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

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

The push and pull of dopamine in cue-reward learning

A recent study by Saunders, Richard, Margolis, and Janak (2018) shows that there is a great deal left to learn about what different mesotelencephalic dopamine circuits contribute to learning about the motivational significance of reward-related cues. Their findings suggest that nigrostriatal and mesolimbic dopamine pathways support distinct reinforcement processes that independently push and pull animals toward their goals

Repeated cocaine exposure dysregulates cognitive control over cue-evoked reward-seeking behavior during Pavlovian-to-instrumental transfer

Drug-paired cues acquire powerful motivational properties, but only lead to active drug-seeking behavior if they are potent enough to overwhelm the cognitive control processes that serve to suppress such urges. Studies using the Pavlovian-to-instrumental transfer (PIT) task have shown that rats pretreated with cocaine or amphetamine exhibit heightened levels of cue-motivated food-seeking behavior, suggesting that exposure to these drugs sensitizes the incentive motivational system. However, the PIT testing protocol can also create conflict between two competing behavioral responses to the reward-paired cue: active reward seeking (e.g., lever pressing) and passive conditioned food-cup approach behavior. We therefore investigated whether repeated cocaine exposure alters the way in which rats use cue-based reward expectations to resolve such conflict. In-depth analysis of previously published and new research confirmed that when drug-naïve rats are given a cue that signals the timing of a delayed noncontingent reward, they adaptively transition from reward seeking to conditioned approach behavior, facilitating efficient collection of the predicted reward. In contrast, cocaine-exposed rats exhibit pronounced behavioral dysregulation, increasing, rather than suppressing, their reward-seeking behavior over time, disrupting their ability to passively collect reward. Such findings speak to the important and sometimes overlooked role that cognitive control plays in determining the motivational impact of cues associated with drug and nondrug rewards

A Closer Look at the Effects of Repeated Cocaine Exposure on Adaptive Decision-Making under Conditions That Promote Goal-Directed Control.

It has been proposed that compulsive drug seeking reflects an underlying dysregulation in adaptive behavior that favors habitual (automatic and inflexible) over goal-directed (deliberative and highly flexible) action selection. Rodent studies have established that repeated exposure to cocaine or amphetamine facilitates the development of habits, producing behavior that becomes unusually insensitive to a reduction in the value of its outcome. The current study more directly investigated the effects of cocaine pre-exposure on goal-directed learning and action selection using an approach that discourages habitual performance. After undergoing a 15-day series of cocaine (15 or 30 mg/kg, i.p.) or saline injections and a drug withdrawal period, rats were trained to perform two different lever-press actions for distinct reward options. During a subsequent outcome devaluation test, both cocaine- and saline-treated rats showed a robust bias in their choice between the two actions, preferring whichever action had been trained with the reward that retained its value. Thus, it appears that the tendency for repeated cocaine exposure to promote habit formation does not extend to a more complex behavioral scenario that encourages goal-directed control. To further explore this issue, we assessed how prior cocaine treatment would affect the rats' ability to learn about a selective reduction in the predictive relationship between one of the two actions and its outcome, which is another fundamental feature of goal-directed behavior. Interestingly, we found that cocaine-treated rats showed enhanced, rather than diminished, sensitivity to this action-outcome contingency degradation manipulation. Given their mutual dependence on striatal dopamine signaling, we suggest that cocaine's effects on habit formation and contingency learning may stem from a common adaptation in this neurochemical system

A Closer Look at the Effects of Repeated Cocaine Exposure on Adaptive Decision-Making under Conditions That Promote Goal-Directed Control.

It has been proposed that compulsive drug seeking reflects an underlying dysregulation in adaptive behavior that favors habitual (automatic and inflexible) over goal-directed (deliberative and highly flexible) action selection. Rodent studies have established that repeated exposure to cocaine or amphetamine facilitates the development of habits, producing behavior that becomes unusually insensitive to a reduction in the value of its outcome. The current study more directly investigated the effects of cocaine pre-exposure on goal-directed learning and action selection using an approach that discourages habitual performance. After undergoing a 15-day series of cocaine (15 or 30 mg/kg, i.p.) or saline injections and a drug withdrawal period, rats were trained to perform two different lever-press actions for distinct reward options. During a subsequent outcome devaluation test, both cocaine- and saline-treated rats showed a robust bias in their choice between the two actions, preferring whichever action had been trained with the reward that retained its value. Thus, it appears that the tendency for repeated cocaine exposure to promote habit formation does not extend to a more complex behavioral scenario that encourages goal-directed control. To further explore this issue, we assessed how prior cocaine treatment would affect the rats' ability to learn about a selective reduction in the predictive relationship between one of the two actions and its outcome, which is another fundamental feature of goal-directed behavior. Interestingly, we found that cocaine-treated rats showed enhanced, rather than diminished, sensitivity to this action-outcome contingency degradation manipulation. Given their mutual dependence on striatal dopamine signaling, we suggest that cocaine's effects on habit formation and contingency learning may stem from a common adaptation in this neurochemical system

Junk Food Exposure Disrupts Selection of Food-Seeking Actions in Rats

There is growing evidence that repeated consumption of highly palatable, nutritionally poor “junk food” diets can produce deficits in cognition and behavioral control. We explored whether long-term junk-food diet exposure disrupts rats' ability to make adaptive choices about which foods to pursue based on (1) expected reward value (outcome devaluation test) and (2) cue-evoked reward expectations (Pavlovian-to-instrumental test). Rats were initially food restricted and trained on two distinct response-outcome contingencies (e.g., left press chocolate pellets, and right press sweetened condensed milk) and stimulus-outcome contingencies (e.g., white noise chocolate pellets, and clicker sweetened condensed milk). They were then given 6 weeks of unrestricted access to regular chow alone (controls) or chow and either 1 or 24 h access to junk food per day. Subsequent tests of decision making revealed that rats in both junk-food diet groups were impaired in selecting actions based on either expected food value or the presence of food-paired cues. These data demonstrate that chronic junk food consumption can disrupt the processes underlying adaptive control over food-seeking behavior. We suggest that the resulting dysregulation of food seeking may contribute to overeating and obesity