Neural signatures of predictive language processing in Parkinson's disease with and without mild cognitive impairment

Abstract

Cognitive deficits are common in Parkinson's disease (PD), with some PD patients meeting criteria for mild cognitive impairment (MCI). An unaddressed question is whether linguistic prediction is preserved in PD. This ability is nowadays deemed crucial in achieving fast and efficient comprehension, and it may be negatively impacted by cognitive deterioration. To fill this gap of knowledge, we used event-related potentials (ERPs) to evaluate mechanisms of linguistic prediction in a sample of PD patients (on dopamine compensation) with and without MCI. To this end, participants read sentence contexts that were predictive or not about a sentence-final word.The final word appeared after 1 second, matching or mismatching the prediction. The introduction of the interval allowed to capture neural responses both before and after sentence-final words, reflecting semantic anticipation and processing. PD patients with normal cognition (N = 58) showed ERP responses comparable to those of matched controls. Specifically, in predictive contexts, a slow negative potential developed prior to sentence-final words, reflecting semantic anticipation. Later, expected words elicited reduced N400 responses (compared to unexpected words), indicating facilitated semantic processing. Besides, PD patients with MCI (N = 20) showed a prolongation of the N400 congruency effect (compared to matched PD patients without MCI), indicating that further cognitive decline impacts semantic processing. Finally, lower verbal fluency scores correlated with prolonged N400 congruency effects and with reduced pre-word differences in all PD patients (N = 78). This relevantly points to a role of deficits in temporal-dependent mechanisms in PD, besides prototypical frontal dysfunction, in altered semantic anticipation and semantic processing during sentence comprehension.

Aberrant Changes in Cortical Complexity in Right-Onset Versus Left-Onset Parkinson’s Disease in Early-Stage

“…As a part of Wernicke’s region ( Binder, 2017 ), the left STG and bank of the STS participate in the composition of the left fronto-temporo-parietal network ( Kroczek et al, 2019 ), which is mainly related to language processing ( Geranmayeh et al, 2016 ; Griffis et al, 2017 ; Kroczek et al, 2019 ) and working memory ( Miró et al, 2020 ). PD-MCI is known to manifest language deficits ( León-Cabrera et al, 2021 ; Letanneux et al, 2021 ) and decreased working memory ( Caminiti et al, 2015 ), and in this part of patients were found that the network ( Bayram et al, 2019 ; Jin Yoon et al, 2021 ) was damaged.…”

Predictive language processing: integrating comprehension and production, and what atypical populations can tell us

“…PD is a neurodegenerative syndrome that initially affects motor control, leading to bradykinesia, rest tremor, and/or rigidity, but later progresses to also impact cognitive and emotional-affective domains ( Bloem et al, 2021 ). León-Cabrera et al (2021) studied prediction during reading in people with PD, both with normal cognition and with mild cognitive impairment, compared to matched controls. The authors recorded EEG and focused on two ERPs relevant for prediction: the prediction negative potentials (PNP) before final words and the N400 at the final word.…”

Predictive brain activity shows congruent semantic specificity in language comprehension and production.

“…Predictive activity precedes predictable stimuli, whereas prediction error signals can only emerge after the critical stimulus arrives. A range of recent noninvasive neurophysiological studies revealed separate and distinct brain indexes of prediction, the so-called PPs, which precede predictable (but not unpredictable) stimuli ( Peelen and Kastner, 2011 ; Kok et al, 2014 , 2016 ; Grisoni et al, 2016 , 2017 , 2021 ; Trapp et al, 2016 ; León-Cabrera et al, 2017 , 2019 , 2021 ) and even reflect predicted information at different levels, such as the acoustic–phonological makeup of spoken words ( Grisoni and Pulvermüller, 2022 ), semantic meaning ( Grisoni et al, 2021 ), and communicative function ( Boux et al, 2021 ). These prediction-related measures show regular relationships to established brain responses recently linked to prediction error, such as the mismatch negativity ( Näätänen et al, 2007 ; Bendixen et al, 2012 ; Grisoni et al, 2016 , 2019a ) and the N400 ( Kutas and Federmeier, 2011 ; Lau et al, 2013 ; Grisoni et al, 2017 , 2021 ).…”