Background: Alzheimer's disease is associated with impairments in decision making that undermine autonomy, health behaviors, and quality of life. Effort-based decision making, the process of weighing reward value against effort costs, is particularly disrupted in aging and Alzheimer's disease. However, aging is also characterized by a shift toward socioemotional and prosocial goals, which may preserve motivation and effortful behavior. Understanding prosocial effort-based decision making and its neural substrates in individuals at risk for AD may reveal early alterations in decision making and neural circuits that support healthy aging.
Methods: Fifty-two older adults from the PREVENT-AD cohort (mean age = 68.48, 38 females, 18 APOE4 carriers) completed an effort-based decision-making task comparing willingness to exert effort for rewards obtained for oneself or for charity. Decision response, response time, and vigor were analyzed using mixed-effects models. Reward-effort relationships were modeled using psychometric functions and compared using random-effects Bayesian model comparison, with parameter estimates from the winning model compared between conditions and between APOE4 carriers and non-carriers. Seed-to-voxel resting-state functional connectivity from the ventromedial prefrontal cortex and anterior cingulate cortex examined neural substrates of prosocial effort-based decision making, and ROI-to-ROI connectivity between regions of a frontostriatal reward network was compared between APOE4 carriers and non-carriers.
Results: Participants showed increased acceptance of effort for prosocial compared to selforiented rewards. The relationship between reward and effort in both conditions was best captured by a sigmoid function, with lower motivation for self-oriented compared to prosocial rewards. Across all participants, higher motivation for prosocial compared to self-oriented rewards was associated with resting-state functional connectivity to the ventromedial prefrontal cortex and anterior cingulate cortex. APOE4 carriers showed lower overall motivation than non-carriers, but higher vigor when exerting effort for prosocial than self-oriented rewards, along with reduced nucleus accumbens-dorsal anterior cingulate connectivity that was associated with lower motivation for effort.
Conclusions: Prosocial incentives may be an effective strategy for motivating effortful behavior in older adults at risk for Alzheimer's disease. Although APOE4 carriers show greater aversion to accepting effort for both reward types, they exhibit heightened vigor when working for prosocial compared to self-oriented rewards. Leveraging prosocial motivation and its underlying neural circuitry may therefore represent a promising strategy to sustain goal-directed behavior and decision making, promote physical and cognitive activity, and support emotional and brain health in at-risk aging.
Keywords: Computational modeling; Effort discounting; Motivation; Preclinical Alzheimer’s disease; Reward processing; fMRI.