Frontostriatal pathways gate processing of behaviorally relevant reward dimensions

Abstract

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.

Choosing to view morbid information involves reward circuitry

“…Although we found activation in regions associated with reward and incentives (Diekhof et al, 2012;Bartra et al, 2013), it is important to be careful with the conclusion that it is "rewarding" to choose negative information (Poldrack, 2006). Reward regions are associated with a multitude of psychological processes (Bartra et al, 2013), and reward is a construct with different dissociable dimensions, including "liking" and "wanting" (e.g., Weber, Kahnt, Quednow & Tobler, 2018;Berridge, Robinson & Aldridge, 2009). In addition, the distributed pattern of activation that we found most likely reflects psychological processes beyond reward as well.…”

Choosing to view morbid information involves reward circuitry

“…Although we found activation in regions associated with reward and incentives, it is important to be careful with the conclusion that it is “rewarding” to choose negative information 42 . Reward regions are associated with a multitude of psychological processes 18 , and reward is a construct with different dissociable dimensions, including “liking” and “wanting” (e.g., 31 , 43 . In addition, the distributed pattern of activation that we found most likely reflects psychological processes beyond reward as well.…”

Differential contributions of ventral striatum subregions to the motivational and hedonic components of the affective processing of the reward

“…By comparison, the involvement of a subregion of the ventral striatum in the sensory pleasure experience is more striking. fMRI studies conducted in humans have sometimes reported the involvement of the ventral striatum in hedonic reactions ( 21,22 ), but less consistently than the mOFC ( 23 ). Studies conducted in rodents have highlighted the presence of small “hedonic hotspots” in the shell division of the ventral striatum enhancing the hedonic experience when stimulated with opioids, orexin, or endocannabinoid ( 13 ).…”

“…Similar to animals, sensory pleasure in humans appears to be modulated by opioidergic activity ( 19 ). However, whereas some studies do find that the magnitude of the experienced sensory pleasure correlates with the activity of the ventral striatum ( 20, 21 ), sensory pleasure has been most consistently reported to correlate with the activity of the medial orbitofrontal cortex (mOFC) rather than the ventral striatum ( 22–24 ).…”