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Review
. 2010 Sep 2:1350:43-64.
doi: 10.1016/j.brainres.2010.04.003. Epub 2010 Apr 11.

The tempted brain eats: pleasure and desire circuits in obesity and eating disorders

Kent C Berridge  1 , Chao-Yi Ho, Jocelyn M Richard, Alexandra G DiFeliceantonio
Affiliations
Review

The tempted brain eats: pleasure and desire circuits in obesity and eating disorders

Kent C Berridge et al. Brain Res. .

Abstract

What we eat, when and how much, all are influenced by brain reward mechanisms that generate "liking" and "wanting" for foods. As a corollary, dysfunction in reward circuits might contribute to the recent rise of obesity and eating disorders. Here we assess brain mechanisms known to generate "liking" and "wanting" for foods and evaluate their interaction with regulatory mechanisms of hunger and satiety, relevant to clinical issues. "Liking" mechanisms include hedonic circuits that connect together cubic-millimeter hotspots in forebrain limbic structures such as nucleus accumbens and ventral pallidum (where opioid/endocannabinoid/orexin signals can amplify sensory pleasure). "Wanting" mechanisms include larger opioid networks in nucleus accumbens, striatum, and amygdala that extend beyond the hedonic hotspots, as well as mesolimbic dopamine systems, and corticolimbic glutamate signals that interact with those systems. We focus on ways in which these brain reward circuits might participate in obesity or in eating disorders.

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Figures

Figure 1
Figure 1
Model of incentive motivation that separates reward ‘wanting’ (incentive salience) from ‘liking’ (hedonic impact of sensory pleasure). This model of incentive salience was originally proposed by Robinson and Berridge (1993), derived from incentive motivation concepts of Toates (1986) and Bindra (1978), and was recently translated into computational form by Zhang et al. (2009). Normal hunger acts as a physiological ’drive’ signal to magnify the incentive’ wanting’ and hedonic ‘liking’ triggered by tasty foods and their associated cues, whereas satiety dampens the multiplicative impact of cues and foods. Relevant to obesity, individuals with endogenously reactivity higher in mesolimbic circuits would have higher incentive salience for foods, and possibly higher hedonic impact, leading to greater ‘wanting’ and-or ‘liking’ to eat, in ways that would promote obesity.
Figure 2
Figure 2. ‘Wanting’ enhancements caused by hypothalamic stimulation or by dopamine elevation
Electrical stimulation of the lateral hypothalamus makes rats eat triple the amount they ordinarily consume (left). Elevation of extra-synaptic dopamine by knockdown of the gene that codes the dopamine transporter makes mutant mice run more eagerly to obtain a sweet Frootloop treat than their control wild-type counterparts (both shown in photo; right). Modified from Berridge and Valenstein (1991) and from Pecina et al. (2003).
Figure 3
Figure 3. ‘Liking’ for sweetness is never enhanced by hypothalamic electrodes or by dopamine elevation
Turning on stimulation of lateral hypothalamic electrodes in the same rats as in Figure 4 causes more ‘disliking’ reactions (e.g., gapes) to sucrose, while not altering positive ‘liking’ reactions (e.g., lip licks), even though the stimulation made the same rats avidly eat more food. Elevation of dopamine in mutant mice only suppresses positive ‘liking’ reactions to sucrose at the highest concentration (while not altering lower ‘liking’ for dilute sucrose solution; aversive reactions were not observed and are not shown), even though the mutants ‘wanted’ sweet rewards more than control wild-type mice. Modified from Berridge and Valenstein (1991) and from Pecina et al. (2003).
Figure 4
Figure 4. Hedonic hotspots and hedonic circuits
Hedonic hotspots are shown in nucleus accumbens, ventral pallidum, and brainstem parabrachial nucleus where opioid or other signals cause amplification of core ‘liking’ reactions to sweetness. Reprinted by permission from (Smith et al., 2010), based on (Kringelbach, 2005; Peciña et al., 2006; Smith and Berridge, 2007).
Figure 5
Figure 5. Taste ‘liking’ reactions and detail map of nucleus accumbens hotspot
Positive ‘liking’ reactions to sweet tastes or aversive ‘disliking’ reactions to bitter tastes are homologous in human newborn, young orangutan, and adult rat (left). Opioid hotspots and coldspots in the nucleus accumbens (medial shell shown in sagittal view; center). Green: the entire medial shell supports opioid-stimulated increases in ‘wanting’ to eat food after microinjections of opioid agonist DAMGO. Red: only a cubic-millimeter sized hedonic hotspot also generates increases in ‘liking’ for sweetness. Blue: in a small hedonic ‘coldspot’ opioid stimulation suppresses ‘liking’ reactions to sucrose, and in a larger purple zone suppresses ‘disliking’ reactions to quinine, all while still stimulating intake. Fluorescent Fos plume to DAMGO microinjection (right). Reprinted by permission from (Smith et al., 2010), based on data from (Peciña and Berridge, 2005).
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