Prosocial deficits in behavioral variant frontotemporal dementia relate to reward network atrophy - PubMed (original) (raw)

. 2017 Sep 14;7(10):e00807.

doi: 10.1002/brb3.807. eCollection 2017 Oct.

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Prosocial deficits in behavioral variant frontotemporal dementia relate to reward network atrophy

Virginia E Sturm et al. Brain Behav. 2017.

Abstract

Introduction: Empathy and shared feelings of reward motivate individuals to share resources with others when material gain is not at stake. Behavioral variant frontotemporal dementia (bvFTD) is a neurodegenerative disease that affects emotion- and reward-relevant neural systems. Although there is diminished empathy and altered reward processing in bvFTD, how the disease impacts prosocial behavior is less well understood.

Methods: A total of 74 participants (20 bvFTD, 15 Alzheimer's disease [AD], and 39 healthy controls) participated in this study. Inspired by token-based paradigms from animal studies, we developed a novel task to measure prosocial giving (the "Giving Game"). On each trial of the Giving Game, participants decided how much money to offer to the experimenter, and prosocial giving was the total amount that participants gave to the experimenter when it cost them nothing to give. Voxel-based morphometry was then used to identify brain regions that were associated with prosocial giving.

Results: Prosocial giving was lower in bvFTD than in healthy controls; prosocial giving in AD did not differ significantly from either of the other groups. Whereas lower prosocial giving was associated with atrophy in the right pulvinar nucleus of the thalamus, greater prosocial giving was associated with atrophy in the left ventral striatum.

Conclusion: These findings suggest that simple acts of generosity deteriorate in bvFTD due to lateralized atrophy in reward-relevant neural systems that promote shared feelings of positive affect.

Keywords: empathy; generosity; giving; neurodegenerative; prosocial.

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Figures

Figure 1

Figure 1

An example of each the four trial types: (a) prosocial giving (giving to the experimenter does not impact the participant's own winnings on that trial), (b) selfless giving (giving to the experimenter decreases the participant's winning on that trial), (c) catch trials 1 (there is one choice that is advantageous to both the participant and the experimenter), and (d) catch trials 2 (there is one choice that is advantageous to the participant without impacting the experimenter's winnings on that trial)

Figure 2

Figure 2

Atrophy patterns in the bv

FTD

and

AD

groups. Voxel‐based morphometry analyses (controlling for age, sex, and total intracranial volume) confirmed that each of the diagnostic groups had atrophy patterns that were consistent with their clinical syndrome (p raw < .001). Compared to the healthy controls (N = 28), (a) patients with bv

FTD

(N = 17) had atrophy in the anterior insula, anterior cingulate cortex, amygdala, thalamus, prefrontal cortex, and orbitofrontal cortex whereas (b) patients with

AD

(N = 13) had atrophy in posterior cingulate cortex, precuneus, hippocampus, and lateral temporoparietal cortex

Figure 3

Figure 3

Neural correlates of prosocial giving. Regions in which smaller gray matter volume was associated with lower prosocial giving (cool colors) and greater prosocial giving (warm colors) at p raw < .001 (covariates included age, sex,

CDR

Total, diagnosis, and total intracranial volume). (a) Across all participants (N = 58), smaller volume in the right pulvinar nucleus of the thalamus was associated with lower prosocial giving. In a subset of participants (N = 35), when we included participants’ confidence ratings as an additional covariate, smaller volume in the left pulvinar nucleus of the thalamus was also associated with lower prosocial giving. (b) In the analyses of both the entire sample and the subset of participants with confidence ratings, smaller volume in left ventral striatum was associated with greater prosocial giving

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