What a stimulus predicts, not what it depicts, determines striatal reward signals

Abstract

Free viewing of emotional pictures activates motivational circuits as a function of arousal and valence, yet, because no real outcomes are delivered, anticipatory wanting and consummatory liking cannot be dissociated. Gustatory neuroimaging paradigms deliver actual rewards but use impoverished, affectively neutral cues that do not engage natural selective attention. We bridged these paradigms by presenting emotional images alongside food photographs that either predicted juice delivery (Food+) or did not (Food-), all within a single fMRI session. On each Food+ trial, participants indicated in real time whether they wanted the juice, enabling a within-subject dissociation of anticipatory from consummatory signals. Nucleus accumbens showed a large and selective response to Food+ cues that exceeded activation to both pleasant (erotica) and unpleasant (mutilation) high-arousal images, establishing that mesolimbic engagement tracked outcome prediction rather than emotional arousal, affective valence, or visual content. A temporal dissociation further revealed that nucleus accumbens carried the dominant anticipatory signal during the cue period, while ventromedial prefrontal cortex carried the dominant outcome-period signal at juice delivery, a pattern consistent with the wanting and liking distinction. Representational similarity analysis confirmed that outcome prediction, rather than emotional arousal, affective valence, or visual category, was the dominant organizing principle of the multivariate neural response across the full region-of-interest network. Together, these findings show that whether a visual stimulus engages reward circuitry depends less on what it depicts than on what it predicts, and provide a framework for studying individual differences in appetitive motivation and cue-induced eating. Significance statementWhether a food image engages brain reward circuitry depends not on what it depicts, but on what it predicts. We scanned participants while they viewed food images that either preceded a real opportunity to receive juice or did not, alongside erotic, threatening, and neutral scenes. Nucleus accumbens, a core reward region, responded selectively to food images predicting juice, with a response that exceeded even the response to erotic images. Ventromedial-prefrontal cortex, by contrast, tracked actual juice receipt, dissociating anticipation from consumption. Across a ten-region network, learned reward prediction, rather than emotional arousal, valence, or visual category, organized the neural response. These findings establish a human neuroimaging paradigm for studying how cue-driven motivation goes awry in obesity, addiction, and compulsive eating.