Language impairment in Parkinson's disease: fMRI study of sentence reading comprehension
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
36967818
PubMed Central
PMC10033839
DOI
10.3389/fnagi.2023.1117473
Knihovny.cz E-zdroje
- Klíčová slova
- Parkinson’s disease, functional connectivity, language impairment, sentence reading comprehension, striatum, task fMRI,
- Publikační typ
- časopisecké články MeSH
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. Nat. Rev. Dis. Primer 7:47. 10.1038/s41572-021-00280-3 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. J. Alzheimers Dis. 55 1429–1435. 10.3233/JAD-160737 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. J. Clin. Exp. Neuropsychol. 29 73–85. 10.1080/13803390500507188 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. Cogn. Brain Res. 25 78–89. 10.1016/j.cogbrainres.2005.04.008 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. Neuropsychology 26 368–384. 10.1037/a0027115 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. Parkinsonism Relat. Disord. 61 187–192. 10.1016/j.parkreldis.2018.10.011 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. Brain Stimulat. 14 571–578. 10.1016/j.brs.2021.03.010 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. Parkinsons Dis. 2011 1–15. 10.4061/2011/213983 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. Brain 134 1591–1609. 10.1093/brain/awr039 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. Neurology 65 404–411. 10.1212/01.wnl.0000171450.97464.49 PubMed DOI PMC
Gajdoš M., Mikl M., Mareèek R. (2016). Mask_explorer: A tool for exploring brain masks in fMRI group analysis. Comput. Methods Programs Biomed. 134 155–163. 10.1016/j.cmpb.2016.07.015 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. Brain Lang. 125 330–343. 10.1016/j.bandl.2013.02.006 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. Brain Cogn. 78 85–93. 10.1016/j.bandc.2011.12.004 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. Neurology 60 775–781. 10.1212/01.WNL.0000044398.73241.13 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. J. Neurol. Sci. 184 123–130. 10.1016/S0022-510X(00)00491-3 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. Brain Lang. 120 52–60. 10.1016/j.bandl.2011.08.007 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. Front. Neurosci. 11:53. 10.3389/fnins.2017.00053 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. Brain Lang. 73 1–16. 10.1006/brln.2000.2290 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. Brain Lang. 80 603–616. 10.1006/brln.2001.2630 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. Cortex 45 991–1011. 10.1016/j.cortex.2009.03.010 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. Brain Lang. 97 243–257. 10.1016/j.bandl.2005.10.011 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. PLoS One 14:e0217922. 10.1371/journal.pone.0217922 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. J. Neurolinguistics 51 221–235. 10.1016/j.jneuroling.2019.03.004 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. Parkinsonism Relat. Disord. 84 122–128. 10.1016/j.parkreldis.2021.02.012 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. Mov. Disord. 30 1098–1106. 10.1002/mds.26167 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. Cortex 45 982–990. 10.1016/j.cortex.2009.02.010 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. Brain Lang. 85 347–356. 10.1016/S0093-934X(03)00063-4 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. PLoS One 17:e0276218. 10.1371/journal.pone.0276218 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. Behav. Neurol. 2015:983606. 10.1155/2015/983606 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. Èes. Slov. Neurol. Neurochir. 81 60–65. 10.14735/amcsnn201860 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. Int. J. Lang. Commun. Disord. 52 456–468. 10.1111/1460-6984.12284 PubMed DOI
McGregor M. M., Nelson A. B. (2019). Circuit mechanisms of Parkinson’s disease. Neuron 101 1042–1056. 10.1016/j.neuron.2019.03.004 PubMed DOI
Mesulam M.-M. (1999). Neuroplasticity failure in Alzheimer’s disease. Neuron 24 521–529. 10.1016/S0896-6273(00)81109-5 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. Brain Stimulat. 13 597–599. 10.1016/j.brs.2020.01.015 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. Soc. Cogn. Affect. Neurosci. 7 604–609. 10.1093/scan/nss055 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. Cortex 45 960–971. 10.1016/j.cortex.2009.02.019 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. Magn. Reson. Med. 55 1227–1235. 10.1002/mrm.20900 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. Mov. Disord. 30 1591–1601. 10.1002/mds.26424 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. Parkinsonism Relat. Disord. 81 96–102. 10.1016/j.parkreldis.2020.10.032 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. Neuropsychologia 39 962–971. 10.1016/S0028-3932(01)00026-4 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. Brain Lang. 185 38–46. 10.1016/j.bandl.2018.08.002 PubMed DOI
Troche M. S., Altmann L. J. P. (2012). Sentence production in Parkinson disease: Effects of conceptual and task complexity. Appl. Psycholinguist. 33 225–251. 10.1017/S0142716411000336 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. NeuroImage 54 264–277. 10.1016/j.neuroimage.2010.06.044 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. Hum. Brain Mapp. 40 2275–2304. 10.1002/hbm.24523 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. Neuropsychologia 50 1794–1800. 10.1016/j.neuropsychologia.2012.04.004 PubMed DOI