A specific role for posterior dorsolateral striatum in human habit learning

Tricomi, Elizabeth; Balleine, Bernard W.; O’Doherty, John P.

doi:10.1111/j.1460-9568.2009.06796.x

Cited by 692 publications

(803 citation statements)

References 46 publications

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“…Similar findings hold in closely related paradigms in humans (Valentin et al, 2007;de Wit et al, 2009;Tricomi et al, 2009;Daw et al, 2011). The shift from early devaluation sensitivity to later devaluation insensitivity can be explained by the statistical properties of model-based and model-free systems, respectively.…”

Section: Motivational Shiftssupporting

confidence: 74%

The role of learning-related dopamine signals in addiction vulnerability

Huys

Tobler

Hasler

et al. 2014

Progress in Brain Research

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Psychostimulants such as methylphenidate (MPH) and antidepressants such as fluoxetine (FLX) are widely used in the treatment of various mental disorders or as cognitive enhancers. These medications are often combined, for example, to treat comorbid disorders. There is a considerable body of evidence from animal models indicating that individually these psychotropic medications can have detrimental effects on the brain and behavior, especially when given during sensitive periods of brain development. However, almost no studies investigate possible interactions between these drugs. This is surprising given that their combined neurochemical effects (enhanced dopamine and serotonin neurotransmission) mimic some effects of illicit drugs such as cocaine and amphetamine. Here, we summarize recent studies in juvenile rats on the molecular effects in the mid-and forebrain and associated behavioral changes, after such combination treatments. Our findings indicate that these combined MPH + FLX treatments can produce similar molecular changes as seen after cocaine exposure while inducing behavioral changes indicative of dysregulated mood and motivation, effects that often endure into adulthood. Tables: 2 References: 254 ABSTRACT Dopaminergic signals play a mathematically precise role in reward-related learning, and variations in dopaminergic signalling have been implicated in vulnerability to addiction. Here, we provide a detailed overview of the relationship between theoretical, mathematical and experimental accounts of phasic dopamine signalling, with implications for the role of learning-related dopamine signalling in addiction and related disorders. We describe the theoretical and behavioural characteristics of model-free learning based on errors in the prediction of reward, including step-by-step explanations of the underlying equations. We then use recent insights from an animal model that highlights individual variation in learning during a Pavlovian conditioning paradigm to describe overlapping aspects of incentive salience attribution and model-free learning. We argue that this provides a computationally coherent account of some features of addiction. CONTENTS

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Section: Motivational Shiftssupporting

confidence: 74%

The role of learning-related dopamine signals in addiction vulnerability

Huys

Tobler

Hasler

et al. 2014

Progress in Brain Research

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“…Converging lines of evidence, from lesion studies in rodents and human neuroimaging studies, demonstrate that these two processes rely on distinct neural networks, with the prefrontal cortex, the dorsomedial thalamus and the dorsomedial striatum supporting goal-directed action (Balleine and Dickinson, 1998;Corbit et al, 2003;Killcross and Coutureau, 2003;Yin et al, 2005;Valentin et al, 2007;de Wit et al, 2009) and the dorsolateral striatum subserving habitual instrumental action (Yin et al, 2004;Tricomi et al, 2009; for review, see Yin and Knowlton, 2006).…”

Section: Introductionmentioning

confidence: 99%

Concurrent Glucocorticoid and Noradrenergic Activity Shifts Instrumental Behavior from Goal-Directed to Habitual Control

Schwabe¹,

Tegenthoff²,

Höffken³

et al. 2010

Journal of Neuroscience

142

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Stress modulates instrumental action in favor of habitual stimulus-response processes that are insensitive to changes in outcome value and at the expense of goal-directed action-outcome processes. The neuroendocrine mechanism underlying this phenomenon is unknown. Here, we tested the hypothesis that concurrent glucocorticoid and noradrenergic activity bias instrumental behavior toward habitual performance. To this end, healthy men and women received hydrocortisone, the ␣2-adrenoceptor antagonist yohimbine or both orally before they were trained in two instrumental actions leading to two distinct food outcomes. After training, one of the outcomes was devalued by inviting participants to eat that food to satiety. A subsequent extinction test revealed whether instrumental performance was goal-directed or habitual. Participants that received hydrocortisone or yohimbine alone decreased responding to the devalued action in the extinction test, i.e., they behaved goal-directed. The combined administration of hydrocortisone and yohimbine, however, rendered participants' behavior insensitive to changes in the value of the goal (i.e., habitual). These findings demonstrate that the concerted action of glucocorticoids and noradrenergic activity shifts instrumental behavior from goal-directed to habitual control.

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“…Learning how to achieve a pleasant state or how to avoid an unpleasant state (i.e., instrumental learning) can be controlled by two anatomically and functionally distinct systems that operate in tandem (Adams, 1982;Balleine and Dickinson, 1991): (1) a goal-directed system that learns causal relationships between an action and the incentive value of the outcome and is supported by the medial prefrontal cortex, the dorsomedial striatum, and the dorsomedial thalamus (Balleine and Dickinson, 1998a;Corbit et al, 2003;Killcross and Coutureau, 2003;Yin et al, 2005;Valentin et al, 2007); and (2) a dorsolateral striatum-dependent habit system that encodes associations between a response and preceding stimuli, without any link to the outcome that is engendered by the response (Yin et al, 2004Tricomi et al, 2009;Balleine and O'Doherty, 2010).…”

Section: Introductionmentioning

confidence: 99%

Preventing the Stress-Induced Shift from Goal-Directed to Habit Action with a β-Adrenergic Antagonist

Schwabe

Höffken²,

Tegenthoff³

et al. 2011

J. Neurosci.

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Stress modulates instrumental action in favor of habit processes that encode the association between a response and preceding stimuli and at the expense of goal-directed processes that learn the association between an action and the motivational value of the outcome. Here, we asked whether this stress-induced shift from goal-directed to habit action is dependent on noradrenergic activation and may therefore be blocked by a ␤-adrenoceptor antagonist. To this end, healthy men and women were administered a placebo or the ␤-adrenoceptor antagonist propranolol before they underwent a stress or a control procedure. Shortly after the stress or control procedure, participants were trained in two instrumental actions that led to two distinct food outcomes. After training, one of the food outcomes was selectively devalued by feeding participants to satiety with that food. A subsequent extinction test indicated whether instrumental behavior was goal-directed or habitual. As expected, stress after placebo rendered participants' behavior insensitive to the change in the value of the outcome and thus habitual. After propranolol intake, however, stressed participants behaved, same as controls, goal-directed, suggesting that propranolol blocked the stress-induced bias toward habit behavior. Our findings show that the shift from goal-directed to habitual control of instrumental action under stress necessitates noradrenergic activation and could have important clinical implications, particularly for addictive disorders.

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A specific role for posterior dorsolateral striatum in human habit learning

Cited by 692 publications

References 46 publications

The role of learning-related dopamine signals in addiction vulnerability

The role of learning-related dopamine signals in addiction vulnerability

Concurrent Glucocorticoid and Noradrenergic Activity Shifts Instrumental Behavior from Goal-Directed to Habitual Control

Preventing the Stress-Induced Shift from Goal-Directed to Habit Action with a β-Adrenergic Antagonist

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