Association Between Social Cognition Changes and Resting State Functional Connectivity in Frontotemporal Dementia, Alzheimer's Disease, Parkinson's Disease, and Healthy Controls.

Namita Multani,David F Tang-Wai,Anne Catherine Vijverman,Cassandra J Anor,Ron Keren,Karen Misquitta,Connie Marras,Foad Taghdiri,Maria Carmela Tartaglia,Brenda Varriano,Susan Fox,Anthony E Lang

doi:10.3389/fnins.2019.01259

Abstract

ObjectiveTo determine the relationship between alterations in resting state functional connectivity and social cognition dysfunction among patients with frontotemporal dementia (FTD), Alzheimer’s disease (AD), Parkinson’s disease (PD), and healthy controls (HC).MethodsFifty-seven participants (FTD = 10, AD = 18, PD = 19, and HC = 10) underwent structural and functional imaging and completed the Awareness of Social Inference Test-Emotion Evaluation Test (TASIT-EET), Behavioral Inhibition System/Behavioral Activation System (BIS/BAS) scale, Revised Self-Monitoring Scale (RSMS), Interpersonal Reactivity Index (IRI), and Social Norms Questionnaire (SNQ). A multi-variate pattern analysis (MVPA) was carried out to determine activation differences between the groups. The clusters from the MVPA were used as seeds for the ROI-to-voxel analysis. Relationship between social cognition deficits and uncinate integrity was also investigated.ResultsBOLD signal activation differed among the four groups of AD, PD, FTD, and HC in the left inferior temporal gyrus-anterior division [L-ITG (ant)], right central opercular cortex (R-COp), right supramarginal gyrus, posterior division (R-SMG, post), right angular gyrus (R-AG), and R-ITG. The BOLD co-activation of the L-ITG (ant) with bilateral frontal pole (FP) and paracingulate gyrus was positively associated with IRI-perspective taking (PT) (r = 0.38, p = 0.007), SNQ total (r = 0.37, p = 0.009), and TASIT-EET (r = 0.47, p < 0.001).ConclusionPatients with neurodegenerative diseases showed alterations in connectivity in brain regions important for social cognition compared with HCs. Functional connectivity correlated with performance on social cognition tasks and alterations could be responsible for some of the social cognition deficits observed in all neurodegenerative diseases.

Highlights

Neurodegenerative diseases consist of a heterogeneous group of conditions, including frontotemporal dementia (FTD), Alzheimer’s disease (AD), and Parkinson’s disease (PD), that present with different clinical syndromes determined by the different brain areas and circuits most often affected
The following regions demonstrated a difference in peak blood oxygenlevel dependent (BOLD) signal between the four groups (i.e., AD, PD, FTD, and healthy controls (HCs)): (a) left inferior temporal gyrus (ITG), anterior division (L-ITG, ant), (b) right central opercular cortex (R-COp), (c) right supramarginal gyrus, posterior division (R-SMG, post), and right angular gyrus (R-AG), and (d) right ITG (R-ITG) (Supplementary Table 1 and Figure 1)
(a) L-ITG ROI (Supplementary Table 3A and Figure 2A): In the AD, PD, and FTD groups, a decreased functional connectivity was found between the L-ITG and the right and left lateral occipital cortex (R-LOC and L-LOC) compared to HC

Summary

Introduction

Neurodegenerative diseases consist of a heterogeneous group of conditions, including frontotemporal dementia (FTD), Alzheimer’s disease (AD), and Parkinson’s disease (PD), that present with different clinical syndromes determined by the different brain areas and circuits most often affected. There are a number of studies that have reported various social cognitive abnormalities in bvFTD patients, including abnormalities in Theory of Mind (ToM) detection of gaze direction, and recognition of facial and/or prosodic emotional expressions, in particular negative emotions such as fear and anger (Gregory et al, 2002; Keane et al, 2002; Rosen et al, 2004; Lavenu and Pasquier, 2005; DiehlSchmid et al, 2007; Eslinger et al, 2007; Kessels et al, 2007; Werner et al, 2007; Bediou et al, 2009). SvPPA and nfvPPA are primarily identified as language disorders, social cognition can be affected (Neary et al, 1998; Hodges and Miller, 2001; Multani et al, 2017) and loss of emotion detection and decreased empathy has been reported in svPPA and nvPPA (Multani et al, 2017)

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