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A selective role for dopamine in stimulus-reward learning.

ABSTRACT: Individuals make choices and prioritize goals using complex processes that assign value to rewards and associated stimuli. During Pavlovian learning, previously neutral stimuli that predict rewards can acquire motivational properties, becoming attractive and desirable incentive stimuli. However, whether a cue acts solely as a predictor of reward, or also serves as an incentive stimulus, differs between individuals. Thus, individuals vary in the degree to which cues bias choice and potentially promote maladaptive behaviour. Here we use rats that differ in the incentive motivational properties they attribute to food cues to probe the role of the neurotransmitter dopamine in stimulus-reward learning. We show that intact dopamine transmission is not required for all forms of learning in which reward cues become effective predictors. Rather, dopamine acts selectively in a form of stimulus-reward learning in which incentive salience is assigned to reward cues. In individuals with a propensity for this form of learning, reward cues come to powerfully motivate and control behaviour. This work provides insight into the neurobiology of a form of stimulus-reward learning that confers increased susceptibility to disorders of impulse control.

SUBMITTER: Flagel SB

PROVIDER: S-EPMC3058375 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

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A selective role for dopamine in stimulus-reward learning.

Flagel Shelly B SB Clark Jeremy J JJ Robinson Terry E TE Mayo Leah L Czuj Alayna A Willuhn Ingo I Akers Christina A CA Clinton Sarah M SM Phillips Paul E M PE Akil Huda H

Nature 20101208 7328

Individuals make choices and prioritize goals using complex processes that assign value to rewards and associated stimuli. During Pavlovian learning, previously neutral stimuli that predict rewards can acquire motivational properties, becoming attractive and desirable incentive stimuli. However, whether a cue acts solely as a predictor of reward, or also serves as an incentive stimulus, differs between individuals. Thus, individuals vary in the degree to which cues bias choice and potentially pr ...[more]

PMID: 21150898

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Project description:In the DSM-5, psychiatric diagnoses are made based on self-reported symptoms and clinician-identified signs. Though helpful in choosing potential interventions based on the available regimens, this conceptualization of psychiatric diseases can limit basic science investigation into their underlying causes. The reward prediction error (RPE) hypothesis of dopamine neuron function posits that phasic dopamine signals encode the difference between the rewards a person expects and experiences. The computational framework from which this hypothesis was derived, temporal difference reinforcement learning (TDRL), is largely focused on reward processing rather than punishment learning. Many psychiatric disorders are characterized by aberrant behaviors, expectations, reward processing, and hypothesized dopaminergic signaling, but also characterized by suffering and the inability to change one's behavior despite negative consequences. In this review, we provide an overview of the RPE theory of phasic dopamine neuron activity and review the gains that have been made through the use of computational reinforcement learning theory as a framework for understanding changes in reward processing. The relative dearth of explicit accounts of punishment learning in computational reinforcement learning theory and its application in neuroscience is highlighted as a significant gap in current computational psychiatric research. Four disorders comprise the main focus of this review: two disorders of traditionally hypothesized hyperdopaminergic function, addiction and schizophrenia, followed by two disorders of traditionally hypothesized hypodopaminergic function, depression and post-traumatic stress disorder (PTSD). Insights gained from a reward processing based reinforcement learning framework about underlying dopaminergic mechanisms and the role of punishment learning (when available) are explored in each disorder. Concluding remarks focus on the future directions required to characterize neuropsychiatric disorders with a hypothesized cause of underlying dopaminergic transmission.

Project description:Orbitofrontal cortex (OFC), medial frontal cortex (MFC), and amygdala mediate stimulus-reward learning, but the mechanisms through which they interact are unclear. Here, we investigated how neurons in macaque OFC and MFC signaled rewards and the stimuli that predicted them during learning with and without amygdala input. Macaques performed a task that required them to evaluate two stimuli and then choose one to receive the reward associated with that option. Four main findings emerged. First, amygdala lesions slowed the acquisition and use of stimulus-reward associations. Further analyses indicated that this impairment was due, at least in part, to ineffective use of negative feedback to guide subsequent decisions. Second, the activity of neurons in OFC and MFC rapidly evolved to encode the amount of reward associated with each stimulus. Third, amygdalectomy reduced encoding of stimulus-reward associations during the evaluation of different stimuli. Reward encoding of anticipated and received reward after choices were made was not altered. Fourth, amygdala lesions led to an increase in the proportion of neurons in MFC, but not OFC, that encoded the instrumental response that monkeys made on each trial. These correlated changes in behavior and neural activity after amygdala lesions strongly suggest that the amygdala contributes to the ability to learn stimulus-reward associations rapidly by shaping encoding within OFC and MFC.SIGNIFICANCE STATEMENT Altered functional interactions among orbital frontal cortex (OFC), medial frontal cortex (MFC), and amygdala are thought to underlie several psychiatric conditions, many related to reward learning. Here, we investigated the causal contribution of the amygdala to the development of neuronal activity in macaque OFC and MFC related to rewards and the stimuli that predict them during learning. Without amygdala inputs, neurons in both OFC and MFC showed decreased encoding of stimulus-reward associations. MFC also showed increased encoding of the instrumental responses that monkeys made on each trial. Behaviorally, changes in neural activity were accompanied by slower stimulus-reward learning. The findings suggest that interactions among amygdala, OFC, and MFC contribute to learning about stimuli that predict rewards.

Dataset Information

A selective role for dopamine in stimulus-reward learning.

Publications

A selective role for dopamine in stimulus-reward learning.

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