Distinct opioid circuits determine the palatability and the desirability of rewarding events

Wassum, Kate M.; Ostlund, Sean B.; Maidment, Nigel T.; Balleine, Bernard W.

doi:10.1073/pnas.0905874106

Cited by 155 publications

(179 citation statements)

References 40 publications

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“…Doses were selected based on their ability to alter reward seeking when infused into the NAc, without causing gross motor impairments (Nadal et al, 1998;Nunes et al, 2013;Pratt and Kelley, 2004). Drugs were infused, as described previously (Wassum et al, 2009), into the NAc in a volume of 0.5 μl over 1 min via an injector inserted into the guide cannula fabricated to protrude 1 mm ventral to the cannula tip, using a microinfusion pump. For Experiment 2, rats were unilaterally infused with either mecamylamine (10 μg/side), scopolamine (10 μg/side), or an equivalent volume (0.5 μl/ side) of ACSF via the cannula attached to the carbon-fiber microelectrode.…”

Section: Drugs and Infusion Proceduresmentioning

confidence: 99%

Nucleus Accumbens Acetylcholine Receptors Modulate Dopamine and Motivation

Collins¹,

Aitken²,

Greenfield³

et al. 2016

Neuropsychopharmacol

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Environmental reward-predictive cues can motivate reward-seeking behaviors. Although this influence is normally adaptive, it can become maladaptive in disordered states, such as addiction. Dopamine release in the nucleus accumbens core (NAc) is known to mediate the motivational impact of reward-predictive cues, but little is known about how other neuromodulatory systems contribute to cue-motivated behavior. Here, we examined the role of the NAc cholinergic receptor system in cue-motivated behavior using a Pavlovian-to-instrumental transfer task designed to assess the motivating influence of a reward-predictive cue over an independently-trained instrumental action. Disruption of NAc muscarinic acetylcholine receptor activity attenuated, whereas blockade of nicotinic receptors augmented cue-induced invigoration of reward seeking. We next examined a potential dopaminergic mechanism for this behavioral effect by combining fast-scan cyclic voltammetry with local pharmacological acetylcholine receptor manipulation. The data show evidence of opposing modulation of cue-evoked dopamine release, with muscarinic and nicotinic receptor antagonists causing suppression and augmentation, respectively, consistent with the behavioral effects of these manipulations. In addition to demonstrating cholinergic modulation of naturally-evoked and behaviorally-relevant dopamine signaling, these data suggest that NAc cholinergic receptors may gate the expression of cue-motivated behavior through modulation of phasic dopamine release.

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Section: Drugs and Infusion Proceduresmentioning

confidence: 99%

Nucleus Accumbens Acetylcholine Receptors Modulate Dopamine and Motivation

Collins¹,

Aitken²,

Greenfield³

et al. 2016

Neuropsychopharmacol

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“…It is well acknowledged today that the dopamine and opioid systems play an important role in the modulation of feeding behaviour, although they are involved in different steps of this process. These two systems, which are important for the 'reward circuit' and play a major role in food pleasure and selection, have been relatively well characterized in humans and rats (Berridge, 2000;Kelley et al, 2002;Barbano and Cador, 2007;Barbano et al, 2009;Wassum et al, 2009) but not yet in pigs.…”

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confidence: 99%

Food preferences and aversions in human health and nutrition: how can pigs help the biomedical research?

Clouard

Meunier-Salaün

Val‐Laillet

2012

Animal

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The establishment of food preferences and aversions determines the modulation of eating behaviour and the optimization of food intake. These phenomena rely on the learning and memory abilities of the organism and depend on different psychobiological mechanisms such as associative conditionings and sociocultural influences. After summarizing the various behavioural and environmental determinants of the establishment of food preferences and aversions, this paper describes several issues encountered in human nutrition when preferences and aversions become detrimental to health: development of eating disorders and obesity, aversions and anorexia in chemotherapy-treated or elderly patients and poor palatability of medical substances and drugs. Most of the relevant biomedical research has been performed in rodent models, although this approach has severe limitations, especially in the nutritional field. Consequently, the final aim of this paper is to discuss the use of the pig model to investigate the behavioural and neurophysiological mechanisms underlying the establishment of food preferences and aversions by reviewing the literature supporting analogies at multiple levels (general physiology and anatomy, sensory sensitivity, digestive function, cognitive abilities, brain features) between pigs and humans.Keywords: pig, conditioned learning, eating behaviour, animal model, biomedical applications ImplicationsInvestigation of the behavioural and neurophysiological mechanisms of the establishment of food preferences and aversions can lead to important developments in the context of human nutrition and health. Because the rodent models are not always adequate in this field, there is a need to develop alternative experimental models. Pigs have numerous similarities with humans in terms of the physiology, anatomy, sensory sensitivity, cognitive abilities and brain functions. The aim of this paper is to promote the use of pigs for biomedical research in human nutrition. IntroductionFeeding is a complex behaviour, which can be described as 'the research and consumption of food and drink to maintain vital functions ' (Bellisle, 1999) and to 'fulfil the metabolic needs of the organism ' (Ferreira, 2004). Today, it is also well acknowledged that a high proportion of human food consumption in developed countries appears to be driven by pleasure (for a review, see Lowe and Butryn, 2007) and sociocultural influences. Food consumption is also involved in fundamental metabolic homeostasis regulation, as it controls the supply of energy and nutrients in the organism (Bellisle, 1999). According to Ferreira (2004), feeding behaviour implies that animals learn to consume high-energy foods and to avoid toxic foods. Establishment of food selection implies that, during its first experience with food, the organism memorizes the sensorial characteristics of the food (e.g. taste, odour, texture and visual cues) and the postingestive consequences of its ingestion, and associates these food characteristics with these consequences (Garcia et ...

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“…Once thought of mainly as a limbic motor translation zone (13), it is now clear that the VP as well as the NAc controls reward motivation and hedonics (1,3,6,(31)(32)(33)(34). Both structures contain subregional hotspots where μ-opioid agonist microinjections induce a doubling of the hedonic impact or palatability of a sweet taste of sucrose (35,36).…”

mentioning

confidence: 99%

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

Smith

Berridge

Aldridge

2011

Proc. Natl. Acad. Sci. U.S.A.

343

328

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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

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Distinct opioid circuits determine the palatability and the desirability of rewarding events

Cited by 155 publications

References 40 publications

Nucleus Accumbens Acetylcholine Receptors Modulate Dopamine and Motivation

Nucleus Accumbens Acetylcholine Receptors Modulate Dopamine and Motivation

Food preferences and aversions in human health and nutrition: how can pigs help the biomedical research?

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

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