Parkinson's disease speech production network as determined by graph-theoretical network analysis

Jana Schill; Kristina Simonyan; Simon Lang; Christian Mathys; Christiane Thiel; Karsten Witt

doi:10.1162/netn_a_00310

Parkinson's disease speech production network as determined by graph-theoretical network analysis

Netw Neurosci. 2023 Jun 30;7(2):712-730. doi: 10.1162/netn_a_00310. eCollection 2023.

Authors

Jana Schill¹, Kristina Simonyan^{2

3}, Simon Lang¹, Christian Mathys^{4

5

6}, Christiane Thiel^{5

7}, Karsten Witt^{1

5}

Affiliations

¹ Department of Neurology, School of Medicine and Health Sciences, University of Oldenburg, Oldenburg, Germany.
² Department of Otolaryngology, Head and Neck Surgery, Harvard Medical School, Boston, MA, USA.
³ Department of Otolaryngology, Head and Neck Surgery, Massachusetts Eye and Ear, Boston, MA, USA.
⁴ Institute of Radiology and Neuroradiology, Evangelisches Krankenhaus, University of Oldenburg, Oldenburg, Germany.
⁵ Research Center Neurosensory Science, University of Oldenburg, Oldenburg, Germany.
⁶ Department of Diagnostic and Interventional Radiology, University of Düsseldorf, Düsseldorf, Germany.
⁷ Department of Psychology, School of Medicine and Health Sciences, University of Oldenburg, Oldenburg, Germany.

Abstract

Parkinson's disease (PD) can affect speech as well as emotion processing. We employ whole-brain graph-theoretical network analysis to determine how the speech-processing network (SPN) changes in PD, and assess its susceptibility to emotional distraction. Functional magnetic resonance images of 14 patients (aged 59.6 ± 10.1 years, 5 female) and 23 healthy controls (aged 64.1 ± 6.5 years, 12 female) were obtained during a picture-naming task. Pictures were supraliminally primed by face pictures showing either a neutral or an emotional expression. PD network metrics were significantly decreased (mean nodal degree, p < 0.0001; mean nodal strength, p < 0.0001; global network efficiency, p < 0.002; mean clustering coefficient, p < 0.0001), indicating an impairment of network integration and segregation. There was an absence of connector hubs in PD. Controls exhibited key network hubs located in the associative cortices, of which most were insusceptible to emotional distraction. The PD SPN had more key network hubs, which were more disorganized and shifted into auditory, sensory, and motor cortices after emotional distraction. The whole-brain SPN in PD undergoes changes that result in (a) decreased network integration and segregation, (b) a modularization of information flow within the network, and (c) the inclusion of primary and secondary cortical areas after emotional distraction.

Keywords: Emotional distraction; Functional magnetic resonance imaging; Network analysis; Parkinson’s disease; Speech production network.

Abstract

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