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Taking the sublexical route: brain dynamics of reading in the semantic variant of primary progressive aphasia.
Brain ( IF 10.6 ) Pub Date : 2020-08-13 , DOI: 10.1093/brain/awaa212
Valentina Borghesani 1 , Leighton B N Hinkley 2 , Kamalini G Ranasinghe 1 , Megan M C Thompson 2, 3 , Wendy Shwe 1 , Danielle Mizuiri 2 , Michael Lauricella 1 , Eduardo Europa 1 , Susanna Honma 2 , Zachary Miller 1 , Bruce Miller 1 , Keith Vossel 4 , Maya M L Henry 5 , John F Houde 6 , Maria L Gorno-Tempini 1, 7 , Srikantan S Nagarajan 2, 6
Affiliation  

Reading aloud requires mapping an orthographic form to a phonological one. The mapping process relies on sublexical statistical regularities (e.g. ‘oo’ to |uː|) or on learned lexical associations between a specific visual form and a series of sounds (e.g. yacht to/jɑt/). Computational, neuroimaging, and neuropsychological evidence suggest that sublexical, phonological and lexico-semantic processes rely on partially distinct neural substrates: a dorsal (occipito-parietal) and a ventral (occipito-temporal) route, respectively. Here, we investigated the spatiotemporal features of orthography-to-phonology mapping, capitalizing on the time resolution of magnetoencephalography and the unique clinical model offered by patients with semantic variant of primary progressive aphasia (svPPA). Behaviourally, patients with svPPA manifest marked lexico-semantic impairments including difficulties in reading words with exceptional orthographic to phonological correspondence (irregular words). Moreover, they present with focal neurodegeneration in the anterior temporal lobe, affecting primarily the ventral, occipito-temporal, lexical route. Therefore, this clinical population allows for testing of specific hypotheses on the neural implementation of the dual-route model for reading, such as whether damage to one route can be compensated by over-reliance on the other. To this end, we reconstructed and analysed time-resolved whole-brain activity in 12 svPPA patients and 12 healthy age-matched control subjects while reading irregular words (e.g. yacht) and pseudowords (e.g. pook). Consistent with previous findings that the dorsal route is involved in sublexical, phonological processes, in control participants we observed enhanced neural activity over dorsal occipito-parietal cortices for pseudowords, when compared to irregular words. This activation was manifested in the beta-band (12–30 Hz), ramping up slowly over 500 ms after stimulus onset and peaking at ∼800 ms, around response selection and production. Consistent with our prediction, svPPA patients did not exhibit this temporal pattern of neural activity observed in controls this contrast. Furthermore, a direct comparison of neural activity between patients and controls revealed a dorsal spatiotemporal cluster during irregular word reading. These findings suggest that the sublexical/phonological route is involved in processing both irregular and pseudowords in svPPA. Together these results provide further evidence supporting a dual-route model for reading aloud mediated by the interplay between lexico-semantic and sublexical/phonological neurocognitive systems. When the ventral route is damaged, as in the case of neurodegeneration affecting the anterior temporal lobe, partial compensation appears to be possible by over-recruitment of the slower, serial attention-dependent, dorsal one.

中文翻译:


采取词汇下途径:原发性进行性失语症语义变异中阅读的大脑动力学。



朗读需要将拼写形式映射到语音形式。映射过程依赖于词汇下的统计规律(例如“oo”到|uː|)或特定视觉形式和一系列声音之间习得的词汇关联(例如“游艇”到/jɑt/)。计算、神经影像学和神经心理学证据表明,词汇下、语音和词汇语义过程依赖于部分不同的神经基质:分别是背侧(枕顶)和腹侧(枕颞)路径。在这里,我们利用脑磁图的时间分辨率和原发性进行性失语症(svPPA)语义变异患者提供的独特临床模型,研究了拼字法到音系映射的时空特征。在行为上,svPPA 患者表现出明显的词汇语义障碍,包括阅读具有特殊的拼写与语音对应关系的单词(不规则单词)的困难。此外,它们表现为前颞叶局灶性神经变性,主要影响腹侧、枕颞叶和词汇路径。因此,这个临床群体允许测试双路径阅读模型的神经实现的特定假设,例如对一条路径的损害是否可以通过过度依赖另一条路径来补偿。为此,我们重建并分析了 12 名 svPPA 患者和 12 名年龄匹配的健康对照受试者在阅读不规则单词(例如游艇)和伪单词(例如pook )时的时间分辨全脑活动。 与之前的发现一致,即背侧路线涉及词汇下、语音过程,在对照参与者中,我们观察到与不规则单词相比,伪单词背侧枕顶皮质的神经活动增强。这种激活表现在 β 频带(12-30 Hz)中,在刺激开始后 500 毫秒内缓慢上升,并在响应选择和产生周围的约 800 毫秒处达到峰值。与我们的预测一致,svPPA 患者没有表现出在对照组中观察到的这种神经活动的时间模式。此外,对患者和对照组之间神经活动的直接比较显示,在不规则的单词阅读过程中存在背侧时空簇。这些发现表明,词汇下/语音路径参与了 svPPA 中不规则词和伪词的处理。这些结果共同提供了进一步的证据,支持由词汇语义和词汇下/语音神经认知系统之间的相互作用介导的双路径朗读模型。当腹侧通路受损时,例如影响前颞叶的神经变性,通过过度招募较慢的、连续注意力依赖的背侧通路似乎可以实现部分补偿。
更新日期:2020-08-26
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