Spatiotemporal dissociation of physical salience and stimulus evaluation in the human midbrain.

Abstract

The brain must detect and evaluate rewards amidst multiple stimuli to generate adaptive behavior. Physically salient stimuli draw greater attention, potentially influencing their subsequent evaluation. An influential framework proposes that rewards are processed through a two-component dopaminergic response: an early, value-agnostic salience signal, followed by a partially overlapping but temporally lagged signal reflecting stimulus evaluation. Yet, evidence for this framework in humans is lacking due to spatiotemporal limitations of neuroimaging methods. Using bespoke simultaneous 7T functional magnetic resonance imaging (fMRI)-electroencephalogram (EEG) developments, we decoupled reward-anticipatory midbrain signals with distinct spatiotemporal profiles: an early signal in posterior substantia nigra (SN) consistent with physical salience, followed by a lagged signal in anterior SN and ventral tegmental area, likely reflecting evaluative processes such as value and/or motivational salience. We also demonstrate that the early physical salience signal enhances this later evaluative response, offering the first evidence of attention-guided reward processing in the human midbrain.