Nucleus Accumbens Neurons Are Innately Tuned for Rewarding and Aversive Taste Stimuli, Encode Their Predictors, and Are Linked to Motor Output

Department of Psychology, University of North Carolina, Chapel Hill, North Carolina 27599, USA.
Neuron (Impact Factor: 15.05). 03/2005; 45(4):587-97. DOI: 10.1016/j.neuron.2004.12.055
Source: PubMed


The nucleus accumbens (NAc) is a key component of the brain's reward pathway, yet little is known of how NAc cells respond to primary rewarding or aversive stimuli. Here, naive rats received brief intraoral infusions of sucrose and quinine paired with cues in a classical conditioning paradigm while the electrophysiological activity of individual NAc neurons was recorded. NAc neurons (102) were typically inhibited by sucrose (39 of 52, 75%) or excited by quinine (30 of 40, 75%) infusions. Changes in firing rate were correlated with the oromotor response to intraoral infusions. Most taste-responsive neurons responded to only one of the stimuli. NAc neurons developed responses to the cues paired with sucrose and quinine. Thus, NAc neurons are innately tuned to rewarding and aversive stimuli and rapidly develop responses to predictive cues. The results indicate that the output of the NAc is very different when rats taste rewarding versus aversive stimuli.

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Available from: Mitchell F Roitman, Apr 11, 2014
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    • "reportedthatapproximately30%ofNAc coreandshellneuronsincreasedinfiringinresponsetosweet rewards(Roitmanetal.,2005,2010;Wheeleretal.,2008). TahaandFields(2005)reportedthatnearly75%ofshelland coreneuronsinNAcshowedincreasesinfiringelicitedby sucroserewards,withhighestfiringtothemostconcentrated sucrosesolution.Additionally,severalotherelectrophysiological studiesreportthatapproximately30%–50%ofNAcshelland coreneuronsincreasefiringduringanticipationorduring instrumentalactionsaimedatobtainingfood,waterorcocaine rewards(Carelli,2000;Carellietal.,2000;Hollanderetal.,2002; Nicolaetal.,2004b). "
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    ABSTRACT: The study of the neural bases of eating behavior, hunger, and reward has consistently implicated the lateral hypothalamus (LH) and its interactions with mesocorticolimbic circuitry, such as mesolimbic dopamine projections to nucleus accumbens (NAc) and ventral pallidum (VP), in controlling motivation to eat. The NAc and VP play special roles in mediating the hedonic impact ("liking") and motivational incentive salience ("wanting") of food rewards, and their interactions with LH help permit regulatory hunger/satiety modulation of food motivation and reward. Here, we review some progress that has been made regarding this circuitry and its functions: the identification of localized anatomical hedonic hotspots within NAc and VP for enhancing hedonic impact; interactions of NAc/VP hedonic hotspots with specific LH signals such as orexin; an anterior-posterior gradient of sites in NAc shell for producing intense appetitive eating vs. intense fearful reactions; and anatomically distributed appetitive functions of dopamine and mu opioid signals in NAc shell and related structures. Such findings help improve our understanding of NAc, VP, and LH interactions in mediating affective and motivation functions, including "liking" and "wanting" for food rewards.
    Frontiers in Systems Neuroscience 06/2015; 9:90. DOI:10.3389/fnsys.2015.00090
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    • "Food-predictive cues also evoke phasic changes in the activity of NAc neurons (Nicola et al. 2004; Roitman et al. 2005; Day et al. 2006). Cue-evoked NAc activity has been directly linked to food-seeking in a variety of behavioral paradigms (Taha et al. 2007; McGinty et al. 2013; Roitman and Loriaux 2014). "
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    ABSTRACT: Environmental stimuli that signal food availability hold powerful sway over motivated behavior and promote feeding, in part, by activating the mesolimbic system. These food-predictive cues evoke brief (phasic) changes in nucleus accumbens (NAc) dopamine concentration and in the activity of individual NAc neurons. Phasic fluctuations in mesolimbic signaling have been directly linked to goal-directed behaviors, including behaviors elicited by food-predictive cues. Food-seeking behavior is also strongly influenced by physiological state (i.e. hunger vs. satiety). Ghrelin, a stomach hormone that crosses the blood-brain barrier, is linked to the perception of hunger and drives food intake, including intake potentiated by environmental cues. Notwithstanding, whether ghrelin regulates phasic mesolimbic signaling evoked by food-predictive stimuli is unknown. Here, rats underwent Pavlovian conditioning in which one cue predicted the delivery of rewarding food (CS+) and a second cue predicted nothing (CS-). After training, we measured the effect of ghrelin infused into the lateral ventricle (LV) on sub-second fluctuations in NAc dopamine using fast-scan cyclic voltammetry and individual NAc neuron activity using in vivo electrophysiology in separate groups of rats. LV ghrelin augmented both phasic dopamine and phasic increases in the activity of NAc neurons evoked by the CS+. Importantly, ghrelin did not affect the dopamine nor NAc neuron response to the CS-, suggesting that ghrelin selectively modulated mesolimbic signaling evoked by motivationally significant stimuli. These data demonstrate that ghrelin, a hunger signal linked to physiological state, can regulate cue-evoked mesolimbic signals that underlie food-directed behaviors. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Journal of Neurochemistry 02/2015; 133(6). DOI:10.1111/jnc.13080 · 4.28 Impact Factor
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    • "Moreover, individual neurons within the NAc respond to the receipt of rewards, the cues that predict them, and operant approach behaviors to obtain them (Carelli 2004; Day et al. 2006; Nicola et al. 2004). NAc neurons respond to such salient events with phasic changes in activity, which appear to play different roles in reward-directed behaviors (Ambroggi et al. 2011; Krause et al. 2010; Roitman et al. 2005; Taha and Fields 2006). "
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    ABSTRACT: Our behavior is powerfully driven by environmental cues that signal the availability of rewarding stimuli. We frequently encounter stimuli - a bowl of candy or smartphone alert - that trigger actions to obtain those rewards, even though there may positive outcomes associated with not acting. The inability to restrain ones action in the presence of reward-associated cues is one type of impulsive behavior, and a component of such maladaptive behaviors as overeating, gambling, and substance abuse. The nucleus accumbens (NAc) is ideally situated to integrate multiple cognitive and affective inputs to bias action via outputs through the basal ganglia. NAc neurons have been shown to respond to cues that predict reward availability, goal-directed behaviors aimed at obtaining them, and delivery of reward itself. As these processes are typically associated, it is difficult to discern whether signals in the NAc are more closely related to processing reward-predictive aspects of goal-directed behavior, or selection of behavioral response. To dissociate these possibilities, we recorded the activity of NAc neurons while rats performed a task in which two different cues both informed rats of reward availability, but required them to either press a lever (Go), or withhold pressing (NoGo) to obtain the reward. Individual cue-responsive neurons showed either increases or decreases in activity at cue onset. Increases in activity were larger, and decreases smaller, when rats withheld lever pressing, whether correctly for NoGo trials or in error on Go trials. Thus, NAc cue responses correlated with action, regardless of cue type or accuracy.
    Journal of Neurophysiology 10/2013; 111(2). DOI:10.1152/jn.00350.2013 · 2.89 Impact Factor
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