Separate brain regions code for salience vs. valence during reward prediction in humans

Abstract

Predicting rewards and avoiding aversive conditions is essential for survival. Recent studies using computational models of reward prediction implicate the ventral striatum in appetitive rewards. Whether the same system mediates an organism's response to aversive conditions is unclear. We examined the question using fMRI blood oxygen level-dependent measurements while healthy volunteers were conditioned using appetitive and aversive stimuli. The temporal difference learning algorithm was used to estimate reward prediction error. Activations in the ventral striatum were robustly correlated with prediction error, regardless of the valence of the stimuli, suggesting that the ventral striatum processes salience prediction error. In contrast, the orbitofrontal cortex and anterior insula coded for the differential valence of appetitive/aversive stimuli. Given its location at the interface of limbic and motor regions, the ventral striatum may be critical in learning about motivationally salient stimuli, regardless of valence, and using that information to bias selection of actions.

A common neural scale for the subjective pleasantness of different primary rewards

“…However, in Investigation 2 the common neural activations in the ventral striatum did not scale linearly with the subjective A C C E P T E D M A N U S C R I P T ACCEPTED MANUSCRIPT 22 pleasantness of both rewards. This is consistent with studies showing that some regions of the striatum encode the salience of monetary rewards (Zink et al, 2004) and respond to both pleasant and unpleasant salient stimuli (Jensen et al, 2007;Seymour et al, 2004).…”

Valence and salience contribute to nucleus accumbens activation

“…Independently manipulating these two factors allowed us to separately examine each factor's influence on NAcc activation. Earlier studies that have focused on valence, using monetary incentives or aversive shock, have not independently varied salience (Abler et al, 2006;Breiter et al, 2001;Jensen et al, 2007;Knutson et al, 2001;Tobler et al, 2007;Tom et al, 2007), while studies that have varied salience have not independently varied valence across gains and losses (Bjork and Hommer, 2006;Jensen et al, 2003;Tricomi et al, 2004;Zink et al, 2006).…”

“…The salience account references evidence that NAcc activation increases with behavioral demands or interference (Tricomi et al, 2004;Zink et al, 2004;Zink et al, 2006), in response to novel nonrewarded events (Zink et al, 2003), or in anticipation of painful stimulation (Berridge and Robinson, 1998;Jensen et al, 2003). At least two studies have reported NAcc activation correlated with salience prediction error models of conditioning for painful stimuli that included decreases during unpredicted avoidance of painful stimuli (Jensen et al, 2007;Seymour et al, 2004). The salience account, like the valence account, pertains primarily to anticipation.…”

The Formation of Abnormal Associations in Schizophrenia: Neural and Behavioral Evidence

“…The ventral striatum plays a central role in reward processing and it has been suggested that activations of the ventral striatum normally mediate the incentive or motivational salience of environmental stimuli (Jensen et al, 2003(Jensen et al, , 2007Zink et al, 2003Zink et al, , 2004Zink et al, , 2006. The stronger responses to the neutral stimulus among patients may reflect an aberrant attribution of motivational salience to neutral stimuli (Kapur, 2003).…”

“…Several recent studies in normal volunteers have shown a significant role of the ventral striatum in the learning of associationsFboth appetitive as well as aversive (eg Jensen et al, 2007;McClure et al, 2003;O'Doherty et al, 2003O'Doherty et al, , 2004. These studies show that as associations are learnt, structures that are initially activated by unconditioned stimuli, come to respond to neutral stimuli as a function of their repeated pairings.…”