The neural basis of prosocial effort-based decision-making in older adults at risk for Alzheimer's disease
Walker, C. S.; Barnoin, G.; Bennett, M.; Tremblay-Mercier, J.; Villeneuve, S.; Spreng, R. N.; Poirier, J.; Morris, L. S.; PREVENT-AD Research Group, ; Geddes, M. R.
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AbstractO_ST_ABSBackgroundC_ST_ABSAlzheimers 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 Alzheimers 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. MethodsFifty-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 monetary rewards obtained for oneself or for charity. Decision response (accept/reject), response time, and vigor were analyzed using mixed-effects models controlling for demographic and clinical covariates. Reward-effort relationships were modeled using various functions and compared using Bayesian model comparison. Seed-to-voxel resting-state functional connectivity from the ventromedial prefrontal cortex and anterior cingulate gyrus examined neural substrates of prosocial effort-based decision making, and ROI-to-ROI connectivity within the frontostriatal reward network was compared between APOE4 carriers and non-carriers. ResultsParticipants were more likely to accept effort for prosocial compared to self-oriented rewards. The relationship between reward and effort in both conditions was best captured by a sigmoid function, with higher bias away from effort expenditure for self-oriented compared to prosocial rewards. Across all participants, lower bias away from effort expenditure for prosocial compared to self-oriented rewards was associated with vmPFC and ACCg resting-state functional connectivity to frontal, temporal, and parietal regions. APOE4 carriers showed greater overall bias away from effort expenditure but higher vigor for prosocial than self-oriented rewards, along with reduced nucleus accumbens-dorsal anterior cingulate connectivity that was associated with bias away from effort. ConclusionsProsocial incentives may be an effective strategy for motivating effortful behavior in older adults at risk for Alzheimers disease. Although APOE4 carriers show greater aversion to initiating effort, 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 aging.
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