The current study demonstrates that alcohol-paired environmental cues can disrupt decision-making; rats tested in a context that signaled alcohol intoxication were found to lack the capacity to select actions based on their anticipated outcomes. Importantly, these rats were able to select their actions in a goal-directed manner when tested in a different context that had not been paired with alcohol, indicating that the influence of the alcohol-paired context on action selection was transitory, and was therefore unlikely to be the product of persistent neuroadaptions induced by the alcohol exposure regimen. The finding that the alcohol-paired context failed to disrupt goal-directed performance when rats were given response-contingent feedback about the current value of the available outcomes provided further support for this conclusion. This pattern of findings is therefore consistent with the hypothesis, presented in the introduction, that cues associated with drugs or alcohol can exert an acute, time-limited influence over decision-making, interfering with the cognitive processes that support goal-directed action selection and choice.
Although we found that ethanol-paired cues rendered instrumental performance insensitive to outcome devaluation, it is not clear how these cues have their effect. It has been argued that drug-related cues tax limited cognitive resources which are essential for non-automatic decision-making, allowing automatic processes to control performance (Tiffany, 1990
). A similar distinction is made in the field of instrumental conditioning, where it has been shown that rats tend to select actions using either a goal-directed strategy based on action–outcome learning or a habit strategy based on stimulus-response learning (see Yin et al., 2008
). Working from this perspective, we have argued (Ostlund and Balleine, 2008
) that drug-paired cues might cause a transition from goal-directed to habitual control, leaving instrumental performance insensitive to outcome devaluation, an account that fits nicely with the results reported here. Alternatively, rather than encouraging habitual performance, it is possible that the alcohol-paired cues interfered with retrieval or implementation of action–outcome associations, preventing rats from using the current value of the two rewards to guide their choice of actions. A third possibility is that the presence of cues signaling alcohol intoxication caused a reappraisal of the two food outcomes such that both outcomes were assigned equivalent, low incentive values (e.g., by producing anhedonia). However, this account is not consistent with our finding that rats exhibited sensitivity to outcome devaluation when they were given response-contingent feedback; this treatment should only have strengthened their assessment that both outcomes were currently undesirable.
It is important to note that rats given pairings between environmental cues and peripheral ethanol injections have been shown to develop a conditioned aversion to those cues (Cunningham, 1979
; van der Kooy et al., 1983
; Bormann and Cunningham, 1998
). Our experimental preparation prevented us from directly measuring our rats’ preference between the ethanol- and saline-paired contexts, but we did find that they displayed significantly lower levels of locomotor activity in the ethanol-paired context at test, which recent findings suggest may be indicative of conditioned place aversion learning (Hill et al., 2007
). It is therefore prudent to consider the possibility that an ethanol-induced conditioned place aversion may have generated a competing behavior (e.g., freezing) that interfered with the expression of instrumental performance, making it difficult for us to evaluate whether this behavior was sensitive to outcome devaluation or not. However, there are several features of our results that are incompatible with this possibility. First, although the ethanol-paired context was effective in suppressing activity at test, this effect was limited to the period before the lever insertion; no differences in activity were observed when the rats were actually pressing the levers. Second, although the mean rate of lever pressing was numerically lower in ethanol-paired context than in the saline-paired context, this effect was not significant. Third, since response rates were not at the behavioral floor (i.e., no presses on either lever) in the ethanol-paired context, any competing response that did exist should not have prevented the rats from displaying an outcome devaluation effect, which involves selectively withholding
whichever action had earned the devalued outcome. Thus, even if the rats had responded at a significantly lower rate in the ethanol-paired context, there was sufficient responding to observe whether their choice between the two levers was guided by goal-directed action selection.
Although this conditioned aversion-induced response competition account does not adequately explain the current results, it is possible that aversive conditioning played some role in mediating the influence of alcohol-paired cues over instrumental performance. Recent studies in rodents (Dias-Ferreira et al., 2009
) and humans (Schwabe and Wolf, 2009
, in press) have demonstrated that stress can promote habitual performance and/or interfere with goal-directed action selection. Therefore, it is possible that the disruption of goal-directed action selection produced by the context paired with alcohol in the current study was mediated by its tendency to evoke an acute stress response. This interpretation is consistent with the widely held view that stress contributes to drug relapse (Sinha, 2001
; Lê and Shaham, 2002
; Goeders, 2003
) and offers a novel behavioral mechanism through which it could be exerting its effects. However, as the current study was not designed to evaluate this hypothesis, further research will be needed to determine what, if any, role stress plays in mediating the disruptive effects of alcohol-paired cues on instrumental action selection.
Recent years have seen considerable interest in theories of addiction that attempt to explain the compulsive nature of drug seeking through the effects of chronic drug use on brain systems responsible for normal learning and memory. Some have suggested that drug use leads to exaggerated habit formation, promoting the use of stimulus-guided rather than outcome-guided action selection in addicts (Tiffany, 1990
; Berke and Hyman, 2000
; Everitt et al., 2001
). Indeed, rats given repeated psychostimulant administration prior to instrumental conditioning with natural food rewards have been shown to display accelerated habit formation, indicating that such treatment results in long-lasting adaptation in the neural circuitry underlying this form of learning (Nelson and Killcross, 2006
). In contrast, the incentive sensitization theory of addiction (Robinson and Berridge, 1993
) proposes that repeated drug exposure results in permanent alterations in the neural circuitry responsible for incentive motivation, which, under normal conditions, allows stimuli associated with natural rewards and drugs to elicit approach behavior and invigorate reward seeking. Drug-induced adaptations in this system result in a sensitization of incentive motivational processes, potentiating the excitatory influence that reward- and drug-paired cues have over behavior (Wyvell and Berridge, 2001
). Although both accounts have received strong experimental support over the years, neither can explain the acute and time-limited disruption of goal-directed action selection produced by ethanol-paired stimuli reported here. The accelerated habit learning account predicts that if our repeated alcohol pre-exposure regimen were to have any effect at all on instrumental performance, it should have resulted in a persistent, context-independent
disruption of goal-directed performance. In contrast, according to the incentive sensitization account, one might expect the presence of ethanol-paired cues to invigorate responding by activating the incentive motivational system, which has presumably been sensitized due to the repeated alcohol administration. Not only did we fail to find such an effect, this account does not directly address the insensitivity of action selection to outcome devaluation. Even if both
actions should have been performed at a higher rate (relative to baseline conditions or when rats were tested in the saline-paired context), one would still expect to observe higher rates of responding on the action whose outcome remained valuable.
The current results may be particularly relevant to the early stages of the addiction process. Experienced drug users are said to display compulsive drug seeking if this behavior persists despite its considerable adverse consequences. As argued elsewhere (Ostlund and Balleine, 2008
), this insensitivity to response-contingent punishment suggests that compulsive drug seeking may be dominated by habitual control; such addicts lack the capacity to shift from habitual to goal-directed performance when confronted by aversive stimuli. However, the current findings demonstrate that drug-paired cues can exert a more subtle, time-limited effect on instrumental control. Although ethanol-paired cues were found to disrupt the rats’ tendency to selectively withhold an action whose outcome had been devalued if tested without feedback (i.e., in extinction), this effect was not observed when the devalued outcome was delivered at test, which may be considered a form of punishment. Thus it appears that context-alcohol learning can interfere with goal-directed action selection without generating truly compulsive behavior. However, even if transient and rapidly overcome, it is possible that exposure to drug-related cues could promote drug use by obstructing the user from considering the consequences of this behavior, thereby rendering action initiation more impulsive. This increased drug exposure could, as a consequence, result in more persistent neuroadaptions, facilitating the transition from drug abuse to addiction.