Variable disruption of a syntactic processing network in primary progressive aphasia

Abstract

Syntactic processing deficits are highly variable in individuals with primary progressive aphasia. Damage to left inferior frontal cortex has been associated with syntactic deficits in primary progressive aphasia in a number of structural and functional neuroimaging studies. However, a contrasting picture of a broader syntactic network has emerged from neuropsychological studies in other aphasic cohorts, and functional imaging studies in healthy controls. To reconcile these findings, we used functional magnetic resonance imaging to investigate the functional neuroanatomy of syntactic comprehension in 51 individuals with primary progressive aphasia, composed of all clinical variants and a range of degrees of syntactic processing impairment. We used trial-by-trial reaction time as a proxy for syntactic processing load, to determine which regions were modulated by syntactic processing in each patient, and how the set of regions recruited was related to whether syntactic processing was ultimately successful or unsuccessful. Relationships between functional abnormalities and patterns of cortical atrophy were also investigated. We found that the individual degree of syntactic comprehension impairment was predicted by left frontal atrophy, but also by functional disruption of a broader syntactic processing network, comprising left posterior frontal cortex, left posterior temporal cortex, and the left intraparietal sulcus and adjacent regions. These regions were modulated by syntactic processing in healthy controls and in patients with primary progressive aphasia with relatively spared syntax, but they were modulated to a lesser extent or not at all in primary progressive aphasia patients whose syntax was relatively impaired. Our findings suggest that syntactic comprehension deficits in primary progressive aphasia reflect not only structural and functional changes in left frontal cortex, but also disruption of a wider syntactic processing network.

Localising memory retrieval and syntactic composition: an fMRI study of naturalistic language comprehension

“…Yet, along-side many of the findings just reviewed, our results stand in contrast to the apparent stability of compositional processes following anterior temporal atrophy (e.g. Wilson et al, 2014aWilson et al, , 2016. The present study does not resolve the tension between these two literatures.…”

Dissociation between Frontal and Temporal-Parietal Contributions to Connected Speech in Acute Stroke

“…Tyler et al, 2010;Rogalsky et al, 2018) raising the question of the role of anterior regions in syntactic processing (e.g. Thothathiri et al, 2012;Magnusdottir et al, 2013;Blank et al, 2016;Wilson et al, 2016;Fedorenko et al, 2018;Rogalsky et al, 2018). Matchin and Hickok (2019) propose that the inherently different processing requirements for language production and comprehension account for the differences in syntactic processing related neural substrates.…”

“…Here, we addressed the question of whether impairments producing the content and structure of spontaneously generated speech are related to different patterns of focal brain damage. Whether unique brain regions are required to produce content and structure during connected speech speaks to a central debate concerning the specificity of brain regions required for syntactic processing (e.g., Wilson and Saygın, 2004;Thothathiri et al, 2012;Magnusdottir et al, 2013;Blank et al, 2016;Wilson et al, 2016;Fedorenko et al, 2018;Rogalsky et al, 2018; cf. Dapretto and Bookheimer, 1999;Hagoort and Indefrey, 2014;Friederici et al, 2017).…”

Linguistic Aspects of Primary Progressive Aphasia

“…Another fMRI study showed greater left inferior frontal activation during grammatically complex sentences compared with simple sentences in controls, whereas patients with naPPA did not show a difference in left inferior frontal activation for these two types of sentences (Wilson et al 2010a). In a more recent study, recruitment of a broad, left hemisphere language network was particularly disrupted in patients with grammatical comprehension difficulty due to naPPA (Wilson et al 2016). Such findings suggest that the language impairment in naPPA is due in part to disruption of large-scale perisylvian neural networks that support language processing.…”