Dopaminergic and Metabolic Correlations With Cognitive Domains in Non-demented Parkinson’s Disease

Linlin Han1, Jiaying Lu2, Yilin Tang1, Yun Fan1, Qi-Si Chen1, Ling Li2, Fengtao Liu1, Jian Wang1, Chuantao Zuo2, Jue Zhao1
1Department of Neurology and National Clinical Research Center for Aging and Medicine, Huashan Hospital, Fudan University, Shanghai, China
2PET Center, Huashan Hospital, Fudan University, Shanghai, China

Tóm tắt

Background

Accruing positron emission tomography (PET) studies have suggested that dopaminergic functioning and metabolic changes are correlated with cognitive dysfunction in Parkinson’s disease (PD). Yet, the relationship between dopaminergic or cerebral metabolism and different cognitive domains in PD is poorly understood. To address this scarcity, we aimed to investigate the interactions among dopaminergic bindings, metabolic network changes, and the cognitive domains in PD patients.

Methods

We recruited 41 PD patients, including PD patients with no cognitive impairment (PD-NC; n = 21) and those with mild cognitive impairment (PD-MCI; n = 20). All patients underwent clinical evaluations and a schedule of neuropsychological tests and underwent both 11C-N-2-carbomethoxy-3-(4-fluorophenyl)-tropane (11C-CFT) and 18F-fluorodeoxyglucose (18F-FDG) PET imaging.

Results

11C-CFT imaging revealed a significant positive correlation between executive function and striatal dopamine transporter (DAT) binding at both the voxel and regional levels. Metabolic imaging revealed that executive function correlated with 18F-FDG uptake, mainly in inferior frontal gyrus, putamen, and insula. Further analysis indicated that striatal DAT binding correlated strictly with metabolic activity in the temporal gyrus, medial frontal gyrus, and cingulate gyrus.

Conclusion

Our findings might promote the understanding of the neurobiological mechanisms underlying cognitive impairment in PD.

Từ khóa


Tài liệu tham khảo

Arsalidou, 2013, The centre of the brain: topographical model of motor, cognitive, affective, and somatosensory functions of the basal ganglia., Hum. Brain Mapp., 34, 3031, 10.1002/hbm.22124

Bohnen, 2015, Frequency of cholinergic and caudate nucleus dopaminergic deficits across the predemented cognitive spectrum of Parkinson disease and evidence of interaction effects., JAMA Neurol., 72, 194, 10.1001/jamaneurol.2014.2757

Bu, 2018, Patterns of dopamine transporter imaging in subtypes of multiple system atrophy., Acta Neurol. Scand., 138, 170, 10.1111/ane.12932

Caffarra, 2002, Rey-Osterrieth complex figure: normative values in an Italian population sample., Neurol. Sci., 22, 443, 10.1007/s100720200003

Christopher, 2014, Combined insular and striatal dopamine dysfunction are associated with executive deficits in Parkinson’s disease with mild cognitive impairment., Brain, 137, 565, 10.1093/brain/awt337

Chung, 2018, Effect of striatal dopamine depletion on cognition in de novo Parkinson’s disease., Parkinsonism Relat. Disord., 51, 43, 10.1016/j.parkreldis.2018.02.048

Emre, 2007, Clinical diagnostic criteria for dementia associated with Parkinson’s disease., Mov. Disord., 22, 1689, 10.1002/mds.21507

Foltynie, 2004, The cognitive ability of an incident cohort of Parkinson’s patients in the UK. The CamPaIGN study., Brain, 127, 550, 10.1093/brain/awh067

Grahn, 2008, The cognitive functions of the caudate nucleus., Prog. Neurobiol., 86, 141, 10.1016/j.pneurobio.2008.09.004

Gratwicke, 2015, Parkinson’s disease dementia: a neural networks perspective., Brain, 138, 1454, 10.1093/brain/awv104

Gratwicke, 2013, The nucleus basalis of Meynert: a new target for deep brain stimulation in dementia., Neurosci. Biobehav. Rev., 37, 2676, 10.1016/j.neubiorev.2013.09.003

Guo, 2009, A comparison study of mild cognitive impairment with 3 memory tests among Chinese individuals., Alzheimer Dis. Assoc. Disord., 23, 253, 10.1097/WAD.0b013e3181999e92

Halliday, 2014, The neurobiological basis of cognitive impairment in Parkinson’s disease., Mov. Disord., 29, 634, 10.1002/mds.25857

Hely, 2008, The Sydney multicenter study of Parkinson’s disease: the inevitability of dementia at 20 years., Mov. Disord., 23, 837, 10.1002/mds.21956

Huang, 2020, Correlations between dopaminergic dysfunction and abnormal metabolic network activity in REM sleep behavior disorder., J. Cereb. Blood Flow Metab., 40, 552, 10.1177/0271678X19828916

Hughes, 1992, Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases., J. Neurol. Neurosurg. Psychiatry, 55, 181, 10.1136/jnnp.55.3.181

Katzman, 1988, A Chinese version of the mini-mental state examination; impact of illiteracy in a Shanghai dementia survey., J. Clin. Epidemiol., 41, 971, 10.1016/0895-4356(88)90034-0

Kehagia, 2010, Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson’s disease., Lancet Neurol., 9, 1200, 10.1016/S1474-4422(10)70212-X

Kim, 2019, Association of striatal dopaminergic neuronal integrity with cognitive dysfunction and cerebral cortical metabolism in Parkinson’s disease with mild cognitive impairment., Nucl. Med. Commun., 40, 1216, 10.1097/MNM.0000000000001098

Krimmel, 2019, Resting state functional connectivity and cognitive task-related activation of the human claustrum., Neuroimage, 196, 59, 10.1016/j.neuroimage.2019.03.075

Litvan, 2012, Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: movement disorder society task force guidelines., Mov. Disord., 27, 349, 10.1002/mds.24893

Liu, 2018, Clinical, dopaminergic, and metabolic correlations in Parkinson disease: a dual-tracer PET study., Clin. Nucl. Med., 43, 562, 10.1097/RLU.0000000000002148

Liu, 2019, Ginsenoside Rb1 regulates prefrontal cortical GABAergic transmission in MPTP-treated mice., Aging, 11, 5008, 10.18632/aging.102095

Lucas, 2005, Mayo’s older African Americans normative studies: norms for Boston naming test, controlled oral word association, category fluency, animal naming, token test, WRAT-3 reading, trail making test, stroop test, and judgment of line orientation., Clin. Neuropsychol., 19, 243, 10.1080/13854040590945337

Ma, 2010, Dopamine cell implantation in Parkinson’s disease: long-term clinical and (18)F-FDOPA PET outcomes., J. Nucl. Med., 51, 7, 10.2967/jnumed.109.066811

Menon, 2010, Saliency, switching, attention and control: a network model of insula function., Brain Struct. Funct., 214, 655, 10.1007/s00429-010-0262-0

Niethammer, 2013, Parkinson’s disease cognitive network correlates with caudate dopamine., Neuroimage, 78, 204, 10.1016/j.neuroimage.2013.03.070

Nobili, 2010, Cognitive-nigrostriatal relationships in de novo, drug-naïve Parkinson’s disease patients: a [I-123]FP-CIT SPECT study., Mov. Disord., 25, 35, 10.1002/mds.22899

Ouchi, 2001, Changes in dopamine availability in the nigrostriatal and mesocortical dopaminergic systems by gait in Parkinson’s disease., Brain, 784, 10.1093/brain/124.4.784

Owen, 2004, Cognitive dysfunction in Parkinson’s disease: the role of frontostriatal circuitry., Neuroscientist, 10, 525, 10.1177/1073858404266776

Papagno, 2018, Cognitive and behavioral disorders in Parkinson’s disease: an update. I: cognitive impairments., Neurol. Sci., 39, 215, 10.1007/s10072-017-3154-8

Pellecchia, 2015, Cognitive performances and DAT imaging in early Parkinson’s disease with mild cognitive impairment: a preliminary study., Acta Neurol. Scand., 131, 275, 10.1111/ane.12365

Polito, 2012, Interaction of caudate dopamine depletion and brain metabolic changes with cognitive dysfunction in early Parkinson’s disease., Neurobiol. Aging, 33, 10.1016/j.neurobiolaging.2010.09.004

Redgrave, 2010, Goal-directed and habitual control in the basal ganglia: implications for Parkinson’s disease., Nat. Rev. Neurosci., 11, 760, 10.1038/nrn2915

Ricci, 2016, The clock drawing test as a screening tool in mild cognitive impairment and very mild dementia: a new brief method of scoring and normative data in the elderly., Neurol. Sci., 37, 867, 10.1007/s10072-016-2480-6

Rinne, 2000, Cognitive impairment and the brain dopaminergic system in Parkinson disease: [18F]fluorodopa positron emission tomographic study., Arch. Neurol., 57, 470, 10.1001/archneur.57.4.470

Schade, 2020, Levodopa equivalent dose conversion factors: an updated proposal including opicapone and safinamide., Mov. Disord. Clin. Pract., 7, 343, 10.1002/mdc3.12921

Sheridan, 2006, Normative symbol digit modalities test performance in a community-based sample., Arch. Clin. Neuropsychol., 21, 23, 10.1016/j.acn.2005.07.003

Siepel, 2014, Cognitive executive impairment and dopaminergic deficits in de novo Parkinson’s disease., Mov. Disord., 29, 1802, 10.1002/mds.26051

Steinberg, 2005, Mayo’s older americans normative studies: age- and IQ-adjusted norms for the trail-making test, the stroop test, and MAE controlled oral word association test., Clin. Neuropsychol., 19, 329, 10.1080/13854040590945210

Tang, 2016, Cerebral metabolic differences associated with cognitive impairment in Parkinson’s disease., PLoS One, 11, 10.1371/journal.pone.0152716

White, 2018, Frontal cortical control of posterior sensory and association cortices through the claustrum., Brain Struct. Funct., 223, 2999, 10.1007/s00429-018-1661-x

Wu, 2018, Clinical characteristics of cognitive impairment in patients with Parkinson’s disease and its related pattern in 18 F-FDG PET imaging., Hum. Brain Mapp., 39, 4652, 10.1002/hbm.24311

Yesavage, 1982, Development and validation of a geriatric depression screening scale: a preliminary report., J. Psychiatr. Res., 17, 37, 10.1016/0022-3956(82)90033-4

Zhao, 2013, The shape trail test: application of a new variant of the trail making test., PLoS One, 8, 10.1371/journal.pone.0057333