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Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions.

ABSTRACT: Shifting between goal-directed and habitual actions allows for efficient and flexible decision making. Here we demonstrate a novel, within-subject instrumental lever-pressing paradigm, in which mice shift between goal-directed and habitual actions. We identify a role for orbitofrontal cortex (OFC) in actions following outcome revaluation, and confirm that dorsal medial (DMS) and lateral striatum (DLS) mediate different action strategies. Simultaneous in vivo recordings of OFC, DMS and DLS neuronal ensembles during shifting reveal that the same neurons display different activities depending on whether presses are goal-directed or habitual, with DMS and OFC becoming more and DLS less engaged during goal-directed actions. Importantly, the magnitude of neural activity changes in OFC following changes in outcome value positively correlates with the level of goal-directed behavior. Chemogenetic inhibition of OFC disrupts goal-directed actions, whereas optogenetic activation of OFC specifically increases goal-directed pressing. These results also reveal a role for OFC in action revaluation, which has implications for understanding compulsive behavior.

SUBMITTER: Gremel CM

PROVIDER: S-EPMC4026062 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions.

Gremel Christina M CM Costa Rui M RM

Nature communications 20130101

Shifting between goal-directed and habitual actions allows for efficient and flexible decision making. Here we demonstrate a novel, within-subject instrumental lever-pressing paradigm, in which mice shift between goal-directed and habitual actions. We identify a role for orbitofrontal cortex (OFC) in actions following outcome revaluation, and confirm that dorsal medial (DMS) and lateral striatum (DLS) mediate different action strategies. Simultaneous in vivo recordings of OFC, DMS and DLS neuron ...[more]

PMID: 23921250

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Project description:Behavioral evidence suggests that instrumental conditioning is governed by two forms of action control: a goal-directed and a habit learning process. Model-based reinforcement learning (RL) has been argued to underlie the goal-directed process; however, the way in which it interacts with habits and the structure of the habitual process has remained unclear. According to a flat architecture, the habitual process corresponds to model-free RL, and its interaction with the goal-directed process is coordinated by an external arbitration mechanism. Alternatively, the interaction between these systems has recently been argued to be hierarchical, such that the formation of action sequences underlies habit learning and a goal-directed process selects between goal-directed actions and habitual sequences of actions to reach the goal. Here we used a two-stage decision-making task to test predictions from these accounts. The hierarchical account predicts that, because they are tied to each other as an action sequence, selecting a habitual action in the first stage will be followed by a habitual action in the second stage, whereas the flat account predicts that the statuses of the first and second stage actions are independent of each other. We found, based on subjects' choices and reaction times, that human subjects combined single actions to build action sequences and that the formation of such action sequences was sufficient to explain habitual actions. Furthermore, based on Bayesian model comparison, a family of hierarchical RL models, assuming a hierarchical interaction between habit and goal-directed processes, provided a better fit of the subjects' behavior than a family of flat models. Although these findings do not rule out all possible model-free accounts of instrumental conditioning, they do show such accounts are not necessary to explain habitual actions and provide a new basis for understanding how goal-directed and habitual action control interact.

Project description:IntroductionHarmful behavior such as smoking may reflect a disturbance in the balance of goal-directed and habitual control. Animal models suggest that habitual control develops after prolonged substance use. In this study, we investigated whether smokers (N = 49) differ from controls (N = 46) in the regulation of goal-directed and habitual behavior. It was also investigated whether individual differences in nicotine dependence levels were associated with habitual responding.MethodsWe used two different multistage instrumental learning tasks that consist of an instrumental learning phase, subsequent outcome devaluation, and a testing phase to measure the balance between goal-directed and habitual responding. The testing phases of these tasks occurred after either appetitive versus avoidance instrumental learning. The appetitive versus aversive instrumental learning stages in the two different tasks modeled positive versus negative reinforcement, respectively.ResultsSmokers and nonsmoking controls did not differ on habitual versus goal-directed control in either task. Individual differences in nicotine dependence within the group of smokers, however, were positively associated with habitual responding after appetitive instrumental learning. This effect seems to be due to impaired stimulus-outcome learning, thereby hampering goal-directed task performance and tipping the balance to habitual responding.ConclusionsThe current finding highlights the importance of individual differences within smokers. For future research, neuroimaging studies are suggested to further unravel the nature of the imbalance between goal-directed versus habitual control in severely dependent smokers by directly measuring activity in the corresponding brain systems.ImplicationsGoal-directed versus habitual behavior in substance use and addiction is highly debated. This study investigated goal-directed versus habitual control in smokers. The findings suggest that smokers do not differ from controls in goal-directed versus habitual control. Individual differences in nicotine dependence within smokers, however, were positively associated with habitual responding after appetitive instrumental learning. This effect seems to be due to impaired stimulus-outcome learning, thereby hampering goal-directed task performance and tipping the balance to habitual responding. These findings add to the ongoing debate on habitual versus goal-directed control in addiction and emphasize the importance of individual differences within smokers.

Project description:Understanding of other's actions as goal-directed is considered a fundamental ability underlying cognitive and social development in human infants. A number of studies using the habituation-dishabituation paradigm have shown that the ability to discern intentional relations, in terms of goal-directedness of an action towards an object, appears around 5 months of age. The question of whether non-human species can perceive other's actions as goal-directed has been more controversial, however there is mounting evidence that at least some primates species do. Recently domestic dogs have been shown to be particularly sensitive to human communicative cues and more so in cooperative and intentional contexts. Furthermore, they have been shown to imitate selectively. Taken together these results suggest that dogs may perceive others' actions as goal-directed, however no study has investigated this issue directly. In the current study, adopting an infant habituation-dishabituation paradigm, we investigated whether dogs attribute intentions to an animate (a human) but not an inanimate (a black box) agent interacting with an object. Following an habituation phase in which the agent interacted always with one of two objects, two sets of 3 trials were presented: new side trials (in which the agent interacted with the same object as in the habituation trial but placed in a novel location) and new goal trials (in which the agent interacted with the other object placed in the old location). Dogs showed a similar pattern of response to that shown in infants, looking longer in the new goal than new side trials when they saw the human agent interact with the object. No such difference emerging with the inanimate agent (the black box). Results provide the first evidence that a non-primate species can perceive another individual's actions as goal-directed. We discuss results in terms of the prevailing mentalisitic and non-mentalistic hypotheses regarding goal-attribution.

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Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions.

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Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions.

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