Blunted Reward Prediction Error Encoding Drives Diminished Motivation to Explore in Apathy Associated With Traumatic Brain Injury

Clinical apathy might result from either a diminished willingness to exert effort for known rewards or from reduced motivation to explore potentially beneficial future opportunities. To identify the underlying cognitive and neural bases of apathy, we used task-based fMRI to examine motivated choice computations in patients with chronic traumatic brain injury (TBI)—a condition frequently associated with apathy—and compared their behavior and neural activity to that of healthy controls (CTRLs). Participants performed two choice tasks involving distinct types of motivational tradeoffs: i) An effort-value tradeoff task (the ‘Apples Task’) requiring them to decide how much physical effort they were willing to exert for varying reward magnitudes, and ii) An explore-exploit tradeoff task (the ‘Novelty-Bandit Task’) requiring them to choose between exploiting options with a known history of reward or exploring novel options with uncertain but potentially higher future value. Across both TBI and CTRL, higher apathy was associated with steeper effort-based discounting of rewards. This behavioral pattern was linked to heightened neural encoding of effort costs in a common network including central somatomotor areas, midcingulate, middle insula, and putamen across both TBI and CTRL. In contrast, the explore-exploit task revealed a neurocomputational signature of apathy unique to TBI. Apathy in TBI was not associated with an impaired ability to learn the immediate expected value of choices, but with a specific reduction in the latent valuation of gaining information about future rewards. This behavioral deficit was directly tied to blunted encoding of reward prediction errors (RPEs) when participants’ received feedback about their choices in frontopolar cortex (FPC), ventromedial prefrontal cortex, cingulate, insula, and dorsal and ventral striatum. These findings suggest a dual-mechanism account of apathy. While an aversion to effort may be a transdiagnostic feature of apathy, clinical apathy acquired after a TBI may be uniquely characterized by an impairment in future-oriented decision making. Optimistic valuation of uncertain choice opportunities elicits RPE when decisions to explore those opportunities are rewarded or unrewarded. We propose that blunted RPE encoding in prefrontal cortex and basal ganglia in TBI degrades a crucial teaching signal—preventing the individual from learning about the benefits of engaging in directed exploration of novel options, thereby diminishing their motivation to explore again in the future. This specific deficit in outcome monitoring and brain networks that encode RPEs at feedback highlights a potential target for neuromodulatory interventions aimed at rescuing motivation in patients with TBI.