Frontostriatal pathways gate processing of behaviorally relevant reward dimensions

• Published in: PLoS biology 2018-10, Vol.16 (10), p.e2005722-e2005722
• Main Authors: Weber, Susanna C, Kahnt, Thorsten, Quednow, Boris B, Tobler, Philippe N
• Format: Article
• Language: English
• Subjects: Adult; Automation; Behavior; Biology and Life Sciences; Brain; Brain - anatomy & histology; Brain - physiology; Brain Mapping - methods; Choice Behavior - physiology; Coding; Decision Making - physiology; Expected values; Female; Gating; Hedonic response; Human behavior; Humans; Information processing; Magnetic Resonance Imaging - methods; Male; Medical imaging; Medicine and Health Sciences; Motivation; Neostriatum; Neural networks; Neuroimaging; Neurosciences; NMR; Nuclear magnetic resonance; Physical Sciences; Prefrontal cortex; Prefrontal Cortex - physiology; Psychiatry; Ratings & rankings; Reinforcement; Research and Analysis Methods; Reward; Scanners; Sensory Gating - physiology; Social Sciences; Supervision; Ventral Striatum - diagnostic imaging; Young Adult
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.2005722

The value of rewards arises from multiple hedonic and motivational dimensions. Reward-encoding brain regions such as the ventral striatum (VS) are known to process these dimensions. However, the mechanism whereby distinct reward dimensions are selected for neural processing and guiding behavior remains unclear. Here, we used functional imaging to investigate how human individuals make either hedonic (liking) or motivational (wanting) evaluations of everyday items. We found that the two types of evaluations were differently modulated depending on whether participants won or lost these items. Neural activity in the VS encoded both hedonic and motivational dimensions of reward, whereas ventromedial prefrontal activity encoded primarily motivational evaluations and central orbitofrontal activity encoded predominantly hedonic evaluations. These distinct prefrontal representations arose regardless of which judgment was currently relevant for behavior. Critically, the VS preferentially processed the reward dimension currently being evaluated and showed judgment-specific functional connectivity with the dimension-specific prefrontal areas. Thus, our data are in line with a gating mechanism by which prefrontal cortex (PFC)-VS pathways flexibly encode reward dimensions depending on their behavioral relevance. These findings provide a prototype for a generalized information selection mechanism through content-tailored frontostriatal communication.