Alcohol-Paired Contextual Cues Produce an Immediate and Selective Loss of Goal-directed Action in Rats

Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, University of California at Los Angeles Los Angeles, CA, USA.
Frontiers in Integrative Neuroscience 07/2010; 4. DOI: 10.3389/fnint.2010.00019
Source: PubMed


We assessed whether the presence of contextual cues paired with alcohol would disrupt rats' capacity to express appropriate goal-directed action control. Rats were first given differential context conditioning such that one set of contextual cues was paired with the injection of ethanol and a second, distinctive set of cues was paired with the injection of saline. All rats were then trained in a third, neutral context to press one lever for grain pellets and another lever for sucrose pellets. They were then given two extinction tests to evaluate their ability to choose between the two actions in response to the devaluation of one of the two food outcomes with one test conducted in the alcohol-paired context and the other conducted in the control (saline-paired) context. In the control context, rats exhibited goal-directed action control; i.e., they were able selectively to withhold the action that previously earned the now devalued outcome. However, these same rats were impaired when tested in the alcohol-paired context, performing both actions at the same rate regardless of the current value of their respective outcomes. Subsequent testing revealed that the rats were capable of overcoming this impairment if they were giving response-contingent feedback about the current value of the food outcomes. These results provide a clear demonstration of the disruptive influence that alcohol-paired cues can exert on decision-making in general and goal-directed action selection and choice in particular.

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Available from: Bernard W Balleine, Oct 05, 2015
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    • "There is direct evidence that alcohol-paired environmental stimuli can promote habitual behavior. For example, Ostlund et al. (2010) found that when rats were tested in a saline-paired context they showed a significant devaluation effect. However, when the same rats with the same training history were tested in a context that had been paired with alcohol they were insensitive to outcome devaluation indicating habitual responding and demonstrating that alcohol-predictive cues can disrupt decision making. "
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    ABSTRACT: Chronic alcohol self-administration leads to alcohol-seeking behavior that is habitual and insensitive to changes in the value of the earned alcohol. Such behavior has been shown to rely on the dorsolateral region of the striatum in rats but the specific pharmacological control of output from this region is not yet understood. In the following experiments rats were trained to self-administer unsweetened 10% (v/v) ethanol in daily sessions for 8 weeks prior to testing for sensitivity to outcome devaluation. We examined the role of glutamatergic AMPA-receptor activation by testing the effects of the antagonist NBQX (0.3 and 1.0 μg/μl) infused specifically into the dorsolateral striatum (DLS) before devaluation testing. In a separate group of rats we examined the role of dopaminergic D2-receptor activation using the D2-receptor antagonist raclopride (0.2 and 1.0 μg/μl) infused into the DLS before devaluation testing. Following control (saline) infusions rats' lever-press performance was insensitive to devaluation of ethanol thus showing evidence of habitual responding. NBQX and racolpride each restored goal-directed control of responding at doses that did not impair overall lever-press rates. These data demonstrate that expression of habitual alcohol seeking relies on glutamatergic inputs to the DLS and D2 receptors within the DLS.
    Frontiers in Behavioral Neuroscience 09/2014; 8:301. DOI:10.3389/fnbeh.2014.00301 · 3.27 Impact Factor
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    • "One possibility is that the effects of ethanol and the VI schedule during training were simply additive, pushing the “strength” of the habit system past some threshold necessary for achieving dominance. Indeed, ethanol exposure has been reported by a number of groups to promote habitual expression of instrumental behavior, which may reflect enhanced S-R mechanisms and/or impaired goal-directed control—depending on the experimental manipulation or assay (Ostlund et al., 2010; Corbit et al., 2012; Hogarth et al., 2012; Hay et al., 2013; Sjoerds et al., 2013). For instance, chronic exposure to ethanol appears to elicit persistent neuroadaptations that enhance habitual expression of instrumental behavior in general. "
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    ABSTRACT: We previously reported that, in male, Long Evans rats, instrumental lever pressing that had been reinforced during limited training under a variable interval (VI) schedule by oral self-administration of a 10% sucrose/10% ethanol (10S10E) solution was insensitive to devaluation of 10S10E. In contrast, lever pressing that had been reinforced under a variable ratio (VR) schedule, or by self-administration of 10% sucrose (10S) alone, was sensitive to outcome devaluation. The relative insensitivity to outcome devaluation indicated that seeking of 10S10E by the VI-trained rats had become an instrumental habit. In the present study we employed an alternative operational definition of an instrumental habit and compared the effect of reversing the action-outcome contingency on lever press performance by rats trained under the same experimental conditions. Male Long Evans rats received daily operant training, in which lever presses were reinforced by 10S10E or 10S, under VI or VR schedules. After nine sessions of VI or VR training, rats were tested over four sessions in which the instrumental contingency was changed so that a lever press would prevent reinforcer delivery for 120 s. We found that rats that had been trained to lever press for 10S10E under the VR schedule showed a greater change in lever pressing across testing sessions than those that had received 10S10E reinforcement under the VI schedule. There was no such interaction with reinforcement schedule for rats that had received only 10S reinforcement during training. These findings are consistent with those of our previous study, and provide further evidence that addition of ethanol to sucrose may promote habitual responding in an instrumental task.
    Frontiers in Behavioral Neuroscience 06/2014; 8:220. DOI:10.3389/fnbeh.2014.00220 · 3.27 Impact Factor
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    • "Furthermore, a recent study found that cocaine-paired contextual stimuli can provoke impulsive decision making in rats [79]. We have also recently shown that contextual cues paired with alcohol intoxication produce a transient disruption in instrumental control, causing rats to shift from goal-directed to habitual performance [31]. Thus, the impact of repeated cocaine exposure on PIT and outcome devaluation performance may be mediated, at least in part, by context-cocaine conditioning. "
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    ABSTRACT: There is growing evidence that mere exposure to drugs can induce long-term alterations in the neural systems that mediate reward processing, motivation, and behavioral control, potentially causing the pathological pursuit of drugs that characterizes the addicted state. The incentive sensitization theory proposes that drug exposure potentiates the influence of reward-paired cues on behavior. It has also been suggested that drug exposure biases action selection towards the automatic execution of habits and away from more deliberate goal-directed control. The current study investigated whether rats given repeated exposure to peripherally administered cocaine would show alterations in incentive motivation (assayed using the Pavlovian-to-instrumental transfer (PIT) paradigm) or habit formation (assayed using sensitivity to reward devaluation). After instrumental and Pavlovian training for food pellet rewards, rats were given 6 daily injections of cocaine (15 mg/kg, IP) or saline, followed by a 10-d period of rest. Consistent with the incentive sensitization theory, cocaine-treated rats showed stronger cue-evoked lever pressing than saline-treated rats during the PIT test. The same rats were then trained on a new instrumental action with a new food pellet reward before undergoing a reward devaluation testing. Although saline-treated rats exhibited sensitivity to reward devaluation, indicative of goal-directed performance, cocaine-treated rats were insensitive to this treatment, suggesting a reliance on habitual processes. These findings, when taken together, indicate that repeated exposure to cocaine can cause broad alterations in behavioral control, spanning both motivational and action selection processes, and could therefore help explain aberrations of decision-making that underlie drug addiction.
    PLoS ONE 04/2013; 8(4):e61355. DOI:10.1371/journal.pone.0061355 · 3.23 Impact Factor
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