Common and distinct neural substrates for approach- and avoidance-motivated actions

Abstract

The motivation to approach rewards and avoid negative outcomes often guides human action. However, whether these opposing motivations for actions engage common or distinct neural pathways in humans remains unresolved. To address this, we conducted a functional magnetic resonance imaging study using a ready–set–go task with potential monetary gains (approach) and losses (avoidance) in 29 healthy individuals (18 males and 11 females). At the prefrontal level, the ventromedial prefrontal cortex and dorsomedial prefrontal cortex were preferentially activated by the anticipation of gains and losses, respectively, indicating distinct cortical representations of approach and avoidance motivations. At the subcortical level, the dorsolateral ventral midbrain (VM) was engaged during the anticipation of both gains and losses, whereas the ventromedial VM was selectively activated by gain anticipation. Crucially, dorsolateral VM activity was positively correlated with the subsequent peak grip force but not the reaction time (RT), suggesting its role in transmitting motivational signals to downstream motor circuits. At the motor cortical level, the activity of the primary motor cortex was correlated with both the grip force and RT. Together, these findings suggest a hierarchical circuit in which approach and avoidance motivations are distinctly represented in the prefrontal cortex, partially converge in the VM, and ultimately influence motor cortex activity to generate motor output. This framework provides evidence that opposing motivations engage both distinct and shared neural pathways and that their integration through subcortical–cortical interactions enables motivational signals to shape human motor action. Significance statement Human actions are energized by both approaching rewards and avoiding punishments, but how these opposing motivated actions converge in the brain remains unclear. Using fMRI during a motivational ready–set–go task, we discovered that approach and avoidance motivations engage distinct prefrontal representations that partially converge in the dorsolateral ventral midbrain. This midbrain region encoded motivational intensity regardless of valence and selectively predicted peak grip force, but not reaction time, suggesting its role in scaling motor output strength, a key component of motor vigor. These findings reveal a hierarchical circuit in which opposing motivations are differentiated cortically, integrated subcortically, and transformed into motor output through mesocortical pathways. This framework advances understanding of motivation‒motor interactions, with implications for treating disorders affecting motivated action.