Reward is not reward: Differential impacts of primary and secondary rewards on expectation, outcome, and prediction error in the human brain's reward processing regions

Abstract

According to their nature, rewarding stimuli are classified as primary (e.g., food, sex) and secondary (e.g., money) rewards. Neuroimaging studies have provided valuable insights in neural reward processing and its various aspects including reward expectation, outcome and prediction error encoding. However, there is only limited evidence of whether the two different types of rewards are processed in common or distinct brain areas, in particular when considering the different functions of reward processing. We analyzed a sample of 42 healthy, male participants using task-based functional magnetic resonance imaging (fMRI) during a variant of the monetary incentive delay task. We aimed to investigate the effects of three different rewarding stimuli-two primary (food and sex) and one secondary (money)-on the various functions of reward processing. To provide a thorough description, we focused on 12 brain regions of interest and utilized the Bayes factor bound (BFB) to express stimulus-related main effects and pairwise differences at different levels of evidence, ranging from weak to decisive. Our results revealed a dominance of sexually charged stimuli in engaging the brain's reward structures for all investigated aspects of reward processing. Nevertheless, the ventral tegmental area, amygdala, ventral caudate, ventromedial prefrontal cortex, subgenual anterior cingulate cortex, and lateral orbitofrontal cortex were activated by both primary and secondary reward outcomes. For other reward processing functions, i.e., reward expectation and the prediction error, effects of the different stimuli were weaker, and effects from one reward type cannot easily be generalized to the other.

Keywords: Bayes factor bound; Neural activation; Prediction error; Primary reinforcer; Secondary reinforcer; fMRI.