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Distinct spatiotemporal patterns of neuronal functional connectivity in primary progressive aphasia variants
Brain ( IF 14.5 ) Pub Date : 2017-08-31 , DOI: 10.1093/brain/awx217
Kamalini G Ranasinghe 1 , Leighton B Hinkley 2 , Alexander J Beagle 1 , Danielle Mizuiri 2 , Susanne M Honma 2 , Ariane E Welch 1 , Isabel Hubbard 1 , Maria Luisa Mandelli 1 , Zachary A Miller 1 , Coleman Garrett 2 , Alice La 1 , Adam L Boxer 1 , John F Houde 2, 3 , Bruce L Miller 1 , Keith A Vossel 1 , Maria Luisa Gorno-Tempini 1 , Srikantan S Nagarajan 2, 3
Affiliation  

Primary progressive aphasia is a syndrome characterized by progressive loss of language abilities with three main phenotypic clinical presentations, including logopenic, non-fluent/agrammatic, and semantic variants. Previous imaging studies have shown unique anatomic impacts within language networks in each variant. However, direct measures of spontaneous neuronal activity and functional integrity of these impacted neural networks in primary progressive aphasia are lacking. The aim of this study was to characterize the spatial and temporal patterns of resting state neuronal synchronizations in primary progressive aphasia syndromes. We hypothesized that resting state brain oscillations will show unique deficits within language network in each variant of primary progressive aphasia. We examined 39 patients with primary progressive aphasia including logopenic variant (n = 14, age = 61 ± 9 years), non-fluent/agrammatic variant (n = 12, age = 71 ± 8 years) and semantic variant (n = 13, age = 65 ± 7 years) using magnetoencephalographic imaging, compared to a control group that was matched in age and gender to each primary progressive aphasia subgroup (n = 20, age = 65 ± 5 years). Each patient underwent a complete clinical evaluation including a comprehensive battery of language tests. We examined the whole-brain resting state functional connectivity as measured by imaginary coherence in each patient group compared to the control cohort, in three frequency oscillation bands—delta-theta (2–8 Hz); alpha (8–12 Hz); beta (12–30 Hz). Each variant showed a distinct spatiotemporal pattern of altered functional connectivity compared to age-matched controls. Specifically, we found significant hyposynchrony of alpha and beta frequency within the left posterior temporal and occipital cortices in patients with the logopenic variant, within the left inferior frontal cortex in patients with the non-fluent/agrammatic variant, and within the left temporo-parietal junction in patients with the semantic variant. Patients with logopenic variant primary progressive aphasia also showed significant hypersynchrony of delta-theta frequency within bilateral medial frontal and posterior parietal cortices. Furthermore, region of interest-based analyses comparing the spatiotemporal patterns of variant-specific regions of interest identified in comparison to age-matched controls showed significant differences between primary progressive aphasia variants themselves. We also found distinct patterns of regional spectral power changes in each primary progressive aphasia variant, compared to age-matched controls. Our results demonstrate neurophysiological signatures of network-specific neuronal dysfunction in primary progressive aphasia variants. The unique spatiotemporal patterns of neuronal synchrony signify diverse neurophysiological disruptions and pathological underpinnings of the language network in each variant.

中文翻译:

原发性进行性失语症中神经元功能连接的不同时空模式

原发性进行性失语症是一种以语言能力逐渐丧失为特征的综合征,表现为三种主要的表型临床表现,包括低语,非流利/语法和语义变异。先前的影像学研究表明,每种变体在语言网络中具有独特的解剖学影响。但是,缺乏在原发进行性失语症中这些受影响的神经网络的自发神经元活动和功能完整性的直接测量方法。这项研究的目的是表征原发性进行性失语症患者的静止状态神经元同步的时空格局。我们假设在原发性失语症的每个变体中,静息状态的大脑振荡将在语言网络内显示出独特的缺陷。n = 14,年龄= 61±9岁),非流利/语法变体(n = 12,年龄= 71±8岁)和语义变体(n = 13,年龄= 65±7岁),通过脑磁图成像进行了比较对照组,该对照组的年龄和性别与每个主要进行性失语症亚组(n= 20岁,年龄= 65±5岁)。每位患者均接受了完整的临床评估,包括一系列全面的语言测试。我们检查了在三个频率振荡频带(δ-θ(2-8 Hz))中,与对照组相比,每个患者组中虚构相干性所测量的全脑静止状态功能连通性。阿尔法(8-12 Hz); β(12–30 Hz)。与年龄匹配的对照相比,每个变体均表现出功能连接改变的独特时空模式。具体而言,我们发现患有轻度变体的患者在左后颞叶和枕叶皮层,非流利/语法变体的患者的左下额叶皮层和左颞顶叶的阿尔法和β频率存在明显的不同步患者语义连接的变体。患有徽标变异的原发性进行性失语症的患者在双侧内侧额叶和顶叶后皮质中也表现出明显的δ-θ频率超同步性。此外,基于兴趣区域的分析比较了与年龄匹配的对照相比识别出的特定于变异的特定目标区域的时空模式,发现原发性进行性失语症变体本身之间存在显着差异。我们还发现,与年龄匹配的对照相比,每个主要进行性失语症变体中区域频谱功率变化的不同模式。我们的结果证明了在原发性进行性失语症变体中网络特定神经元功能障碍的神经生理学特征。
更新日期:2017-09-06
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