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Kelley AE, Baldo BA, Pratt WE, Will MJ. Corticostriatal-hypothalamic circuitry and food motivation: Integration of energy, action and reward. Physiol Behav 86: 773-795

Department of Psychiatry, University of Wisconsin-Madison Medical School, 6001 Research Park Blvd., Madison, WI 53719, USA.
Physiology & Behavior (Impact Factor: 2.98). 01/2006; 86(5):773-95. DOI: 10.1016/j.physbeh.2005.08.066
Source: PubMed

ABSTRACT

Work over the past decade has supported the idea that discrete aspects of appetitive motivation are differentially mediated by separate but interacting neurochemical systems within the nucleus accumbens (Acb). We review herein a series of studies in rats comparing the effects of manipulating Acb amino acid, opioid, acetylcholine, and dopamine systems on tests of free-feeding and food-reinforced operant responding. Results from our laboratory and in the literature support three general conclusions: (1) GABA output neurons localized exclusively within the Acb shell directly influence hypothalamic effector mechanisms for feeding motor patterns, but do not participate in the execution of more complex food-seeking strategies; (2) enkephalinergic neurons distributed throughout the Acb and caudate-putamen mediate the hedonic impact of palatable (high sugar/fat) foods, and these neurons are under modulatory control by striatal cholinergic interneurons; and (3) dopamine transmission in the Acb governs general motoric and arousal processes related to response selection and invigoration, as well as motor learning-related plasticity. These dissociations may reflect the manner in which these neurochemical systems differentially access pallido-thalamo-cortical loops reaching the voluntary motor system (in the case of opioids and dopamine), versus more restricted efferent connections to hypothalamic motor/autonomic control columns (in the case of Acb shell GABA and glutamate systems). Moreover, we hypothesize that while these systems work in tandem to coordinate the anticipatory and consummatory phases of feeding with hypothalamic energy-sensing substrates, the striatal opioid network evolved a specialized capacity to promote overeating of energy-dense foods beyond acute homeostatic needs, to ensure an energy reserve for potential future famine.

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    • "Consistent with these pharmacological studies, unit recordings in freely feeding rats have identified subpopulations of NAcSh neurons that reduce their activity during feeding (Krause et al., 2010; Roitman et al., 2010; Tellez et al., 2012) and that shift to increased firing when animals are presented with aversive conditioned food (Roitman et al., 2010). From these studies, a model has been proposed in which inhibitory projections from the NAcSh to the LH serve as a sensory sentinel, allowing rapid control over food consumption in response to motivational or sensory signals (Baldo and Kelley, 2007; Kelley et al., 2005b). However, this circuit has not been resolved at the cellular level and its temporal dynamics have not been characterized. "
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    ABSTRACT: Feeding satisfies metabolic need but is also controlled by external stimuli, like palatability or predator threat. Nucleus accumbens shell (NAcSh) projections to the lateral hypothalamus (LH) are implicated in mediating such feeding control, but the neurons involved and their mechanism of action remain elusive. We show that dopamine D1R-expressing NAcSh neurons (D1R-MSNs) provide the dominant source of accumbal inhibition to LH and provide rapid control over feeding via LH GABA neurons. In freely feeding mice, D1R-MSN activity reduced during consumption, while their optogenetic inhibition prolonged feeding, even in the face of distracting stimuli. Conversely, activation of D1R-MSN terminals in LH was sufficient to abruptly stop ongoing consumption, even during hunger. Direct inhibition of LH GABA neurons, which received input from D1R-MSNs, fully recapitulated these findings. Together, our study resolves a feeding circuit that overrides immediate metabolic need to allow rapid consumption control in response to changing external stimuli.
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    • "Rather, the affective reactions reflect the palatability of tastes, i.e., whether the taste is 'liked' or 'disliked'. The ventral pallidum (VP) is the chief target of the nucleus accumbens and integrates and processes reward information flowing through the mesocorticolimbic system [29] [33] [46] [58] [61] [66]. VP projections additionally target preoptic regions of the lateral hypothalamus, the mediodorsal nucleus of the thalamus, and in turn connect to larger limbic cortico-striatopallidalthalamocortical loops, and to additional basal ganglia and brainstem nuclei such as the subthalamic nucleus, substantia nigra, and pedunculopontine nucleus [11] [23] [32]. "
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    ABSTRACT: The hedonic value of a sweet food reward, or how much a taste is 'liked', has been suggested to be encoded by neuronal firing in the posterior ventral pallidum (VP). Hedonic impact can be altered by psychological manipulations, such as taste aversion conditioning, which can make an initially pleasant sweet taste become perceived as disgusting. Pairing nausea-inducing LiCl injection as a Pavlovian unconditioned stimulus (UCS) with a novel taste that is normally palatable as the predictive conditioned stimulus (CS+) suffices to induce a learned taste aversion that changes orofacial 'liking' responses to that sweet taste (e.g., lateral tongue protrusions) to 'disgust' reactions (e.g., gapes) in rats. We used two different sweet tastes of similar initial palatability (a sucrose solution and a polycose/saccharin solution, CS± assignment was counterbalanced across groups) to produce a discriminative conditioned aversion. Only one of those tastes (arbitrarily assigned and designated as CS+) was associatively paired with LiCl injections as UCS to form a conditioned aversion. The other taste (CS-) was paired with mere vehicle injections to remain relatively palatable as a control sweet taste. We recorded the neural activity in VP in response to each taste, before and after aversion training. We found that the safe and positively hedonic taste always elicited excitatory increases in firing rate of VP neurons. By contrast, aversion learning reversed the VP response to the 'disgusting' CS+ taste from initial excitation into a conditioned decrease in neuronal firing rate after training. Such neuronal coding of hedonic impact by VP circuitry may contribute both to normal pleasure and disgust, and disruptions of VP coding could result in affective disorders, addictions and eating disorders.
    No preview · Article · Nov 2015 · Behavioural brain research
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    • "For example, it has already been shown that CeA activity is required to observe feeding driven by an energy deficit (24-hr food deprivation) (Baldo, Alsene, Negron, & Kelley, 2005; Minano, Meneres Sancho, Sancibrian, Salinas, & Myers, 1992). Furthermore, inactivation of the CeA, but not the BLA, blocks intra-Acb muscimolinduced feeding (Baldo et al., 2005), a pharmacological model that parallels the motivational state induced by energy deficit (i.e., food restriction; see Kelley et al., 2005, for review). "

    Full-text · Dataset · Aug 2015
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