Differential language network functional connectivity alterations in Alzheimer's disease and the semantic variant of primary progressive aphasia

Montembeault, Maxime; Jarret, Julien; Boukadi, Mariem; Laforce, Robert; Wilson, Maximiliano A.; Rouleau, Isabelle; Brambati, Simona Maria

doi:10.1016/j.cortex.2019.03.018

Cited by 41 publications

(41 citation statements)

References 82 publications

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“…Our findings align with recent evidence from task-free fMRI studies reporting alterations in intrinsic functional connectivity networks in svPPA patients. Decreased connectivity in the ventral semantic network (as expected given the atrophy pattern) is accompanied by spared connectivity in the orthography-to-phonology conversion network and increased connectivity in the dorsal articulatory-phonological one (Battistella et al, 2019;Montembeault et al, 2019). Taken together, these results suggest that neurodegeneration leads to a dynamic reorganization of the interplay between ventral and dorsal pathways, where the downregulation of specific neurocognitive systems is associated with the upregulation of other ones.…”

Section: The Latency Of the Dorsal Activation Indicates Slow Serial supporting

confidence: 63%

Taking the sub-lexical route: brain dynamics of reading in the semantic variant of Primary Progressive Aphasia

Borghesani

Hinkley

Ranasinghe

et al. 2019

Preprint

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368 words Introduction: 1040 words Discussion: 2135 words Whole paper: 5769 words Tables: 4 Figures: 4 50-word Abbreviated Summary:Borghesani et al. investigate brain dynamics during irregular word reading using magnetoencephalographic imaging in patients with semantic variant of primary progressive aphasia. Due to anterior temporal lobe neurodegeneration, patients rely more on dorsal, occipitoparietal brain regions -providing novel evidence on the interplay between ventral and dorsal reading routes. AbstractReading aloud requires mapping an orthographic form to a phonological one. The mapping process relies on sub-lexical 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 sub-lexical and lexical 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 sub-lexical processes capitalizing the time resolution of magnetoencephalography and the unique clinical model offered by patients with semantic variant of Primary Progressive Aphasia (svPPA). Behaviorally, svPPA patients manifest marked lexico-semantic impairments including difficulties in reading words with exceptional orthographic to phonological correspondance (irregular words). Moreover, they present with focal neurodegeneration in the anterior temporal lobe (ATL), affecting primarily the ventral, occipitotemporal, 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 analyzed time-resolved whole-brain activity in 12 svPPA patients and 12 healthy age-matched controls while reading irregular words (e.g., yacht) and pseudowords (e.g., pook).Consistent with previous findings that the dorsal route is involved in sub-lexical 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 betaband (13-20 Hz), ramping up slowly over 500 ms after stimulus onset and peaking at ~800 ms, around response selection and production. This temporal pattern of neural activity was not observed in svPPA patients. 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 sub-lexical route is involved in processing both irregular and pseudo-words in svPPA.Together these results provide further evidence supporting a dual-route model for reading aloud -mediated by the interplay between lexical (ventral) and sub-lexical (dorsal) neuro-cognitive systems. When the lexical route is damaged, as in ...

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Section: The Latency Of the Dorsal Activation Indicates Slow Serial supporting

confidence: 63%

Taking the sub-lexical route: brain dynamics of reading in the semantic variant of Primary Progressive Aphasia

Borghesani

Hinkley

Ranasinghe

et al. 2019

Preprint

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“…The activation of the DMN in task-free functional studies is well established and has been associated with several cognitive processes (Greicius et al, 2003), including semantics (for meta-analysis, see Binder et al, 2009). The aMTG region used as a seed to build this network consistently is damaged in svPPA patients with profound semantic memory loss (Hodges et al, 1992), and recent studies have shown decreased functional connectivity of this region to the angular gyrus in this patient population (Battistella et al, 2019;Montembeault et al, 2019). Recent models of language suggest that the angular gyrus is involved in retrieval and/or executive semantic processes (Binder and Desai, 2011;Ralph et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Task-Free Functional Language Networks: Reproducibility and Clinical Application

et al. 2019

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Intrinsic connectivity networks (ICNs) identified through task-free fMRI (tf-fMRI) offer the opportunity to investigate human brain circuits involved in language processes without requiring participants to perform challenging cognitive tasks. In this study, we assessed the ability of tf-fMRI to isolate reproducible networks critical for specific language functions and often damaged in primary progressive aphasia (PPA). First, we performed whole-brain seed-based correlation analyses on tf-fMRI data to identify ICNs anchored in regions known for articulatory, phonological, and semantic processes in healthy male and female controls (HCs). We then evaluated the reproducibility of these ICNs in an independent cohort of HCs, and recapitulated their functional relevance with a post hoc meta-analysis on task-based fMRI. Last, we investigated whether atrophy in these ICNs could inform the differential diagnosis of nonfluent/agrammatic, semantic, and logopenic PPA variants. The identified ICNs included a dorsal articulatory-phonological network involving inferior frontal and supramarginal regions; a ventral semantic network involving anterior middle temporal and angular gyri; a speech perception network involving superior temporal and sensorimotor regions; and a network between posterior inferior temporal and intraparietal regions likely linking visual, phonological, and attentional processes for written language. These ICNs were highly reproducible across independent groups and revealed areas consistent with those emerging from task-based meta-analysis. By comparing ICNs' spatial distribution in HCs with patients' atrophy patterns, we identified ICNs associated with each PPA variant. Our findings demonstrate the potential use of tf-fMRI to investigate the functional status of language networks in patients for whom activation studies can be methodologically challenging.

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“…This result is, however, unsurprising, given the early stage of AD participants that were recruited in the current study. Indeed, Montembeault et al (2019) recruited AD participants with a slightly lower MMSE than AD participants in the current study (24.9±3.1 in their study vs. 25.5±2.6 in the current study). They showed that only one cluster (the right posterior temporal gyrus) was significantly less connected to the left posterior temporal gyrus in prodromal AD, while there was no difference with the control group when the LIFG was used a seed.…”

Section: Univariate Analysesmentioning

confidence: 79%

“…They also showed that connectivity changes were only marginally correlated with AD participants' language performance (i.e. no significant correlations in Mascali et al, 2018, no correlations with IFG's connectivity map in Montembeault et al, 2019). However, it is possible that some changes remain unnoticed when focusing exclusively on the language network.…”

Section: Introductionmentioning

confidence: 99%

“…Muller et al, 2016; Muller & Meyer, 2014). In AD, only few studies focused on this network, reporting lower functional connectivity in AD (Weiler et al, 2014, patients’ mean MMSE: 18.86; Mascali et al, 2018, patients’ mean MMSE: 20.5) and prodromal AD (Montembeault et al, 2019, patients’ mean MMSE: 24.9) compared to healthy controls. These studies used the left IFG (Mascali et al, 2018; Montembeault et al, 2019) or left posterior temporal gyrus (Mascali et al, 2018; Montembeault et al, 2019; Weiler et al, 2014) as a seed.…”

Section: Introductionmentioning

confidence: 99%

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Language network connectivity increases in prodromal Alzheimer’s disease

Pistono¹,

Senoussi

Guerrier

et al. 2020

Preprint

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Language production deficits occur early in the course of Alzheimer’s disease (AD); however, only few studies have focused on language functional networks in prodromal AD. The current study aims to uncover the extent of language alteration at a prodromal stage, on a behavioral, structural and functional level, using univariate and multivariate analyses. Twenty-four AD participants and 24 matched healthy controls underwent a comprehensive language evaluation, a structural T1-3D MRI and resting-state fMRI. We performed seed-based analyses, using the left inferior frontal gyrus and left posterior temporal gyrus as seeds. Then, we analyzed connectivity between executive control networks and language network in each group. Finally, we used multivariate pattern analyses to test whether the two groups could be distinguished based on the pattern of atrophy within the language network; atrophy within the executive control networks, as well as the pattern of functional connectivity within the language network; and functional connectivity within executive control networks. AD participants had language impairment during standardized language tasks and connected-speech production. Univariate analyses were not able to discriminate participants at this stage, while multivariate pattern analyses could significantly predict the group membership of prodromal patients and healthy controls, both when classifying atrophy patterns or connectivity patterns of the language network. Language functional networks could discriminate AD participants better than executive control networks. Most notably, they revealed an increased connectivity at a prodromal stage. Multivariate analyses represent a useful tool for investigating the functional and structural (re-)organization of the neural bases of language.HighlightsLanguage network connectivity discriminates prodromal AD from healthy controlsLanguage network connectivity increases in prodromal ADAtrophy patterns in the language network do not correlate with connectivity patterns in AD

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Differential language network functional connectivity alterations in Alzheimer's disease and the semantic variant of primary progressive aphasia

Cited by 41 publications

References 82 publications

Taking the sub-lexical route: brain dynamics of reading in the semantic variant of Primary Progressive Aphasia

Taking the sub-lexical route: brain dynamics of reading in the semantic variant of Primary Progressive Aphasia

Task-Free Functional Language Networks: Reproducibility and Clinical Application

Language network connectivity increases in prodromal Alzheimer’s disease

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