Hypotheses of striatal orchestration of behavior ascribe distinct functions to striatal subregions, with the dorsolateral striatum (DLS) especially implicated in habitual and skilled performance. Thus neural activity patterns recorded from the DLS, but not the dorsomedial striatum (DMS), should be correlated with habitual and automatized performance. Here, we recorded DMS and DLS neural activity in rats during training in a task promoting habitual lever pressing. Despite improving performance across sessions, clear changes in corresponding neural activity patterns were not evident in DMS or DLS during early training. Although DMS and DLS activity patterns were distinct during early training, their activity was similar following extended training. Finally, performance after extended training was not associated with DMS disengagement, as would be predicted from prior work. These results suggest that behavioral sequences may continue to engage both striatal regions long after initial acquisition, when skilled performance is consolidated.
Flexible and efficient decision-making in complex environments can be achieved through constant interactions between the goal-directed and habitual systems. While goal-directed behavior is considered dependent upon Response-Outcome (R-O) associations, habits instead rely on Stimulus-Response (S-R) associations. However, the stimuli that support the S-R association underlying habitual responding in typical instrumental procedures are poorly defined. To resolve this issue, we designed a discrete-trials procedure, in which rats must wait for lever insertion and complete a sequence of five lever presses to obtain a reward (20% sucrose or grain-based pellets). Lever insertion thus constituted an audio-visual stimulus signaling the opportunity for reward. Using sensory-specific satiety-induced devaluation, we found that rats trained with grain-based pellets remained sensitive to outcome devaluation over the course of training with this procedure whereas rats trained with a solution of 20% sucrose rapidly developed habit, and that insensitivity to outcome devaluation in rats trained with sucrose did not result from a bias in general satiety. Importantly, although rats trained with pellets were sensitive to satiety-induced devaluation, their performance was not affected by degradation of instrumental contingency and devaluation by conditioned taste aversion (CTA), suggesting that these rats may also have developed habitual responding. To test whether the discrete-trials procedure biases subjects towards habitual responding, we compared discrete-trials to free-running instrumental responding, and found that rats trained with sucrose in a fixed-ratio 5 (FR5) procedure with continuous presentation of the lever were goal-directed. Together, these results demonstrate that discrete presentations of a stimulus predictive of reward availability promoted the formation of S-R habit in rats trained with liquid sucrose. Further research is necessary to explain inconsistencies in sensitivity to outcome devaluation when rats are trained with grain-based pellets.
Ample evidence shows that the setting can control drug choices in both humans and animals. Here we reveal in rats that a major mechanism of this control involves a regulation of the drug influence on other competing options at the time of choice. Briefly, rats were offered a choice between a drug dose (cocaine or heroin) and a brief access to water sweetened with saccharin in two different settings. In one setting, choosing under the influence was not possible and rats largely preferred saccharin over either cocaine or heroin. In contrast, when the same rats were shifted to a setting where choosing under the influence was possible, they chose the drug either nonexclusively or exclusively depending on whether the drug enhanced or suppressed sweet reward, respectively. Thus, when rats were under the orexigenic influence of heroin at the time of choice, they more frequently chose saccharin in alternation with heroin. In contrast, when rats were under the anorexic influence of cocaine, they stopped choosing saccharin and continued taking cocaine exclusively. These settingand drug-specific changes in preference were rapid and reversible, and could be induced by passively administering cocaine or heroin before choice. Finally, rats behaved as if they were oblivious to the drug influence on their choices. This behavior could explain why rats are vulnerable to harm themselves, sometimes to the point of death, in settings where choices are made under the drug influence, notably if this influence excludes other important options or, conversely, enhances harmful ones.
It has long been suggested that alcohol or substance use disorders could emerge from the progressive development and dominance of drug habits. Like habits, drug-related behaviors are often triggered by drug-associated cues. Like habits, addictive behaviors are strong, rigid and "hard to break". Like habits, these behaviors are insensitive to their outcome and persist despite negative consequences. "Pathological habit" thus appears as a good candidate to explain the transition to compulsive drug use. However, drug use could also be considered as a goal-directed choice, driven by the expectation of drug outcomes. For example, drug addicts may engage in drug-seeking behaviors because they view the drug as more valuable than available alternatives. Substance use disorders therefore may not be all about habit, nor fully intentional, and could be considered as resulting from an imbalance between goal-directed and habitual control. The main objective of this review is to disentangle the relative contribution of habit formation and impairment of goal-directed behavior in this unbalanced control of addictive behaviors. Although deficits in goal-directed behavior have been demonstrated in alcohol and substance use disorders, reliable demonstration of abnormal habit formation has been curtailed by the paucity of paradigms designed to assess habit as a positive result. Refining our animal and human model of habit is therefore required to precisely define the place of habit in substance use disorders and develop appropriate and adapted neurobehavioral treatments.
Addiction was suggested to emerge from the progressive dominance of habits over goaldirected behaviors. However, it is generally assumed that habits do not persist in choice settings. Therefore, it is unclear how drug habits may persist in real-world scenarios where this factor predominates. Here, we discuss the poor translational validity of the habit construct, which impedes our ability to determine its role in addiction. New evidence of habitual behavior in a drug choice setting are then described and discussed. Interestingly, habitual preference did not promote drug choice but instead favored abstinence. Here, we propose several clues to reconcile these unexpected results with the habit theory of addiction, and we highlight the need in experimental research to face the complexity of drug addicts' decision-making environments by investigating drug habits in the context of choice and in the presence of cues. On a theoretical level, we need to consider more complex frameworks, taking into account continuous interactions between goal-directed and habitual systems, and alternative decision-making models more representative of real-world conditions. Drugs promote habitA large number of studies in rodents show that drugs of abuse promote habit. Following drug selfadministration training, drugs can be devalued using either sensory-specific satiety or conditioned taste aversion (CTA) before responding for the drug is tested under extinction (box 1). Using this procedure, it was shown that responding for ethanol [11][12][13][14][15][16][17], cocaine [18,19] and nicotine [20,21] becomes habitual after various length of training. In some studies, the transition to habit was faster for the drug compared to a non-drug reward suggesting stronger facilitation of habit formation for drug-seeking [11,13,15,18,21]. Interestingly, studies in which rats are trained to self-administer cocaine or heroin in a seeking-taking schedule (e.g. heterogeneous chains; seeking RI30 -taking FR1 on separate levers) reveal that rats correctly encode the contingency between the seeking response,
The biological robustness in the neural substrates of sugar and sweet reward may be sufficient to explain why many people can have difficultly to control the consumption of foods high in sugar when continuously exposed to them.
The concept of compulsive cocaine-seeking habits is difficult to reconcile with other evidence showing that humans and even rats remain able to shift their choice away from the drug and toward an alternative nondrug reward, when available. This paradox could dissolve if preference for the nondrug option reflected in fact inflexible habitual decision-making (i.e., fixed in a habitual control mode, with no return to a goal-directed control mode). Previous research in rats has shown that prior drug use can favor habit formation, but whether the resulting habits are inflexible or not is largely unknown. Here we addressed this question by manipulating the value of water in rats that chose between water and cocaine in a discrete-trials procedure. Rats preferred water when thirsty and maintained this preference despite water devaluation by satiation. Only with repeated daily testing under water satiation did they progressively reverse their preference toward cocaine. Additional evidence showed that this progressive reversal of preference reflected in fact new interoceptive discrimination learning. Overall, this study suggests that rats seem to be stuck in a habitual decision-making mode, unable to return to a goal-directed mode upon experiencing a change in options value. It also reveals that inflexible decision-making does not necessarily promote drug choice, but can also under some circumstances favor abstinence.
For proper execution of goal-directed behaviors, individuals require both a general representation of the goal and an ability to monitor their own progress toward that goal. Here, we examine how dorsomedial striatum (DMS), a region pivotal for forming associations among stimuli, actions, and outcomes, encodes the execution of goal-directed action sequences that require self-monitoring of behavior. We trained rats to complete a sequence of at least five consecutive lever presses (without visiting the reward port) to obtain a reward and recorded the activity of individual cells in DMS while rats performed the task. We found that the pattern of DMS activity gradually changed during the execution of the sequence, permitting accurate decoding of sequence progress from neural activity at a population level. Moreover, this sequence-related activity was blunted on trials where rats did not complete a sufficient number of presses. Overall, these data suggest a link between DMS activity and the execution of behavioral sequences that require monitoring of ongoing behavior.
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