Dopamine-Related Reduction of Semantic Spreading Activation in Patients With Parkinson’s Disease

Impaired performance in verbal fluency (VF) tasks is a frequent observation in Parkinson’s disease (PD). As to the nature of the underlying cognitive deficit, it is commonly attributed to a frontal-type dysexecutive syndrome due to nigrostriatal dopamine depletion. Whereas dopaminergic medication ty...

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Main Authors: Hannes Ole Tiedt, Felicitas Ehlen, Fabian Klostermann
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-03-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnhum.2022.837122/full
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author Hannes Ole Tiedt
Felicitas Ehlen
Felicitas Ehlen
Fabian Klostermann
Fabian Klostermann
author_facet Hannes Ole Tiedt
Felicitas Ehlen
Felicitas Ehlen
Fabian Klostermann
Fabian Klostermann
author_sort Hannes Ole Tiedt
collection DOAJ
description Impaired performance in verbal fluency (VF) tasks is a frequent observation in Parkinson’s disease (PD). As to the nature of the underlying cognitive deficit, it is commonly attributed to a frontal-type dysexecutive syndrome due to nigrostriatal dopamine depletion. Whereas dopaminergic medication typically improves VF performance in PD, e.g., by ameliorating impaired lexical switching, its effect on semantic network activation is unclear. Data from priming studies suggest that dopamine causes a faster decay of semantic activation spread. The aim of the current study was to examine the impact of dopaminergic medication on the dynamic change of word frequency during VF performance as a measure of semantic spreading activation. To this end, we performed a median split analysis of word frequency during phonemic and semantic VF task performance in a PD group tested while receiving dopaminergic medication (ON) as well as after drug withdrawal (i.e., OFF), and in a sample of age-matched healthy volunteers (both groups n = 26). Dopaminergic medication in the PD group significantly affected phonemic VF with improved word production as well as increased error-rates. The expected decrease of word frequency during VF task performance was significantly smaller in the PD group ON medication than in healthy volunteers across semantic and phonemic VF. No significant group-difference emerged between controls and the PD group in the OFF condition. The comparison between both treatment conditions within the PD group did not reach statistical significance. The observed pattern of results indicates a faster decay of semantic network activation during lexical access in PD patients on dopaminergic medication. In view of improved word generation, this finding is consistent with a concept of more focused neural activity by an increased signal-to-noise ratio due to dopaminergic neuromodulation. However, the effect of dopaminergic stimulation on VF output suggests a trade-off between these beneficial effects and increased error-rates.
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spelling doaj.art-e9094343b2fb438bba7801c0430104952022-12-22T03:13:35ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612022-03-011610.3389/fnhum.2022.837122837122Dopamine-Related Reduction of Semantic Spreading Activation in Patients With Parkinson’s DiseaseHannes Ole Tiedt0Felicitas Ehlen1Felicitas Ehlen2Fabian Klostermann3Fabian Klostermann4Department of Neurology, Motor and Cognition Group, Charité—Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universitätzu Berlin, Berlin, GermanyDepartment of Neurology, Motor and Cognition Group, Charité—Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universitätzu Berlin, Berlin, GermanyDepartment of Psychiatry, Jüdisches Krankenhaus Berlin, Berlin, GermanyDepartment of Neurology, Motor and Cognition Group, Charité—Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universitätzu Berlin, Berlin, GermanyBerlin School of Mind and Brain, Humboldt-Universität zu Berlin, Berlin, GermanyImpaired performance in verbal fluency (VF) tasks is a frequent observation in Parkinson’s disease (PD). As to the nature of the underlying cognitive deficit, it is commonly attributed to a frontal-type dysexecutive syndrome due to nigrostriatal dopamine depletion. Whereas dopaminergic medication typically improves VF performance in PD, e.g., by ameliorating impaired lexical switching, its effect on semantic network activation is unclear. Data from priming studies suggest that dopamine causes a faster decay of semantic activation spread. The aim of the current study was to examine the impact of dopaminergic medication on the dynamic change of word frequency during VF performance as a measure of semantic spreading activation. To this end, we performed a median split analysis of word frequency during phonemic and semantic VF task performance in a PD group tested while receiving dopaminergic medication (ON) as well as after drug withdrawal (i.e., OFF), and in a sample of age-matched healthy volunteers (both groups n = 26). Dopaminergic medication in the PD group significantly affected phonemic VF with improved word production as well as increased error-rates. The expected decrease of word frequency during VF task performance was significantly smaller in the PD group ON medication than in healthy volunteers across semantic and phonemic VF. No significant group-difference emerged between controls and the PD group in the OFF condition. The comparison between both treatment conditions within the PD group did not reach statistical significance. The observed pattern of results indicates a faster decay of semantic network activation during lexical access in PD patients on dopaminergic medication. In view of improved word generation, this finding is consistent with a concept of more focused neural activity by an increased signal-to-noise ratio due to dopaminergic neuromodulation. However, the effect of dopaminergic stimulation on VF output suggests a trade-off between these beneficial effects and increased error-rates.https://www.frontiersin.org/articles/10.3389/fnhum.2022.837122/fullParkinson’s diseasedopaminesemantic systemspreading activationverbal fluency
spellingShingle Hannes Ole Tiedt
Felicitas Ehlen
Felicitas Ehlen
Fabian Klostermann
Fabian Klostermann
Dopamine-Related Reduction of Semantic Spreading Activation in Patients With Parkinson’s Disease
Frontiers in Human Neuroscience
Parkinson’s disease
dopamine
semantic system
spreading activation
verbal fluency
title Dopamine-Related Reduction of Semantic Spreading Activation in Patients With Parkinson’s Disease
title_full Dopamine-Related Reduction of Semantic Spreading Activation in Patients With Parkinson’s Disease
title_fullStr Dopamine-Related Reduction of Semantic Spreading Activation in Patients With Parkinson’s Disease
title_full_unstemmed Dopamine-Related Reduction of Semantic Spreading Activation in Patients With Parkinson’s Disease
title_short Dopamine-Related Reduction of Semantic Spreading Activation in Patients With Parkinson’s Disease
title_sort dopamine related reduction of semantic spreading activation in patients with parkinson s disease
topic Parkinson’s disease
dopamine
semantic system
spreading activation
verbal fluency
url https://www.frontiersin.org/articles/10.3389/fnhum.2022.837122/full
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