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Cortex. 2018 Nov;108:252-264. doi: 10.1016/j.cortex.2018.08.002. Epub 2018 Aug 11.

Altered topology of the functional speech production network in non-fluent/agrammatic variant of PPA.

Author information

1
Department of Neurology, Memory and Aging Center, University of California San Francisco, CA, USA. Electronic address: MariaLuisa.Mandelli@ucsf.edu.
2
Department of Neurology, Memory and Aging Center, University of California San Francisco, CA, USA.
3
Memory Unit, Department of Neurology, Hospital de la Santa Creu i Sant Pau - Biomedical Research Institute Sant Pau - Universitat Autonoma de Barcelona, Spain; Centro de Investigacion Biomedica en Red de Enfermedades Neurodegenerativas - CIBERNED, Spain.
4
Department of Communication Science and Disorders, Faculty of Rehabilitation Medicine, University of Alberta, Edmonton, AB, Canada.
5
Department of Communication Sciences and Disorders, University of Texas, Austin, USA.
6
Cognition and Brain Plasticity Group [Bellvitge Biomedical Research Institute-IDIBELL], L'Hospitalet de Llobregat, Barcelona, Spain; Fundació ACE Memory Clinic and Research Center, Institut Catalá de Neurociències Aplicades, Barcelona, Spain.
7
Memory Unit, Department of Neurology, Hospital de la Santa Creu i Sant Pau - Biomedical Research Institute Sant Pau - Universitat Autonoma de Barcelona, Spain.
8
Department of Neurology, Memory and Aging Center, University of California San Francisco, CA, USA; Department of Pathology, University of California San Francisco, CA, USA.

Abstract

Non-fluent/agrammatic primary progressive aphasia (nfvPPA) is caused by neurodegeneration within the left fronto-insular speech and language production network (SPN). Graph theory is a branch of mathematics that studies network architecture (topology) by quantifying features based on its elements (nodes and connections). This approach has been recently applied to neuroimaging data to explore the complex architecture of the brain connectome, though few studies have exploited this technique in PPA. Here, we used graph theory on functional MRI resting state data from a group of 20 nfvPPA patients and 20 matched controls to investigate topological changes in response to focal neurodegeneration. We hypothesized that changes in the network architecture would be specific to the affected SPN in nfvPPA, while preserved in the spared default mode network (DMN). Topological configuration was quantified by hub location and global network metrics. Our findings showed a less efficiently wired and less optimally clustered SPN, while no changes were detected in the DMN. The SPN in the nfvPPA group showed a loss of hubs in the left fronto-parietal-temporal area and new critical nodes in the anterior left inferior-frontal and right frontal regions. Behaviorally, speech production score and rule violation errors correlated with the strength of functional connectivity of the left (lost) and right (new) regions respectively. This study shows that focal neurodegeneration within the SPN in nfvPPA is associated with network-specific topological alterations, with the loss and gain of crucial hubs and decreased global efficiency that were better accounted for through functional rather than structural changes. These findings support the hypothesis of selective network vulnerability in nfvPPA and may offer biomarkers for future behavioral intervention.

KEYWORDS:

Functional connectivity; Graph theory; Primary progressive aphasia; Speech production network; Topological configuration

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