Dynamic Computation of Incentive Salience: “Wanting” What Was Never “Liked”

Abstract

Pavlovian cues for rewards become endowed with incentive salience, guiding "wanting" to their learned reward. Usually, cues are "wanted" only if their rewards have ever been "liked," but here we show that mesocorticolimbic systems can recompute "wanting" de novo by integrating novel physiological signals with a cue's preexisting associations to an outcome that lacked hedonic value. That is, a cue's incentive salience can be recomputed adaptively. We demonstrate that this recomputation is encoded in neural signals coursing through the ventral pallidum. Ventral pallidum neurons do not ordinarily fire vigorously to a cue that predicts the previously "disliked" taste of intense salt, although they do fire to a cue that predicts the taste of previously "liked" sucrose. Yet we show that neural firing rises dramatically to the salt cue immediately and selectively when that cue is encountered in a never-before-experienced state of physiological salt depletion. Crucially, robust neural firing to the salt cue occurred the first time it was encountered in the new depletion state (in cue-only extinction trials), even before its associated intense saltiness has ever been tasted as positively "liked" (salt taste had always been "disliked" before). The amplification of incentive salience did not require additional learning about the cue or the newly positive salt taste. Thus dynamic recomputation of cue-triggered "wanting" signals can occur in real time at the moment of cue re-encounter by combining previously learned Pavlovian associations with novel physiological information about a current state of specific appetite.

An Orexin Hotspot in Ventral Pallidum Amplifies Hedonic ‘Liking’ for Sweetness

“…Our results indicate that the VP reward circuit also is influenced by LH regulatory circuits. That is consistent with previous findings mentioned above, and with VP modulation of neuronal firing to tastes and their associated cues related to a type of alliesthesia (sodium appetite) (Tindell et al, 2006;Tindell et al, 2009). Conceivably, such modulation may occur also for caloric foods that activate the VP (Beaver et al, 2006;Stoeckel et al, 2008).…”

Measuring wanting and liking from animals to humans: A systematic review

“…Neither the cue nor the physiological state is by itself sufficient to trigger wanting: the synergetic combination of these two elements is critical. An individual in a particular physiological state will not show any wanting behavior if he or she does not encounter a cue, and a cue will not elicit wanting behavior if the associated reward is not relevant for the physiological state of the individual (Robinson and Berridge, 2013;Tindell et al, 2009;Wyvell and Berridge, 2000;Zhang et al, 2009). Therefore, all the procedures that did not measure wanting during or after the perception of a real or vividly imagined cue are unlikely to truly reflect the specific influence of wanting.…”

Disentangling pleasure from incentive salience and learning signals in brain reward circuitry

“…Presentation of cues for food, sex, drugs, or money to humans can evoke an increase in VP blood oxygen level dependence (BOLD) signals (14,18,19,61), and in rodents, robust firing in VP neurons is evoked by cues for sensory rewards (46,62). It has usually been difficult to determine which component of Pavlovian reward (prediction, incentive salience, or hedonic impact) is represented by a neural activation in VP and larger circuitry, because all these reward components covary together in most cases.…”

“…Second, even for VP neurons that represented combined wanting and liking enhancements, CS+2 effects were potentially distinguishable by a faster-latency rise in activation than sucrose UCS effects. These population and temporal firing mechanisms would allow liking, wanting, and prediction signals to be told apart within ventral striatopallidal circuits during natural appetite, drug intoxication or withdrawal, or stress states known to elevate reward measures (1,2,4,22,25,27,30,31,46,76). We suggest that these VP neuronal signals for reward components could be related to reports of activity in human posterior VP positively correlated with pleasant food images (17) and mechanisms by which opioid and related stimulation in a VP hotspot can modulate the hedonic impact of sensory rewards (33,36,77).…”

“…Firing patterns of neurons within the VP encode Pavlovian conditioned stimulus (CS) features, such as prediction and incentive salience, and unconditioned stimulus (UCS) reward features, such as hedonic impact (45,46). Problematically, however, it has never been clear how NAc-VP circuitry could distinguish various reward signals from each other.…”