Functional connectivity of spoken language processing in early-stage Parkinson’s disease: An MEG study

Parkinson’s disease (PD) is a neurodegenerative disorder, well-known for its motor symptoms; however, it also adversely affects cognitive functions, including language, a highly important human ability. PD pathology is associated, even in the early stage of the disease, with alterations in the funct...

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Main Authors: Rasha Hyder, Mads Jensen, Andreas Højlund, Lilli Kimppa, Christopher J. Bailey, Jeppe L. Schaldemose, Martin B. Kinnerup, Karen Østergaard, Yury Shtyrov
Format: Article
Language:English
Published: Elsevier 2021-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158221001625
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author Rasha Hyder
Mads Jensen
Andreas Højlund
Lilli Kimppa
Christopher J. Bailey
Jeppe L. Schaldemose
Martin B. Kinnerup
Karen Østergaard
Yury Shtyrov
spellingShingle Rasha Hyder
Mads Jensen
Andreas Højlund
Lilli Kimppa
Christopher J. Bailey
Jeppe L. Schaldemose
Martin B. Kinnerup
Karen Østergaard
Yury Shtyrov
Functional connectivity of spoken language processing in early-stage Parkinson’s disease: An MEG study
NeuroImage: Clinical
Parkinson’s disease (PD)
Magnetoencephalography (MEG)
Functional connectivity
Classification
Action verb
Morphosyntax
author_facet Rasha Hyder
Mads Jensen
Andreas Højlund
Lilli Kimppa
Christopher J. Bailey
Jeppe L. Schaldemose
Martin B. Kinnerup
Karen Østergaard
Yury Shtyrov
author_sort Rasha Hyder
title Functional connectivity of spoken language processing in early-stage Parkinson’s disease: An MEG study
title_short Functional connectivity of spoken language processing in early-stage Parkinson’s disease: An MEG study
title_full Functional connectivity of spoken language processing in early-stage Parkinson’s disease: An MEG study
title_fullStr Functional connectivity of spoken language processing in early-stage Parkinson’s disease: An MEG study
title_full_unstemmed Functional connectivity of spoken language processing in early-stage Parkinson’s disease: An MEG study
title_sort functional connectivity of spoken language processing in early-stage parkinson’s disease: an meg study
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2021-01-01
description Parkinson’s disease (PD) is a neurodegenerative disorder, well-known for its motor symptoms; however, it also adversely affects cognitive functions, including language, a highly important human ability. PD pathology is associated, even in the early stage of the disease, with alterations in the functional connectivity within cortico-subcortical circuitry of the basal ganglia as well as within cortical networks. Here, we investigated functional cortical connectivity related to spoken language processing in early-stage PD patients. We employed a patient-friendly passive attention-free paradigm to probe neurophysiological correlates of language processing in PD patients without confounds related to active attention and overt motor responses. MEG data were recorded from a group of newly diagnosed PD patients and age-matched healthy controls who were passively presented with spoken word stimuli (action and abstract verbs, as well as grammatically correct and incorrect inflectional forms) while focussing on watching a silent movie. For each of the examined linguistic aspects, a logistic regression classifier was used to classify participants as either PD patients or healthy controls based on functional connectivity within the temporo-fronto-parietal cortical language networks. Classification was successful for action verbs (accuracy = 0.781, p-value = 0.003) and, with lower accuracy, for abstract verbs (accuracy = 0.688, p-value = 0.041) and incorrectly inflected forms (accuracy = 0.648, p-value = 0.021), but not for correctly inflected forms (accuracy = 0.523, p-value = 0.384). Our findings point to quantifiable differences in functional connectivity within the cortical systems underpinning language processing in newly diagnosed PD patients compared to healthy controls, which arise early, in the absence of clinical evidence of deficits in cognitive or general language functions. The techniques presented here may aid future work on establishing neurolinguistic markers to objectively and noninvasively identify functional changes in the brain’s language networks even before clinical symptoms emerge.
topic Parkinson’s disease (PD)
Magnetoencephalography (MEG)
Functional connectivity
Classification
Action verb
Morphosyntax
url http://www.sciencedirect.com/science/article/pii/S2213158221001625
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spelling doaj-6d8b58e72f1e41298e2b337019131b4d2021-08-28T04:44:57ZengElsevierNeuroImage: Clinical2213-15822021-01-0132102718Functional connectivity of spoken language processing in early-stage Parkinson’s disease: An MEG studyRasha Hyder0Mads Jensen1Andreas Højlund2Lilli Kimppa3Christopher J. Bailey4Jeppe L. Schaldemose5Martin B. Kinnerup6Karen Østergaard7Yury Shtyrov8Center of Functionally Integrative Neuroscience (CFIN), Department of Clinical Medicine, Aarhus University, Aarhus, Denmark; Institute of Clinical Neuroscience and Medical Psychology, Heinrich‐Heine University Düsseldorf, Düsseldorf, Germany; Corresponding authors at: Center of Functionally Integrative Neuroscience (CFIN), Universitetsbyen 3, Building 1710, Aarhus C 8000, Denmark.Center of Functionally Integrative Neuroscience (CFIN), Department of Clinical Medicine, Aarhus University, Aarhus, Denmark; Research Unit for Robophilosophy and Integrative Social Robotics, Aarhus University, DenmarkCenter of Functionally Integrative Neuroscience (CFIN), Department of Clinical Medicine, Aarhus University, Aarhus, DenmarkCenter of Functionally Integrative Neuroscience (CFIN), Department of Clinical Medicine, Aarhus University, Aarhus, Denmark; Cognitive Brain Research Unit, Department of Psychology and Logopedics, Faculty of Medicine, University of Helsinki, FinlandCenter of Functionally Integrative Neuroscience (CFIN), Department of Clinical Medicine, Aarhus University, Aarhus, DenmarkDepartment of Nuclear Medicine and PET Centre, Aarhus University Hospital, Aarhus, DenmarkDepartment of Nuclear Medicine and PET Centre, Aarhus University Hospital, Aarhus, DenmarkSano Private Hospital, Denmark; Department of Neurology, Aarhus University Hospital (AUH), DenmarkCenter of Functionally Integrative Neuroscience (CFIN), Department of Clinical Medicine, Aarhus University, Aarhus, Denmark; Centre for Cognition and Decision Making, Institute for Cognitive Neuroscience, HSE University, Moscow, Russian Federation; Corresponding authors at: Center of Functionally Integrative Neuroscience (CFIN), Universitetsbyen 3, Building 1710, Aarhus C 8000, Denmark.Parkinson’s disease (PD) is a neurodegenerative disorder, well-known for its motor symptoms; however, it also adversely affects cognitive functions, including language, a highly important human ability. PD pathology is associated, even in the early stage of the disease, with alterations in the functional connectivity within cortico-subcortical circuitry of the basal ganglia as well as within cortical networks. Here, we investigated functional cortical connectivity related to spoken language processing in early-stage PD patients. We employed a patient-friendly passive attention-free paradigm to probe neurophysiological correlates of language processing in PD patients without confounds related to active attention and overt motor responses. MEG data were recorded from a group of newly diagnosed PD patients and age-matched healthy controls who were passively presented with spoken word stimuli (action and abstract verbs, as well as grammatically correct and incorrect inflectional forms) while focussing on watching a silent movie. For each of the examined linguistic aspects, a logistic regression classifier was used to classify participants as either PD patients or healthy controls based on functional connectivity within the temporo-fronto-parietal cortical language networks. Classification was successful for action verbs (accuracy = 0.781, p-value = 0.003) and, with lower accuracy, for abstract verbs (accuracy = 0.688, p-value = 0.041) and incorrectly inflected forms (accuracy = 0.648, p-value = 0.021), but not for correctly inflected forms (accuracy = 0.523, p-value = 0.384). Our findings point to quantifiable differences in functional connectivity within the cortical systems underpinning language processing in newly diagnosed PD patients compared to healthy controls, which arise early, in the absence of clinical evidence of deficits in cognitive or general language functions. The techniques presented here may aid future work on establishing neurolinguistic markers to objectively and noninvasively identify functional changes in the brain’s language networks even before clinical symptoms emerge.http://www.sciencedirect.com/science/article/pii/S2213158221001625Parkinson’s disease (PD)Magnetoencephalography (MEG)Functional connectivityClassificationAction verbMorphosyntax