Ventral Pallidum Firing Codes Hedonic Reward: When a Bad Taste Turns Good

Abstract

The ventral pallidum (VP) is a key structure in brain mesocorticolimbic reward circuits that mediate "liking" reactions to sensory pleasures. Do firing patterns in VP actually code sensory pleasure? Strong evidence for hedonic coding requires showing that neural signals track positive increases in sensory pleasure or even reversals from bad to good. A useful test is the salt alliesthesia of physiological sodium depletion that makes even aversively intense NaCl taste become palatable and "liked." We compared VP neural firing activity in rats during aversive "disliking" reactions elicited by a noxiously intense NaCl taste (triple-seawater 1.5 M concentration) in normal homeostatic state versus in a physiological salt appetite state that made the same NaCl taste palatable and elicit positive "liking" reactions. We also compared firing elicited by palatable sucrose taste, which always elicited "liking" reactions in both states. A dramatic doubling in the amplitude of VP neural firing peaks to NaCl was caused by salt appetite that matched the affective switch from aversive ("disliking") to positive hedonic ("liking") reactions. By contrast, VP neural activity to "liked" sucrose taste was always high and never altered. In summary, VP firing activity selectively tracks the hedonic values of tastes, even across hedonic reversals caused by physiological changes. Our data provide the strongest evidence yet for neural hedonic coding of natural sensory pleasures and suggest, by extension, how abnormalities in VP firing patterns might contribute to clinical hedonic dysfunctions.

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

“…When CS+1 and CS+2 are separated by several seconds, a gradual rise in incentive salience begins soon after the CS+1 onset, motivating anticipatory behavioral approach (e.g., head entries into a sucrose dish) which reaches maximum levels around the moment of CS+2 presentation and just before the UCS (48,49). The final event in the sequence, the UCS sucrose infusion (i.e., the reward), carried the strongest hedonic impact, which was confirmed by taste reactivity results (45). Separately from this CS+1 → CS+2 → UCS trial sequence, a distinct CS− tone was randomly interleaved during the session as a control stimulus that predicted nothing and thus, carried little predictive, motivation, or hedonic value.…”

“…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.…”

The Reward Circuit: Linking Primate Anatomy and Human Imaging

“…It, like the VS, is an area of focus in the study of addictive behaviors (Mitrovic and Napier, 2002;Smith and Berridge, 2007;Tindell et al, 2006). The term VP was first used to describe, in rats, the forebrain region below the anterior commissure, extending into the anterior perforated space that contained pallidal-like cells.…”

Affective neuroscience of pleasure: reward in humans and animals

“…Also, converging evidence comes from studies of the neuronal coding of natural pleasure enhancements within hedonic hotspots Kringelbach 2005). For example, salt appetite induced by physiological sodium depletion causes sudden 'liking' of an intensely salty taste that is normally 'disliked' (triple seawater NaCl concentration) and simultaneously makes neurons in the ventral pallidum hotspot fire as vigorously to the salty taste as they do to sweetness (but do not similarly fire to 'disliked' salt or other stimuli; Aldridge and Berridge 2008;Tindell et al 2006;Wheeler and Carelli 2006). Such observations tend to support the idea that when drugs in limbic hotspots enhance 'liking' reactions, the experiment has tapped into the affective generation of pleasure.…”

“…This might be explained if tonic dopamine facilitates phasic nondopamine signal processing that mediates learning in downstream limbic structures. For example, a dose of amphetamine that elevates tonic dopamine actually amplifies the neural encoding of phasic 100-ms learned reward cue-triggered signals in the ventral pallidum (which probably reach ventral pallidum via nondopamine afferent projections) that convey learned information about future reward (Tindell et al 2006). Similarly, tonic dopamine elevation by amphetamine elevates behavioral performance triggered by reward cues or directed toward obtaining them (in ways that are too specific to the learned motivating value of cues to be explained by tonic activation or general response strengthening effects of a drug; Cardinal et al 2002;Everitt et al 2001;Everitt et al 1999;Wyvell and Berridge 2001).…”