Parkinson's disease (PD) affects the language processes, with a significant impact on the patients' daily communication. We aimed to describe specific alterations in the comprehension of syntactically complex sentences in patients with PD (PwPD) as compared to healthy controls (HC) and to identify the neural underpinnings of these deficits using a functional connectivity analysis of the striatum. A total of 20 patients PwPD and 15 HC participated in the fMRI study. We analyzed their performance of a Test of sentence comprehension (ToSC) adjusted for fMRI. A task-dependent functional connectivity analysis of the striatum was conducted using the psychophysiological interaction method (PPI). On the behavioral level, the PwPD scored significantly lower (mean ± sd: 77.3 ± 12.6) in the total ToSC score than the HC did (mean ± sd: 86.6 ± 8.0), p = 0.02, and the difference was also significant specifically for sentences with a non-canonical word order (PD-mean ± sd: 69.9 ± 14.1, HC-mean ± sd: 80.2 ± 11.5, p = 0.04). Using PPI, we found a statistically significant difference between the PwPD and the HC in connectivity from the right striatum to the supplementary motor area [SMA, (4 8 53)] for non-canonical sentences. This PPI connectivity was negatively correlated with the ToSC accuracy of non-canonical sentences in the PwPD. Our results showed disturbed sentence reading comprehension in the PwPD with altered task-dependent functional connectivity from the right striatum to the SMA, which supports the synchronization of the temporal and sequential aspects of language processing. The study revealed that subcortical-cortical networks (striatal-frontal loop) in PwPD are compromised, leading to impaired comprehension of syntactically complex sentences.

2nd Department of Neurology Faculty of Medicine Comenius University Bratislava Slovakia

Brain and Mind Research Central European Institute of Technology Masaryk University Brno Czechia

Department of Communication Disorders Faculty of Education Comenius University Bratislava Slovakia

Zobrazit více v PubMed

Aarsland D., Batzu L., Halliday G. M., Geurtsen G. J., Ballard C., Ray Chaudhuri K., et al. (2021). Parkinson disease-associated cognitive impairment. PubMed DOI

Abrevaya S., Sedeño L., Fitipaldi S., Pineda D., Lopera F., Buritica O., et al. (2016). The road less traveled: Alternative pathways for action-verb processing in Parkinson’s disease. PubMed DOI

Angwin A. J., Chenery H. J., Copland D. A., Murdoch B. E., Silburn P. A. (2007). The speed of lexical activation is altered in Parkinson’s disease. PubMed DOI

Angwin A. J., Chenery H. J., Copland D. A., Murdoch B. E., Silburn P. A. (2005). Summation of semantic priming and complex sentence comprehension in Parkinson’s disease. PubMed DOI

Ash S., Xie S. X., Gross R. G., Dreyfuss M., Boller A., Camp E., et al. (2012). The organization and anatomy of narrative comprehension and expression in Lewy body spectrum disorders. PubMed DOI PMC

Brabenec L., Klobusiakova P., Barton M., Mekyska J., Galaz Z., Zvoncak V., et al. (2019). Non-invasive stimulation of the auditory feedback area for improved articulation in Parkinson’s disease. PubMed DOI

Brabenec L., Klobusiakova P., Simko P., Kostalova M., Mekyska J., Rektorova I. (2021). Non-invasive brain stimulation for speech in Parkinson’s disease: A randomized controlled trial. PubMed DOI

Colman K. S. F., Koerts J., Stowe L. A., Leenders K. L., Bastiaanse R. (2011). Sentence comprehension and its association with executive functions in patients with Parkinson’s disease. PubMed DOI PMC

Cramer S. C., Sur M., Dobkin B. H., O’Brien C., Sanger T. D., Trojanowski J. Q., et al. (2011). Harnessing neuroplasticity for clinical applications. PubMed DOI PMC

Dickerson B. C., Salat D. H., Greve D. N., Chua E. F., Rand-Giovannetti E., Rentz D. M., et al. (2005). Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. PubMed DOI PMC

Gajdoš M., Mikl M., Mareèek R. (2016). Mask_explorer: A tool for exploring brain masks in fMRI group analysis. PubMed DOI

Gross R. G., Camp E., McMillan C. T., Dreyfuss M., Gunawardena D., Cook P. A., et al. (2013). Impairment of script comprehension in Lewy body spectrum disorders. PubMed DOI PMC

Gross R. G., McMillan C. T., Chandrasekaran K., Dreyfuss M., Ash S., Avants B., et al. (2012). Sentence processing in Lewy body spectrum disorder: The role of working memory. PubMed DOI PMC

Grossman M., Cooke A., DeVita C., Lee C., Alsop D., Detre J., et al. (2003). Grammatical and resource components of sentence processing in Parkinson’s disease: An fMRI study. PubMed DOI

Grossman M., Glosser G., Kalmanson J., Morris J., Stern M. B., Hurtig H. I. (2001). Dopamine supports sentence comprehension in Parkinson’s disease. PubMed DOI

Grossman M., Gross R. G., Moore P., Dreyfuss M., McMillan C. T., Cook P. A., et al. (2012). Difficulty processing temporary syntactic ambiguities in Lewy body spectrum disorder. PubMed DOI PMC

Grossman M., Irwin D. J., Jester C., Halpin A., Ash S., Rascovsky K., et al. (2017). Narrative organization deficit in lewy body disorders is related to Alzheimer pathology. PubMed DOI PMC

Grossman M., Kalmanson J., Bernhardt N., Morris J., Stern M. B., Hurtig H. I. (2000). Cognitive resource limitations during sentence comprehension in Parkinson’s disease. PubMed DOI

Grossman M., Lee C., Morris J., Stern M. B., Hurtig H. I. (2002). Assessing resource demands during sentence processing in Parkinson’s disease. PubMed DOI

Hochstadt J. (2009). Set-shifting and the on-line processing of relative clauses in Parkinson’s disease: Results from a novel eye-tracking method. PubMed DOI

Hochstadt J., Nakano H., Lieberman P., Friedman J. (2006). The roles of sequencing and verbal working memory in sentence comprehension deficits in Parkinson’s disease. PubMed DOI

Hope T. R., Selnes P., Rektorová I., Anderkova L., Nemcova-Elfmarkova N., Balážová Z., et al. (2019). Diffusion tensor and restriction spectrum imaging reflect different aspects of neurodegeneration in Parkinson’s disease. PubMed DOI PMC

Johari K., Walenski M., Reifegerste J., Ashrafi F., Behroozmand R., Daemi M., et al. (2019). A dissociation between syntactic and lexical processing in Parkinson’s disease. PubMed DOI PMC

Klobusiakova P., Mekyska J., Brabenec L., Galaz Z., Zvoncak V., Mucha J., et al. (2021). Articulatory network reorganization in Parkinson’s disease as assessed by multimodal MRI and acoustic measures. PubMed DOI

Kojovic M., Kassavetis P., Bologna M., Pareés I., Rubio-Agusti I., Beraredelli A., et al. (2015). Transcranial magnetic stimulation follow-up study in early Parkinson’s disease: A decline in compensation with disease progression?: DECLINE in compensatory changes with PD progression. PubMed DOI

Kotz S. A., Schwartze M., Schmidt-Kassow M. (2009). Non-motor basal ganglia functions: A review and proposal for a model of sensory predictability in auditory language perception. PubMed DOI

Lee C., Grossman M., Morris J., Stern M. B., Hurtig H. I. (2003). Attentional resource and processing speed limitations during sentence processing in Parkinson’s disease. PubMed DOI

Lowit A., Thies T., Steffen J., Scheele F., Roheger M., Kalbe E., et al. (2022). Task-based profiles of language impairment and their relationship to cognitive dysfunction in Parkinson’s disease. PubMed DOI PMC

Lucza T., Karádi K., Kállai J., Weintraut R., Janszky J., Makkos A., et al. (2015). Screening mild and major neurocognitive disorders in Parkinson’s disease. PubMed DOI PMC

Marková J., Hajdúk M., Košutzká Z., Kušnírová A., Pápayová M., Egryová M., et al. (2018). Sentence comprehension in Slovak-speaking patients with Parkinson disease. DOI

Marková J., Horváthová Ĺ, Králová M., Cséfalvay Z. (2017). Sentence comprehension in Slovak-speaking patients with Alzheimer’s disease: Sentence comprehension in Alzheimer’s disease. PubMed DOI

McGregor M. M., Nelson A. B. (2019). Circuit mechanisms of Parkinson’s disease. PubMed DOI

Mesulam M.-M. (1999). Neuroplasticity failure in Alzheimer’s disease. PubMed DOI

Novakova L., Gajdos M., Rektorova I. (2020). Theta-burst transcranial magnetic stimulation induced cognitive task-related decrease in activity of default mode network: An exploratory study. PubMed DOI

O’Reilly J. X., Woolrich M. W., Behrens T. E. J., Smith S. M., Johansen-Berg H. (2012). Tools of the trade: Psychophysiological interactions and functional connectivity. PubMed DOI PMC

Péran P., Cardebat D., Cherubini A., Piras F., Luccichenti G., Peppe A., et al. (2009). Object naming and action-verb generation in Parkinson’s disease: A fMRI study. PubMed DOI

Poser B. A., Versluis M. J., Hoogduin J. M., Norris D. G. (2006). BOLD contrast sensitivity enhancement and artifact reduction with multiecho EPI: Parallel-acquired inhomogeneity-desensitized fMRI. PubMed DOI

Postuma R. B., Berg D., Stern M., Poewe W., Olanow C. W., Oertel W., et al. (2015). MDS clinical diagnostic criteria for Parkinson’s disease: MDS-PD Clinical Diagnostic Criteria. PubMed DOI

Sejnoha Minsterova A., Klobusiakova P., Pies A., Galaz Z., Mekyska J., Novakova L., et al. (2020). Patterns of diffusion kurtosis changes in Parkinson’s disease subtypes. PubMed DOI

Skeel R. L., Crosson B., Nadeau S. E., Algina J., Bauer R. M., Fennell E. B. (2001). Basal ganglia dysfunction, working memory, and sentence comprehension in patients with Parkinson’s disease. PubMed DOI

Smith K. M., Caplan D. N. (2018). Communication impairment in Parkinson’s disease: Impact of motor and cognitive symptoms on speech and language. PubMed DOI

Troche M. S., Altmann L. J. P. (2012). Sentence production in Parkinson disease: Effects of conceptual and task complexity. DOI

Tziortzi A. C., Searle G. E., Tzimopoulou S., Salinas C., Beaver J. D., Jenkinson M., et al. (2011). Imaging dopamine receptors in humans with [11C]-(+)-PHNO: Dissection of D3 signal and anatomy. PubMed DOI

Walenski M., Europa E., Caplan D., Thompson C. K. (2019). Neural networks for sentence comprehension and production: An ALE-based meta-analysis of neuroimaging studies. PubMed DOI PMC

Ye Z., Milenkova M., Mohammadi B., Kollewe K., Schrader C., Dengler R., et al. (2012). Impaired comprehension of temporal connectives in Parkinson’s disease—A neuroimaging study. PubMed DOI

Sentence comprehension in Lewy body diseases: a functional magnetic resonance imaging study

Language dysfunction as a primary feature of cognitive decline in neurological populations