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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Available from: Matthew J Will, Sep 29, 2015
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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). "
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    • "To relate the behavioral studies to neural activity, we recorded the responses to DEP20 in the NAc shell, a brain region involved in reward, feeding, and motor activity (Brown et al. 2011; Kelley et al. 2005; Li et al. 2012 "
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    ABSTRACT: Obesity is a worldwide health problem that has reached epidemic proportions. To ameliorate this problem, one approach is the use of appetite suppressants. These compounds are frequently amphetamine congeners such as diethylpropion (DEP), phentermine (PHEN), and bupropion (BUP), whose effects are mediated through serotonin, norepinephrine, and dopaminergic pathways. The nucleus accumbens (NAc) shell receives dopaminergic inputs and is involved in feeding and motor activity. However, little is known about how appetite suppressants modulate its activity. Therefore, we characterized behavioral and neuronal NAc shell responses to short-term treatments of DEP, PHEN, and BUP. These compounds caused a transient decrease in weight and food intake while increasing locomotion, stereotypy, and insomnia. They evoked a large inhibitory imbalance in NAc shell spiking activity that correlated with the onset of locomotion and stereotypy. Analysis of the local field potentials (LFPs) showed that all three drugs modulated beta, theta, and delta oscillations. These oscillations do not reflect an aversive-malaise brain state, as ascertained from taste aversion experiments, but tracked both the initial decrease in weight and food intake and the subsequent tolerance to these drugs. Importantly, the appetite suppressant-induced weight loss and locomotion were markedly reduced by intragastric (and intra-NAc shell) infusions of dopamine antagonists SCH-23390 (D1 receptor) or raclopride (D2 receptor). Furthermore, both antagonists attenuated appetite suppressant-induced LFP oscillations and partially restored the imbalance in NAc shell activity. These data reveal that appetite suppressant-induced behavioral and neuronal activity recorded in the NAc shell depend, to various extents, on dopaminergic activation and thus point to an important role for D1/D2-like receptors (in the NAc shell) in the mechanism of action for these anorexic compounds.
    Journal of Neurophysiology 07/2015; 114(1):585-607. · 2.89 Impact Factor
    • "Since the ergogenic effect observed in this previous research was elicited immediately after the ingestion of the solution, the underlying mechanism is likely to be of a central origin rather than a metabolic effect resulting from the intestinal absorption of quinine. In support of this notion, the activation of bitter taste receptors has been shown to result in the excitation of afferent nerve fibers and the subsequent activation of several brain areas (Small et al. 2003; Zald et al. 2002) that may have the capacity to affect corticomotor excitability and thereby influence performance (Critchley 2005; Kelley et al. 2005). One way to test the hypothesis that quinine mouth rinsing and ingestion impacts corticomotor excitability is with the use of transcranial magnetic stimulation (TMS), a non-invasive method commonly used to investigate the physiological state of neural networks between the motor cortex and skeletal muscles. "
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    ABSTRACT: Recently, we have shown that the combination of mouth rinsing and ingesting a bitter-tasting quinine solution immediately prior to the performance of a maximal 30-s cycling sprint significantly improves mean and peak power output. This ergogenic effect was proposed to be related to the activation of the corticomotor pathway by afferent taste signals originating from bitter taste receptors in the oral cavity. The aim of the present study was to use single-pulse transcranial magnetic stimulation to investigate whether mouth rinsing and ingestion of a bitter quinine solution increases corticomotor excitability. A series of 10 motor-evoked potentials (MEPs) were recorded from the relaxed first dorsal interosseus muscle in 16 male competitive cyclists immediately before and after they rinsed their mouth for 10 s and then ingested either a 2 mM bitter quinine solution or plain water. Mean MEP amplitude was significantly increased in response to quinine administration by 16 % (p < 0.05), with no evidence of a time-dependent effect over the 10 pulses. Mean MEP amplitude also increased by 10 % in response to water administration (p < 0.05), though this increase was significantly smaller than the response to quinine (p < 0.05). We conclude that the activation of bitter taste receptors in the oral cavity and upper gastrointestinal tract has the capacity to increase corticomotor excitability in male competitive cyclists.
    Arbeitsphysiologie 06/2015; 115(10). DOI:10.1007/s00421-015-3200-2 · 2.19 Impact Factor
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