Excessive disgust caused by brain lesions or temporary inactivations: mapping hotspots of the nucleus accumbens and ventral pallidum

Abstract

Disgust is a prototypical type of negative affect. In animal models of excessive disgust, only a few brain sites are known in which localized dysfunction (lesions or neural inactivations) can induce intense ‘disgust reactions’ (e.g., gapes) to a normally pleasant sensation such as sweetness. Here we aimed to map forebrain candidates more precisely to identify where either local neuronal damage (excitotoxin lesions) or local pharmacological inactivation (muscimol-baclofen microinjections) caused rats to emit excessive sensory disgust reactions to sucrose. Our study compared subregions of nucleus accumbens shell, ventral pallidum, lateral hypothalamus and adjacent extended amygdala. Results indicated the posterior half of ventral pallidum to be the only forebrain site where intense sensory disgust gapes to sucrose were induced by both lesions and temporary inactivations (this site was previously identified as a hedonic hotspot for enhancements of sweetness ‘liking’). By comparison, for the nucleus accumbens, temporary GABA inactivations in the caudal half of the medial shell also generated sensory disgust but lesions never did at any site. Further, even inactivations failed to induce disgust in the rostral half of accumbens shell (which also contains a hedonic hotspot). In other structures, neither lesions nor inactivations induced disgust as long as the posterior ventral pallidum remained spared. We conclude that the posterior ventral pallidum is an especially crucial hotspot for producing excessive sensory disgust by local pharmacological/lesion dysfunction. By comparison, the nucleus accumbens appears to segregate sites for pharmacological disgust induction and hedonic enhancement into separate posterior versus rostral halves of medial shell.

Dynamic Changes in Amygdala Psychophysiological Connectivity Reveal Distinct Neural Networks for Facial Expressions of Basic Emotions

“…Amygdala enhanced connection with the olfactory (pyriform) cortex is clearly coherent with the ancestral origin of disgust that is anchored on chemical senses, and fits well with behavioural evidence that recognition of disgusted faces is improved by the presentation of an olfactory stimulus irrespective of its emotional valence90. Amygdala integration with the NAc and ventral pallidum (VP) finds direct support in rodent studies on disgust, showing that lesions and temporary inactivation of either structures generate intense sensory disgust91. The thalamus has been found to respond selectively to disgust in meta-analyses310 or to images of rotten food and mutilation92, whereas MVPA found that voxels within the thalamus, especially the ventral anterior nuclei, are particularly accurate in classifying disgust movies clips6.…”

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

“…Scopolamine microinjections throughout nearly the entire NAc medial shell also doubled the number of 'disgust' reactions elicited by bitter quinine. However, scopolamine's induction of negative affect was never strong enough to actually create 'disgust' reactions to the sweet taste of sucrose (unlike GABA stimulations in caudal shell, which can reverse sucrose reactions from 'liking' to 'disgust' (Faure et al, 2010;Ho and Berridge, 2014;Reynolds and Berridge, 2002)). Finally, ACh blockade by scopolamine specifically in the caudal half of medial shell additionally elicited fear-related defensive treading behavior, which was directed toward locations in the chamber that may have been perceived as more threatening than others (eg, light-reflecting corners).…”

Liking, wanting, and the incentive-sensitization theory of addiction.

“…S. Smith & Berridge, 2007). In addition to enhancing ‘liking’ for intense pleasure, this ventral pallidal hotspot is the only known site in the brain where a small lesion conversely also eliminates normal pleasure, and reverses the hedonic impact of sweet sensation from ‘liked’ to instead ‘disgusting’ (so that afterwards sucrose elicits bitterness-typical gapes and related negative expressions) (Berridge & Kringelbach, 2015; Ho & Berridge, 2014). …”