Neural substrates underlying distinct dual cognitive syndromes in Parkinson's disease

IF 3.9 2区医学 Q1 CLINICAL NEUROLOGY European Journal of Neurology Pub Date : 2024-12-24 DOI:10.1111/ene.70022

Kenji Yoshimura, Atsushi Shima, Daisuke Kambe, Koji Furukawa, Akira Nishida, Ikko Wada, Yusuke Sakato, Haruhi Sakamaki-Tsukita, Yuta Terada, Hodaka Yamakado, Yosuke Taruno, Etsuro Nakanishi, Masanori Sawamura, Koji Fujimoto, Yasutaka Fushimi, Tomohisa Okada, Yuji Nakamoto, Takashi Hanakawa, Ryosuke Takahashi, Nobukatsu Sawamoto

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Abstract

Background

A dual-syndrome hypothesis, which states the cognitive impairments in Parkinson's disease (PD) are attributable to frontostriatal dopaminergic dysregulation and cortical disturbance—each associated with attention/executive and memory/visuospatial dysfunction, respectively—has been widely accepted. This multisystem contribution also underlies highly heterogeneous progression rate to dementia.

Methods

Nondemented PD patients who underwent [¹²³I]N-ω-fluoropropyl-2β-carbomethoxy-3β-(4-iodophenyl) nortropane ([¹²³I]FP-CIT) SPECT and neuropsychological examinations were enrolled. Patients who agreed to participate and age- and sex-matched healthy controls (HCs) also underwent 7-T MRI. Patients were classified as cognitively normal (PD-CN) or mild cognitive impairment (PD-MCI) following the level II criteria of Movement Disorder Society Guideline.

Results

A total of 155 patients (PD-CN/PD-MCI 74/81) were enrolled, whereas 76 patients (PD-CN/PD-MCI 35/41) and 56 HCs underwent 7 T-MRI. The caudate [¹²³I]FP-CIT uptake in PD was correlated with the performance of attention/working memory (trail-making test [TMT]-A and symbol digit modality test) and executive (TMT-B) domains. In contrast, the regional cortical thickness in the left frontotemporal and right frontal lobes in PD was correlated with performance of memory (Hopkins verbal learning test-revised delayed recall) and visuospatial (judgment of line orientation) domains. Moreover, compared to 37 HCs with a Montreal Cognitive Assessment score of >25, PD-CN patients showed broad occipitoparietal cortical thinning.

Conclusions

We demonstrated distinctive impairments of dopaminergic frontostriatal deficits and cortical degeneration as neural bases for the dual-syndrome hypothesis. Our findings suggest that occipitoparietal lobe thinning occurs at a cognitively normal stage, and additional frontotemporal lobe thinning underlies impairments in the memory and visuospatial domains at the PD-MCI stage.

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帕金森病中不同双重认知综合征的神经基质。

背景：双综合征假说认为帕金森病（PD）的认知障碍可归因于额纹状体多巴胺能失调和皮层紊乱，两者分别与注意/执行和记忆/视觉空间功能障碍相关，这一假说已被广泛接受。这种多系统贡献也导致了痴呆的高度异质性进展率。方法：选取经[123I]N-ω-氟丙基-2β-碳甲氧基-3β-（4-碘苯基）- nortropane ([123I]FP-CIT) SPECT和神经心理学检查的非痴呆性PD患者。同意参与的患者以及年龄和性别匹配的健康对照（hc）也接受了7-T MRI。患者按照运动障碍协会指南II级标准分为认知正常（PD-CN）或轻度认知障碍（PD-MCI）。结果：共入组155例患者（PD-CN/PD-MCI 74/81）， 76例患者（PD-CN/PD-MCI 35/41）和56例hcc患者接受了7次T-MRI检查。PD患者尾状核[123I]FP-CIT摄取与注意/工作记忆（TMT]-A和符号数字模态测试）和执行（TMT- b）域的表现相关。相比之下，PD患者的左额颞叶和右额叶区域皮质厚度与记忆（霍普金斯语言学习测试修订的延迟回忆）和视觉空间（线方向判断）域的表现相关。此外，与蒙特利尔认知评估评分为bbbb25的37名hc相比，PD-CN患者表现出广泛的枕顶皮质变薄。结论：我们证明了多巴胺能额纹状体缺陷和皮质退化是双重综合征假说的神经基础。我们的研究结果表明，枕顶叶变薄发生在认知正常阶段，而额外的额颞叶变薄是PD-MCI阶段记忆和视觉空间域受损的基础。

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来源期刊

European Journal of Neurology 医学-临床神经学

CiteScore

9.70

自引率

2.00%

发文量

418

审稿时长

1 months

期刊介绍： The European Journal of Neurology is the official journal of the European Academy of Neurology and covers all areas of clinical and basic research in neurology, including pre-clinical research of immediate translational value for new potential treatments. Emphasis is placed on major diseases of large clinical and socio-economic importance (dementia, stroke, epilepsy, headache, multiple sclerosis, movement disorders, and infectious diseases).