Mapping excessive "disgust" in the brain: Ventral pallidum inactivation recruits distributed circuitry to make sweetness "disgusting".

Abstract

The ventral pallidum (VP) is an important structure in processing reward. The VP may be the only brain structure where localized lesions in rats replace normal facial "liking" expressions to sweetness with excessive "disgust" reactions, such as gapes and chin rubs, that are normally reserved for unpalatable tastes. The posterior half of the VP (pVP) contains a hedonic hot spot where opioid or related neurochemical stimulations can amplify positive "liking" reactions to sweet taste. This is the same site where lesions or pharmacological inactivations replace positive hedonic reactions to sucrose with intense negative "disgust." In the present study, we aimed to identify brain networks recruited by pVP inactivation to generate excessive "disgust," using neuronal Fos expression as a marker of neurobiological activation. Microinjections in pVP of inhibitory GABAA/B agonists (muscimol and baclofen) caused rats to exhibit excessive "disgust" reactions to sucrose. Excessive "disgust" was accompanied by recruitment of neural Fos activation in several subcortical structures, including the posterior medial shell of nucleus accumbens (which also contains another GABAergic "disgust"-inducing "hedonic cold spot"), the bed nucleus of stria terminalis, lateral habenula, hypothalamus, and midbrain ventral tegmentum. Fos suppression was found in cortical limbic regions, including previously identified hedonic hot spots in the anteromedial orbitofrontal cortex and posterior insula. Finally, in addition to inducing excessive "disgust," pVP inactivation abolished motivational "wanting" to eat palatable food, reduced positive social interactions, and reordered sensorimotor relations. Our findings identify potential "disgust" generators in the brain that are released into excitation by pVP inhibition and may serve as targets for future research.