A specific role for posterior dorsolateral striatum in human habit learning. Eur J Neurosci 29: 2225-2232

Department of Psychology, Rutgers University, Newark, NJ 07102, USA.
European Journal of Neuroscience (Impact Factor: 3.67). 06/2009; 29(11):2225-32. DOI: 10.1111/j.1460-9568.2009.06796.x
Source: PubMed

ABSTRACT Habits are characterized by an insensitivity to their consequences and, as such, can be distinguished from goal-directed actions. The neural basis of the development of demonstrably outcome-insensitive habitual actions in humans has not been previously characterized. In this experiment, we show that extensive training on a free-operant task reduces the sensitivity of participants' behavior to a reduction in outcome value. Analysis of functional magnetic resonance imaging data acquired during training revealed a significant increase in task-related cue sensitivity in a right posterior putamen-globus pallidus region as training progressed. These results provide evidence for a shift from goal-directed to habit-based control of instrumental actions in humans, and suggest that cue-driven activation in a specific region of dorsolateral posterior putamen may contribute to the habitual control of behavior in humans.

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Available from: Bernard W Balleine, Aug 28, 2015
    • "Thus, if the involvement of the putamen in S-R learning dissipates after a period of stable habitual performance, Tricomi et al. (2009) may not have sampled behavior beyond that stable period, whereas our accelerated habitual learning paradigm allowed us to do so. It is also worth noting , that, whereas Tricomi et al. (2009) reported effects in a small area in the very far posterior putamen, our effects extend throughout the right putamen and globus pallidus. One feature of the present results is that areas in which discriminatory neural activity was correlated with between-subject variation in devaluation insensitivity did not also show differential main effects in a comparison of S-R and R-O conditions. "
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    ABSTRACT: Considerable behavioral data indicate that operant actions can become habitual, as demonstrated by insensitivity to changes in the action-outcome contingency and in subjective outcome values. Notably, although several studies have investigated the neural substrates of habits, none has clearly differentiated the areas of the human brain that support habit formation from those that implement habitual control. We scanned participants with functional magnetic resonance imaging as they learned and performed an operant task in which the conditional structure of the environment encouraged either goal-directed encoding of the consequences of actions, or a habit-like mapping of actions to antecedent cues. Participants were also scanned during a subsequent assessment of insensitivity to outcome devaluation. We identified dissociable roles of the cerebellum and ventral striatum, across learning and test performance, in behavioral insensitivity to outcome devaluation. We also showed that the inferior parietal lobule (an area previously implicated in several aspects of goal-directed action selection, including the attribution of intent and awareness of agency) predicted sensitivity to outcome devaluation. Finally, we revealed a potential functional homology between the human subgenual cortex and rodent infralimbic cortex in the implementation of habitual control. In summary, our findings suggested a broad systems division, at the cortical and subcortical levels, between brain areas mediating the encoding and expression of action-outcome and stimulus-response associations. © 2015 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
    European Journal of Neuroscience 04/2015; DOI:10.1111/ejn.12897 · 3.67 Impact Factor
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    • "In contrast, if the habit system has gained control over action, an individual should continue to respond in both valued and devalued conditions at a cost of 1¢ per trial. To exclude the possibility that new learning contributed to devaluation test performance, outcomes were not shown to participants during the test stage (Figure 2A) (de Wit & Dickinson, 2009; Tricomi et al., 2009). Participants were warned about this change in task procedure, told that they would not longer see the result of their choices (i.e. "
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    ABSTRACT: Studies in humans and rodents suggest that behavior can at times be ‘goal-directed’, i.e. planned, and purposeful, and at times ‘habitual’, i.e. inflexible and automatically evoked by stimuli. Their distinction is central to conceptions of pathological compulsion, as in drug abuse and obsessive-compulsive disorder. Evidence for this distinction primarily comes from outcome devaluation studies, where the sensitivity of a previously learned behavior to motivational change is used to assay the dominance of habits vs. goal- directed actions. However, little is known about how habits and goal-directed control arise. Specifically, the present study sought to reveal the trial-by-trial dynamics of instrumental learning that promote, and protect against, developing habits. In two complementary experiments with independent samples, participants completed a sequential decision task that dissociates two computational learning mechanisms, model- based and model-free. We then tested for habits by devaluing one of the rewards that had reinforced behavior. In each case, we found that individual differences in model-based learning predicted the participants’ subsequent sensitivity to outcome devaluation, suggesting an associative mechanism underlying a bias toward habit formation in healthy individuals.
    Cognitive Affective & Behavioral Neuroscience 02/2015; 15(3). DOI:10.3758/s13415-015-0347-6 · 3.21 Impact Factor
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    • "Despite the limitations discussed below, we suspect that our finding of progressive putaminal engagement reflects the formation of S-R associations rather than other types of associations. Previous human studies linked the posterolateral putamen [Knowlton et al., 1996] to habit formation, showing that putaminal activation at the onset of task blocks increased over the course of each training day and across days of training [Tricomi et al., 2009], and to valuation following extensive training [Wunderlich et al., 2012]. We instead focused on rapidly acquired associations that likely represent an early phase of habit learning. "
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    ABSTRACT: Many computational models assume that reinforcement learning relies on changes in synaptic efficacy between cortical regions representing stimuli and striatal regions involved in response selection, but this assumption has thus far lacked empirical support in humans. We recorded hemodynamic signals with fMRI while participants navigated a virtual maze to find hidden rewards. We fitted a reinforcement-learning algorithm to participants' choice behavior and evaluated the neural activity and the changes in functional connectivity related to trial-by-trial learning variables. Activity in the posterior putamen during choice periods increased progressively during learning. Furthermore, the functional connections between the sensorimotor cortex and the posterior putamen strengthened progressively as participants learned the task. These changes in corticostriatal connectivity differentiated participants who learned the task from those who did not. These findings provide a direct link between changes in corticostriatal connectivity and learning, thereby supporting a central assumption common to several computational models of reinforcement learning. Hum Brain Mapp, 2014. © 2014 Wiley Periodicals, Inc.
    Human Brain Mapping 02/2015; 36(2). DOI:10.1002/hbm.22665 · 6.92 Impact Factor
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