Behavioral and neuroimaging evidence for overreliance on habit learning in alcohol-dependent patients

Sjoerds, Zsuzsika; Wit, Sanne de; Brink, Wim van den; Robbins, Trevor W.; Beekman, Aartjan T.F.; Penninx, Brenda W. J. H.; Veltman, Dick J.

doi:10.1038/tp.2013.107

Cited by 282 publications

(251 citation statements)

References 63 publications

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“…Hence these findings need to be treated with caution and require replication. Furthermore, while animal studies have convincingly shown a shift towards model-free choices in addiction, and indeed with alcohol [4,5,7], there have been only limited investigations to substantiate this in humans so far [23,27]. One reason may be that it has been difficult to measure these two systems in humans and often has required rather laborious tasks involving extended training [71,72].…”

Section: Discussionmentioning

confidence: 99%

“…This may hint at an effect of alcohol on more general measures of cognitive functioning [58]. Goal-directed control has also been associated with prefrontal areas [27,59,60]. This raises the question of whether drugs directly affect goal-directed choices or do so only secondarily to their effects on other, more general cognitive functions.…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, the goal-directed system is likely to depend on the kind of cognitive processes that are known to be impaired by alcohol [25,26]. Sjoerds et al [27] used an instructed devaluation in a slip of action tasks which involves complex relationships between stimuli, outcomes and responses. They found evidence for a shift towards habits in alcohol-dependent patients, which was accompanied by an increased functional magnetic resonance imaging signal in habit-related areas like the posterior putamen [28] and a decreased signal in goal-directed ventromedial prefrontal and anterior putamen areas [29,30,31], which parallels findings in animals [32].…”

Section: Introductionmentioning

confidence: 99%

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Model-Based and Model-Free Decisions in Alcohol Dependence

et al. 2014

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Background: Human and animal work suggests a shift from goal-directed to habitual decision-making in addiction. However, the evidence for this in human alcohol dependence is as yet inconclusive. Methods: Twenty-six healthy controls and 26 recently detoxified alcohol-dependent patients underwent behavioral testing with a 2-step task designed to disentangle goal-directed and habitual response patterns. Results: Alcohol-dependent patients showed less evidence of goal-directed choices than healthy controls, particularly after losses. There was no difference in the strength of the habitual component. The group differences did not survive controlling for performance on the Digit Symbol Substitution Task. Conclusion: Chronic alcohol use appears to selectively impair goal-directed function, rather than promoting habitual responding. It appears to do so particularly after nonrewards, and this may be mediated by the effects of alcohol on more general cognitive functions subserved by the prefrontal cortex. © 2014 S. Karger AG, Basel

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Model-Based and Model-Free Decisions in Alcohol Dependence

et al. 2014

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“…Indeed, decreased vmPFC activity has been observed in alcoholics showing elevated propensity toward habitual behavior (Sjoerds et al 2013). Others have suggested that the human vmPFC may be involved in the suppression of irrelevant information, potentially by integrating information from separable components of limbic corticostriatal circuitry (Nieuwenhuis and Takashima 2011).…”

Section: Potential For Translation To the Human Disease Statementioning

confidence: 99%

A unifying model of the role of the infralimbic cortex in extinction and habits

2014

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The infralimbic prefrontal cortex (IL) has been shown to be critical for the regulation of flexible behavior, but its precise function remains unclear. This region has been shown to be critical for the acquisition, consolidation, and expression of extinction learning, leading many to hypothesize that IL suppresses behavior as part of a "stop" network. However, this framework is at odds with IL function in habitual behavior in which the IL has been shown to be required for the expression and acquisition of ongoing habitual behavior. Here, we will review the current state of knowledge of IL anatomy and function in behavioral flexibility and provide a testable framework for a single IL mechanism underlying its function in both extinction and habit learning.Addiction is characterized both by the inability to terminate or reduce drug taking even in the face of adverse consequences and by chronic relapse to drug taking. Investigation into the neurobiological substrates of the loss of behavioral flexibility in addiction has relied heavily on animal models of addictive behavior, including habit and extinction learning paradigms that investigate distinct components of inflexible behavior.The prefrontal cortex (PFC) has repeatedly been identified as critical for the cognitive control of flexible actions (Jentsch and Taylor 1999;Everitt et al. 2008;George and Koob 2010;Willcocks and McNally 2012). Subregions of the PFC have distinct connectivity that likely underlies their separable roles in behavior. The infralimbic PFC (IL) has been shown to have a unique role in the development and expression of inflexible reward seeking. Interestingly, IL has been shown to have opposing effects on behavior when compared with the adjacent prelimbic PFC (PL) or, more broadly, the dorsomedial PFC (dmPFC). Perhaps most surprising are the apparently contradictory roles of IL in different measures of behavioral flexibility. In the current review, we discuss models of inflexible drug seeking and the role of IL in the regulation of these behavioral processes. In particular, we focus on the precise function of IL in the acquisition and extinction of drug seeking and the development and expression of habitual drug-seeking behavior. We propose a framework for reconciling the seemingly contradictory role of IL in the regulation of flexible reward seeking through the suppression of the ability of established action-outcome contingencies to guide behavior.

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“…After an outcome devaluation (e.g., through satiation), the MB system can change preferences quickly, but the MF system cannot. Individual variation in the balance between MB and MF decisions, with a shift toward MF and away from MB learning, is associated with addictive and impulsive traits in animals (Huys et al, 2014;Everitt & Robbins, 2005), and a bias has been reported in conditions such as addiction and obsessive-compulsive disorder where behavioral preferences persist against explicit desires (Voon et al, , 2015Gillan et al, 2011Gillan et al, , 2014Sebold et al, 2014;Sjoerds et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Don't Think, Just Feel the Music: Individuals with Strong Pavlovian-to-Instrumental Transfer Effects Rely Less on Model-based Reinforcement Learning

Sebold

Schad

Nebe

et al. 2016

Journal of Cognitive Neuroscience

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Behavioral choice can be characterized along two axes. One axis distinguishes reflexive, modelfree systems that slowly accumulate values through experience and a model-based system that uses knowledge to reason prospectively. The second axis distinguishes Pavlovian valuation of stimuli from instrumental valuation of actions or stimulus-action pairs. This results in four values and many possible interactions between them, with important consequences for accounts of individual variation. We here explored whether individual variation along one axis was related to individual variation along the other. Specifically, we asked whether individuals' balance between model-based and model-free learning was related to their tendency to show Pavlovian interferences with instrumental decisions. In two independent samples with a total of 243 participants, Pavlovian-instrumental transfer effects were negatively correlated with the strength of model-based reasoning in a two-step task. This suggests a potential common underlying substrate predisposing individuals to both have strong Pavlovian interference and be less model-based and provides a framework within which to interpret the observation of both effects in addiction. Abstract ■ Behavioral choice can be characterized along two axes. One axis distinguishes reflexive, model-free systems that slowly accumulate values through experience and a model-based system that uses knowledge to reason prospectively. The second axis distinguishes Pavlovian valuation of stimuli from instrumental valuation of actions or stimulus-action pairs. This results in four values and many possible interactions between them, with important consequences for accounts of individual variation. We here explored whether individual variation along one axis was related to individual variation along the other. Specifically, we asked whether individuals' balance between model-based and model-free learning was related to their tendency to show Pavlovian interferences with instrumental decisions. In two independent samples with a total of 243 participants, Pavlovianinstrumental transfer effects were negatively correlated with the strength of model-based reasoning in a two-step task. This suggests a potential common underlying substrate predisposing individuals to both have strong Pavlovian interference and be less model-based and provides a framework within which to interpret the observation of both effects in addiction. ■

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Behavioral and neuroimaging evidence for overreliance on habit learning in alcohol-dependent patients

Cited by 282 publications

References 63 publications

Model-Based and Model-Free Decisions in Alcohol Dependence

Model-Based and Model-Free Decisions in Alcohol Dependence

A unifying model of the role of the infralimbic cortex in extinction and habits

Don't Think, Just Feel the Music: Individuals with Strong Pavlovian-to-Instrumental Transfer Effects Rely Less on Model-based Reinforcement Learning

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