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Opioid receptors in the nucleus accumbens regulate attentional learning in the blocking paradigm.

ABSTRACT: Fear learning depends on prediction error, or the discrepancy between the actual and expected outcome of a conditioning trial. These experiments used blocking and unblocking designs to study the role of opioid receptors in the nucleus accumbens (Acb) in predictive fear learning. Previous fear conditioning to a context blocked later fear conditioning to a conditioned stimulus (CS) in that context. Fear learning proceeded normally (i.e., unblocking occurred) if the CS signaled a more intense footshock than was used during previous context conditioning. Blocking and unblocking were mediated by Acb opioid receptors. Acb microinjections of a nonselective opioid receptor agonist prevented blocking, whereas a nonselective antagonist prevented unblocking. Examination of the associative mechanism for blocking and unblocking revealed that Acb opioid receptors mediate indirect predictive learning by controlling learned variations in attention. Mu-opioid and kappa-opioid receptors contribute to this learned regulation of attention because Acb microinjections of a mu-opioid receptor agonist impaired, whereas a kappa-opioid receptor agonist facilitated, blocking. Acb microinjections of a mu-opioid receptor antagonist also prevented unblocking. Microinjections of a delta-opioid receptor agonist or antagonist were without effect on blocking and unblocking. Our data show that the Acb mediates attentional selection between competing predictors of motivationally significant events to enable learning about the best predictor of such events at the expense of worse predictors. During fear learning, Acb mu-opioid receptors upregulate attention to conditioned stimuli that are predictive of shock, whereas kappa-opioid receptors downregulate attention to conditioned stimuli that are redundant or noninformative predictors of shock.

SUBMITTER: Iordanova MD

PROVIDER: S-EPMC6673876 | biostudies-literature | 2006 Apr

REPOSITORIES: biostudies-literature

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Opioid receptors in the nucleus accumbens regulate attentional learning in the blocking paradigm.

Iordanova Mihaela D MD McNally Gavan P GP Westbrook R Frederick RF

The Journal of neuroscience : the official journal of the Society for Neuroscience 20060401 15

Fear learning depends on prediction error, or the discrepancy between the actual and expected outcome of a conditioning trial. These experiments used blocking and unblocking designs to study the role of opioid receptors in the nucleus accumbens (Acb) in predictive fear learning. Previous fear conditioning to a context blocked later fear conditioning to a conditioned stimulus (CS) in that context. Fear learning proceeded normally (i.e., unblocking occurred) if the CS signaled a more intense foots ...[more]

PMID: 16611820

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Project description:BackgroundChronic ethanol exposure reduces dopamine transmission in the nucleus accumbens, which may contribute to the negative affective symptoms associated with ethanol withdrawal. Kappa opioid receptors have been implicated in withdrawal-induced excessive drinking and anxiety-like behaviors and are known to inhibit dopamine release in the nucleus accumbens. The effects of chronic ethanol exposure on kappa opioid receptor-mediated changes in dopamine transmission at the level of the dopamine terminal and withdrawal-related behaviors were examined.MethodsFive weeks of chronic intermittent ethanol exposure in male C57BL/6 mice were used to examine the role of kappa opioid receptors in chronic ethanol-induced increases in ethanol intake and marble burying, a measure of anxiety/compulsive-like behavior. Drinking and marble burying were evaluated before and after chronic intermittent ethanol exposure, with and without kappa opioid receptor blockade by nor-binaltorphimine (10mg/kg i.p.). Functional alterations in kappa opioid receptors were assessed using fast scan cyclic voltammetry in brain slices containing the nucleus accumbens.ResultsChronic intermittent ethanol-exposed mice showed increased ethanol drinking and marble burying compared with controls, which was attenuated with kappa opioid receptor blockade. Chronic intermittent ethanol-induced increases in behavior were replicated with kappa opioid receptor activation in naïve mice. Fast scan cyclic voltammetry revealed that chronic intermittent ethanol reduced accumbal dopamine release and increased uptake rates, promoting a hypodopaminergic state of this region. Kappa opioid receptor activation with U50,488H concentration-dependently decreased dopamine release in both groups; however, this effect was greater in chronic intermittent ethanol-treated mice, indicating kappa opioid receptor supersensitivity in this group.ConclusionsThese data suggest that the chronic intermittent ethanol-induced increase in ethanol intake and anxiety/compulsive-like behaviors may be driven by greater kappa opioid receptor sensitivity and a hypodopaminergic state of the nucleus accumbens.

Dataset Information

Opioid receptors in the nucleus accumbens regulate attentional learning in the blocking paradigm.

Publications

Opioid receptors in the nucleus accumbens regulate attentional learning in the blocking paradigm.

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