., Magnani, G., Santangelo, R., Marcone, A., Cappa, S. F., & Perani, D. (2015) · NeuroImage: Clinical · doi:10.1016/j.nicl.2014.12.004 · Cited by 127 · see citing works
Self-citationGuzmán-Ramos, K., Moreno-Castilla, P., Castro-Cruz, M., McGaugh, J. L., Martínez-Coria, H., LaFerla, F. M., & Bermúdez-Rattoni, F. (2012) · Learning & Memory · doi:10.1101/lm.026070.112 · Cited by 127 · see citing works
The substantia nigra and ventral tegmental area in Alzheimer’s disease and Down’s syndrome
Gibb, W. R., Mountjoy, C. Q., Mann, D. M., & Lees, A. J. (1989) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.52.2.193 · Cited by 122 · see citing works
Morbelli, S. D., Perneczky, R., Drzezga, A. E., Frisoni, G. B., Caroli, A., van Berckel, B. N. M., Ossenkoppele, R., Guedj, É., Didic, M., Brugnolo, A., et al. (2013) · Journal of Nuclear Medicine · doi:10.2967/jnumed.112.113928 · Cited by 120 · see citing works
Metabolic connectivity mapping reveals effective connectivity in the resting human brain
Riedl, V., Utz, L., Castrillón, G., Grimmer, T., Rauschecker, J. P., Ploner, M., Friston, K. J., Drzezga, A. E., & Sorg, C. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1513752113 · Cited by 120 · see citing works
Malpetti, M., Ballarini, T., Presotto, L., Garibotto, V., Tettamanti, M., Perani, D., Initiative, A. D. N., & Network for Efficiency and Standardization of Dementia Diagnosis (NEST‐DD) database (2017) · Human Brain Mapping · doi:10.1002/hbm.23659 · Cited by 119 · see citing works
Self-citationLevodopa ameliorates learning and memory deficits in a murine model of Alzheimer’s disease
Ambrée, O., Richter, H., Sachser, N., Lewejohann, L., Dere, E., de Souza Silva, M. A., Herring, A., Keyvani, K., Paulus, W., & Schäbitz, W.-R. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.11.010 · Cited by 115 · see citing works
Liu, Y., Paajanen, T. I., Zhang, Y., Westman, E., Wahlund, L., Simmons, A., Tunnard, C., Sobów, T., Mecocci, P., Tsolaki, M., et al. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.01.022 · Cited by 114 · see citing works
Joyce, J. N., Smutzer, G., Whitty, C. J., et al. (1997) · Movement Disorders · doi:10.1002/mds.870120609 · Cited by 114 · see citing works
Marco, M. D., & Venneri, A. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-171018 · Cited by 103 · see citing works
D’Amelio, M., Puglisi‐Allegra, S., & Mercuri, N. B. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.01.016 · Cited by 95 · see citing works
Altered brain metabolic connectivity at multiscale level in early Parkinson’s disease
Sala, A., Caminiti, S. P., Presotto, L., Premi, E., Pilotto, A., Turrone, R., Cosseddu, M., Alberici, A., Paghera, B., Borroni, B., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-04102-z · Cited by 93 · see citing works
Self-citationPerani, D., Cerami, C., Caminiti, S. P., Santangelo, R., Coppi, E., Ferrari, L. D., Pinto, P., Passerini, G., Falini, A., Iannaccone, S., et al. (2015) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-015-3170-y · Cited by 91 · see citing works
Self-citationIn vivo mapping of brainstem nuclei functional connectivity disruption in Alzheimer’s disease
Serra, L., D'Amelio, M., Di Domenico, C., Dipasquale, O., Marra, C., Mercuri, N. B., Caltagirone, C., Cercignani, M., & Bozzali, M. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.08.012 · Cited by 91 · see citing works
Dopaminergic correlates of metabolic network activity in Parkinson's disease
Holtbernd, F., Ma, Y., Peng, S., et al. (2015) · Human Brain Mapping · doi:10.1002/hbm.22863 · Cited by 89 · see citing works
Brain glucose metabolism in Lewy body dementia: implications for diagnostic criteria
Caminiti, S. P., Sala, A., Iaccarino, L., Beretta, L., Pilotto, A., Gianolli, L., Iannaccone, S., Magnani, G., Padovani, A., Ferini-Strambi, L., et al. (2019) · Alzheimer's Research & Therapy · doi:10.1186/s13195-019-0473-4 · Cited by 86 · see citing works
Self-citationSala, A., & Perani, D. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00617 · Cited by 85 · see citing works
Self-citationDopamine and reward: a view from the prefrontal cortex
Chau, B. K. H., Jarvis, H., Law, C.-K., & Chong, T. T. ‐. (2018) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000424 · Cited by 84 · see citing works
VTA Projection Neurons Releasing GABA and Glutamate in the Dentate Gyrus
Ntamati, N. R., & Lüscher, C. (2016) · eNeuro · doi:10.1523/eneuro.0137-16.2016 · Cited by 78 · see citing works
Metabolic connectomics targeting brain pathology in dementia with Lewy bodies
Caminiti, S. P., Tettamanti, M., Sala, A., Presotto, L., Iannaccone, S., Cappa, S. F., Magnani, G., Perani, D., & Initiative, A. D. N. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16654497 · Cited by 77 · see citing works
Self-citationRossato, J. I., Radiske, A., Kohler, C. A., Gonzalez, C., Bevilaqua, L. R., Medina, J. H., & Cammarota, M. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.07.012 · Cited by 75 · see citing works
FDG-PET and amyloid-PET imaging
Perani, D. (2014) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000109 · Cited by 66 · see citing works
Self-citationBallarini, T., Iaccarino, L., Magnani, G., Ayakta, N., Miller, B. L., Jagust, W. J., Gorno‐Tempini, M., Rabinovici, G. D., & Perani, D. (2016) · Human Brain Mapping · doi:10.1002/hbm.23305 · Cited by 65 · see citing works
Self-citationLoss of Dopamine Uptake Sites Labeled with [ <sup>3</sup> H]GBR-12935 in Alzheimer’s Disease
Allard, P., Alafuzoff, I., Carlsson, A., Eriksson, K., Ericson, E., Gottfries, C.-G., & Marcusson, J. O. (2008) · European Neurology · doi:10.1159/000117341 · Cited by 64 · see citing works
Cerami, C., Dodich, A., Greco, L. C., Iannaccone, S., Magnani, G., Marcone, A., Pelagallo, E., Santangelo, R., Cappa, S. F., & Perani, D. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-160682 · Cited by 62 · see citing works
Self-citationSmiley, J. F., & Mesulam, M. M. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00202-4 · Cited by 60 · see citing works
Predicting long‐term clinical stability in amyloid‐positive subjects by FDG‐PET
Iaccarino, L., Sala, A., & Perani, D. (2019) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.782 · Cited by 56 · see citing works
Self-citationShape Abnormalities of the Striatum in Alzheimer's Disease
de Jong, L. W., Ferrarini, L., van der Grond, J., Milles, J., Reiber, J. H. C., Westendorp, R. G. J., Bollen, E. L. E. M., Middelkoop, H. A. M., & van Buchem, M. A. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-101026 · Cited by 55 · see citing works
Pagani, M., Giuliani, A., Öberg, J., et al. (2017) · Journal of Nuclear Medicine · doi:10.2967/jnumed.116.184309 · Cited by 52 · see citing works
The emerging role of PET imaging in dementia
Iaccarino, L., Sala, A., Caminiti, S. P., & Perani, D. (2017) · F1000Research · doi:10.12688/f1000research.11603.1 · Cited by 51 · see citing works
Self-citationCaminiti, S. P., Alongi, P., Majno, L., Volonté, M. A., Cerami, C., Gianolli, L., Comı, G., & Perani, D. (2017) · European Journal of Neurology · doi:10.1111/ene.13269 · Cited by 46 · see citing works
Self-citationValidation of 18F–FDG-PET Single-Subject Optimized SPM Procedure with Different PET Scanners
Presotto, L., Ballarini, T., Caminiti, S. P., Bettinardi, V., Gianolli, L., & Perani, D. (2017) · Neuroinformatics · doi:10.1007/s12021-016-9322-9 · Cited by 41 · see citing works
Self-citationAlzheimer disease neuropathology:understanding autonomic dysfunction
Engelhardt, E., & Laks, J. (2008) · Dementia & Neuropsychologia · doi:10.1590/s1980-57642009dn20300004 · Cited by 34 · see citing works
A biomarker study in long-lasting amnestic mild cognitive impairment
Cerami, C., Dodich, A., Iannaccone, S., Magnani, G., Santangelo, R., Presotto, L., Marcone, A., Gianolli, L., Cappa, S. F., & Perani, D. (2018) · Alzheimer s Research & Therapy · doi:10.1186/s13195-018-0369-8 · Cited by 34 · see citing works
Self-citationBrain dopamine D-1 receptors in senile dementia
Rinne, J. O., Säkö, E., Paljärvi, L., Mölsä, P. K., & Rinne, U. K. (1986) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(86)90132-2 · Cited by 29 · see citing works
Metabolic regional and network changes in Alzheimer's disease subtypes
Herholz, K., Haense, C., Gerhard, A., Jones, M. S., Anton‐Rodriguez, J., Segobin, S. H., Snowden, J. S., Thompson, J. C., & Kobylecki, C. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17718436 · Cited by 27 · see citing works
Zheng, L., Vinters, H. V., Mack, W. J., Weiner, M. W., Chui, H. C., & for the IVD program project (2015) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2015.152 · Cited by 26 · see citing works
From metabolic connectivity to molecular connectivity: application to dopaminergic pathways
Verger, A., Horowitz, T., Chawki, M. B., Eusébio, A., Bordonné, M., Azulay, J., Girard, N. J., & Guedj, É. (2019) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-019-04574-3 · Cited by 24 · see citing works
Gallivanone, F., Rosa, P. A. D., Perani, D., et al. (2017) · The Quarterly Journal of Nuclear Medicine and Molecular Imaging · doi:10.23736/s1824-4785.16.02749-7 · Cited by 22 · see citing works
Self-citationUnfavourable gender effect of high body mass index on brain metabolism and connectivity
Malpetti, M., Sala, A., Vanoli, E. G., Gianolli, L., Luzi, L., & Perani, D. (2018) · Scientific Reports · doi:10.1038/s41598-018-30883-y · Cited by 22 · see citing works
Self-citationThe 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
Flagged first, then by citations
Cited by
Sorted by citations
La Barbera, L., Vedele, F., Nobili, A., Krashia, P., Spoleti, E., Latagliata, E. C., Cutuli, D., Cauzzi, E., Marino, R., Viscomi, M. T., et al. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.102031 · Cited by 98 · see citing works
- Authors
- Iaccarino, L., Sala, A., Caminiti, S. P., Presotto, L., Perani, D., & Initiative, F. T. A. D. N.
- Affiliations
- Vita-Salute San Raffaele University (IT)
- IRCCS Ospedale San Raffaele (IT)
- Corresponding author
- Perani, Daniela
- Venue
- Journal of Alzheimer s Disease
- Publisher
- SAGE Publications
- Published
- 2020-05-04
- Volume
- 75
- Issue
- 3
- Pages
- 1003-1016
- ISSN
- 1387-2877 (ISSN-L)
- 1875-8908
- OpenAlex
- W3023784418
- Cited by
- 40
- References
- 99
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 7 · 2023: 5 · 2022: 8 · 2021: 8 · 2020: 3
- FWCI
- 4.37
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Alzheimer s Disease (publishedVersion)
- PubMed (publishedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion)
- Archivio Istituzionale della Ricerca - Università Vita-Salute San Raffaele (submittedVersion)
- ORBi (University of Liège) (submittedVersion)
- Funders
- National Institutes of Health (5u01ag024904-10)
- Canadian Institutes of Health Research
- National Institute on Aging (U01-AG-024904)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- Alzheimer's disease, dopaminergic pathways
- MeSH terms
- Aged, Alzheimer Disease, Brain, Dopamine, Female, Humans, Magnetic Resonance Imaging, Male, Neural Pathways, Retrospective Studies, Positron-Emission Tomography, Gray Matter
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
