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

Abstract

Multiple signals for reward-hedonic impact, motivation, and learned associative prediction-are funneled through brain mesocorticolimbic circuits involving the nucleus accumbens and ventral pallidum. Here, we show how the hedonic "liking" and motivation "wanting" signals for a sweet reward are distinctly modulated and tracked in this circuit separately from signals for Pavlovian predictions (learning). Animals first learned to associate a fixed sequence of Pavlovian cues with sucrose reward. Subsequent intraaccumbens microinjections of an opioid-stimulating drug increased the hedonic liking impact of sucrose in behavior and firing signals of ventral pallidum neurons, and likewise, they increased incentive salience signals in firing to the reward-proximal incentive cue (but did not alter firing signals to the learned prediction value of a reward-distal cue). Microinjection of a dopamine-stimulating drug instead enhanced only the motivation component but did not alter hedonic impact or learned prediction signals. Different dedicated neuronal subpopulations in the ventral pallidum tracked signal enhancements for hedonic impact vs. incentive salience, and a faster firing pattern also distinguished incentive signals from slower hedonic signals, even for a third overlapping population. These results reveal separate neural representations of wanting, liking, and prediction components of the same reward within the nucleus accumbens to ventral pallidum segment of mesocorticolimbic circuitry.addiction | obesity | limbic | reinforcement | striatum

Reversible online control of habitual behavior by optogenetic perturbation of medial prefrontal cortex

“…Our experiments do not settle how this coordination is accomplished or whether it is accomplished exclusively online. Still, our anatomical evidence from using the viral vector to trace the connections from the IL-injection sites confirmed that this region did not have detectable direct connections with the sensorimotor striatum but, rather, with regions (10) that should give the IL cortex direct access to circuits involved in flexibility and reinforcement as well as addiction (e.g., via projections to prelimbic neocortex and to the medial and ventral striatum) (3,4,6,7,15,23,25,26), and also to habit-promoting circuits through the central amygdala (27). Each could be important for the IL habit-toggling function.…”

“…There is usually a close coupling of reward-proximal stimuli and actions to current value (7,21,24,25); the fact that the rats drank the devalued reward after this late manipulation of IL suggests that the reward might no longer have been aversive. However, this interpretation must face three issues.…”

Depletion of nucleus accumbens dopamine leads to impaired reward and aversion processing in mice: Relevance to motivation pathologies

“…Such findings demonstrate that NAcc DA regulates the motivation for ("wanting") sweet-tasting stimuli (Nunes et al, 2013). In contrast, NAcc DA does not regulate appetite for homeostatic dietary need (Cousins and Salamone, 1994) or hedonic responding to ("liking") sweet stimuli (Smith et al, 2011). There is also interest in DA regulation of the motivation required under cognitively effortful conditions.…”

Orexin in Rostral Hotspot of Nucleus Accumbens Enhances Sucrose ‘Liking’ and Intake but Scopolamine in Caudal Shell Shifts ‘Liking’ Toward ‘Disgust’ and ‘Fear’

“…Conversely, in caudal shell, agonist microinjections reveal a 'hedonic coldspot', where opioid stimulation suppresses sucrose hedonic impact (Castro and Berridge, 2014;Pecina and Berridge, 2005). By contrast to the localized hotspot for sweetness 'liking', mu-opioid stimulations increase motivation to eat much more widely and homogeneously throughout the entire NAc shell (and in related structures), measured as increases in cue-triggered 'wanting' to obtain food rewards (eg, in instrumental breakpoint and pavlovian-instrumental transfer tests), as well as in food consumption (Castro and Berridge, 2014;Covelo et al, 2014;Maldonado-Irizarry et al, 1995;Pecina and Berridge, 2005;Pecina and Berridge, 2013;Smith and Berridge, 2005;Smith et al, 2011;Zhang and Kelley, 2000).…”