Abstract
Patients with Parkinson’s disease have difficulties with self-initiating a task and maintaining a steady task performance. We hypothesized that these difficulties relate to reorganization in the sensorimotor execution, cingulo-opercular task-set maintenance, and frontoparietal adaptive control networks. We tested this hypothesis using graph theory-based network analysis of a composite network including a total of 86 nodes, derived from the three networks of interest. Resting-state functional magnetic resonance images were collected from 30 patients with Parkinson’s disease (age 42–75 years, 11 females; Hoehn and Yahr score 2–3, average 2.4 ± 0.4) in their off-medication state and 30 matched control subjects (age 44–75 years, 10 females). For each node, we calculated strength as a general measure of connectivity, global efficiency and betweenness centrality as measures of functional integration, and clustering coefficient and local efficiency as measures of functional segregation. We found reduced node strength, clustering, and local efficiency in sensorimotor and posterior temporal nodes. There was also reduced node strength and betweenness centrality in the dorsal anterior insula and temporoparietal junction nodes of the cingulo-opercular network. These nodes are involved in integrating multimodal information, specifically related to self-awareness, sense of agency, and ultimately to intact perception of self-in-action. Moreover, we observed significant correlations between global disease severity and averaged graph metrics of the whole network. In addition to the well-known task-related frontostriatal mechanisms, we propose that the resting-state reorganization in the composite network can contribute to problems with self-initiation and task-set maintenance in Parkinson’s disease.
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Acknowledgments
This work was supported by the National Institute of Neurological Disorders and Stroke Intramural Research Program. The authors thank Kazumi Iseki and Cecile Gallea for their help with data collection, Pritha Ghosh and Sarah Kranick for their help with patient assessments, Patrick Malone for his help with pilot data analysis, Ziad Saad for his help with data preprocessing, and Devera Schoenberg, M.Sc., for editorial assistance.
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Appendix: Box
Appendix: Box
Graph metric definitionsFootnote 1
Functional segregation of a neural network refers to its ability for specialized processing within clusters of nodes.
Functional integration is related to a neural network’s ability to bind information efficiently from distributed regions.
Node strength indicates how strongly one node is connected to the rest of the nodes in the network. It is computed as the sum of the weights of the connections that link a node to the rest of the nodes.
Path is the shortest distance (i.e., minimum number of connections) between a node and every other node in the network. Efficiency is inversely related to path length.
Global efficiency is calculated as the inverse of the average shortest path length between all pairs of nodes in the network. It is a measure of functional integration.
Node Betweenness Centrality indicates how central a node is to the communication among other nodes in the network. It is computed as the fraction of all shortest paths in the network that contain a given node. Nodes with high values of betweenness centrality participate in a large number of shortest paths and potentially function as hubs.
Clustering coefficient measures the density of connections between neighboring nodes. It is computed as the number of connections that exist between the nearest neighbors of a node as a proportion of the maximum number of possible connections. High clustering is associated with high local efficiency of information transfer.
Local efficiency reflects how relevant a node is for the communication among neighbors. It is computed as the inverse of the average shortest path connecting all neighbors of a node. It is a nodal measure of the average efficiency within a local neighborhood, and is related to the clustering coefficient.
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Tinaz, S., Lauro, P., Hallett, M. et al. Deficits in task-set maintenance and execution networks in Parkinson’s disease. Brain Struct Funct 221, 1413–1425 (2016). https://doi.org/10.1007/s00429-014-0981-8
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DOI: https://doi.org/10.1007/s00429-014-0981-8