Ventromedial prefrontal cortex lesions disrupt learning to reward others

Reinforcement learning is a fundamental process through which humans and other animals attain rewards for themselves. However, to act prosocially, we must also learn how our choices reward others. The ventromedial prefrontal cortex has been independently linked to reinforcement learning and prosocial behaviour, yet its causal impact on prosocial reinforcement learning and the roles of its multiple subregions remain unknown. Here, a large group of adults with rare focal ventromedial prefrontal cortex damage (n = 28) and two carefully age- and gender-matched control groups (lesions elsewhere, n = 21; healthy controls, n = 124) completed a reinforcement learning task where they learnt to win rewards for another person (prosocial), for themselves (self) or in a control condition where participants saw points, but they were not translated into rewards for either individual (no one, control condition) on separate trials. A novel computational model incorporating separate learning rates for positive and negative prediction errors best explained behaviour in all groups. Importantly, compared to both control groups, patients with ventromedial prefrontal cortex damage were less accurate and had lower learning rates from positive prediction errors when rewarding another person relative to when no one benefitted, and higher learning rates for negative prediction errors when learning for others relative to self. Unlike controls, ventromedial prefrontal cortex lesion patients also showed a reduced self-benefitting advantage. They were equally accurate and learnt at a similar rate from positive prediction errors for self and neither individual. Strikingly, voxel-based lesion-symptom mapping revealed that damage to subgenual anterior cingulate cortex and anterior cingulate cortex gyrus specifically disrupted prosocial reinforcement learning. These findings highlight the importance of ventromedial prefrontal cortex integrity for multiple aspects of reinforcement learning, with damage to subgenual anterior cingulate cortex and anterior cingulate cortex gyrus critical in learning to reward others.