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

Rasha Hyder; Mads Jensen; Andreas Højlund; Lilli Kimppa; Christopher J. Bailey; Jeppe L. Schaldemose; Martin B. Kinnerup; Karen Østergaard; Yury Shtyrov

doi:10.1016/j.nicl.2021.102718

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

Rasha Hyder^*, Mads Jensen, Andreas Højlund, Lilli Kimppa, Christopher J. Bailey, Jeppe L. Schaldemose, Martin B. Kinnerup, Karen Østergaard, Yury Shtyrov^*

^*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

13 Citationer (Scopus)

Abstract

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.

Originalsprog	Engelsk
Artikelnummer	102718
Tidsskrift	NeuroImage: Clinical
Vol/bind	32
Antal sider	14
ISSN	2213-1582
DOI	https://doi.org/10.1016/j.nicl.2021.102718
Status	Udgivet - jan. 2021

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10.1016/j.nicl.2021.102718Licens: CC BY-NC-ND

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title = "Functional connectivity of spoken language processing in early-stage Parkinson's disease: An MEG study",

abstract = "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.",

keywords = "Action verb, Classification, Functional connectivity, Magnetoencephalography (MEG), Morphosyntax, Parkinson's disease (PD)",

author = "Rasha Hyder and Mads Jensen and Andreas H{\o}jlund and Lilli Kimppa and Bailey, {Christopher J.} and Schaldemose, {Jeppe L.} and Kinnerup, {Martin B.} and Karen {\O}stergaard and Yury Shtyrov",

note = "Funding Information: This work was supported by the Center of Functionally Integrative Neuroscience (Department of Clinical Medicine, Aarhus University), Danish Council for Independent Research (DFF 6110-00486, project 23776), Danish Association of Parkinson's Disease (Parkinsonforeningen, project 30121), Basic Research Program of the NRU Higher School of Economics (HSE University) and Lundbeck Foundation (grants R140-2013-12951, R164-2013-15801). We declare no conflict of interest. We wish to thank neurologist Dr Adjmal Nahimi for his help in the clinical assessments of the PD patients included in this study. Funding Information: This work was supported by the Center of Functionally Integrative Neuroscience (Department of Clinical Medicine, Aarhus University), Danish Council for Independent Research (DFF 6110-00486, project 23776), Danish Association of Parkinson{\textquoteright}s Disease (Parkinsonforeningen, project 30121), Basic Research Program of the NRU Higher School of Economics (HSE University) and Lundbeck Foundation (grants R140-2013-12951, R164-2013-15801). We declare no conflict of interest. We wish to thank neurologist Dr Adjmal Nahimi for his help in the clinical assessments of the PD patients included in this study. Publisher Copyright: {\textcopyright} 2021 The Authors",

year = "2021",

month = jan,

doi = "10.1016/j.nicl.2021.102718",

language = "English",

volume = "32",

journal = "NeuroImage: Clinical",

issn = "2213-1582",

publisher = "Elsevier BV",

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TY - JOUR

T1 - Functional connectivity of spoken language processing in early-stage Parkinson's disease: An MEG study

AU - Hyder, Rasha

AU - Jensen, Mads

AU - Højlund, Andreas

AU - Kimppa, Lilli

AU - Bailey, Christopher J.

AU - Schaldemose, Jeppe L.

AU - Kinnerup, Martin B.

AU - Østergaard, Karen

AU - Shtyrov, Yury

N1 - Funding Information: This work was supported by the Center of Functionally Integrative Neuroscience (Department of Clinical Medicine, Aarhus University), Danish Council for Independent Research (DFF 6110-00486, project 23776), Danish Association of Parkinson's Disease (Parkinsonforeningen, project 30121), Basic Research Program of the NRU Higher School of Economics (HSE University) and Lundbeck Foundation (grants R140-2013-12951, R164-2013-15801). We declare no conflict of interest. We wish to thank neurologist Dr Adjmal Nahimi for his help in the clinical assessments of the PD patients included in this study. Funding Information: This work was supported by the Center of Functionally Integrative Neuroscience (Department of Clinical Medicine, Aarhus University), Danish Council for Independent Research (DFF 6110-00486, project 23776), Danish Association of Parkinson’s Disease (Parkinsonforeningen, project 30121), Basic Research Program of the NRU Higher School of Economics (HSE University) and Lundbeck Foundation (grants R140-2013-12951, R164-2013-15801). We declare no conflict of interest. We wish to thank neurologist Dr Adjmal Nahimi for his help in the clinical assessments of the PD patients included in this study. Publisher Copyright: © 2021 The Authors

PY - 2021/1

Y1 - 2021/1

N2 - 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.

AB - 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.

KW - Action verb

KW - Classification

KW - Functional connectivity

KW - Magnetoencephalography (MEG)

KW - Morphosyntax

KW - Parkinson's disease (PD)

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U2 - 10.1016/j.nicl.2021.102718

DO - 10.1016/j.nicl.2021.102718

M3 - Journal article

C2 - 34455187

AN - SCOPUS:85111631134

SN - 2213-1582

VL - 32

JO - NeuroImage: Clinical

JF - NeuroImage: Clinical

M1 - 102718

ER -

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

Abstract

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