Elsevier

Brain Research Reviews

Volume 59, Issue 1, November 2008, Pages 164-184
Brain Research Reviews

Review
Functional neuroimaging of reward processing and decision-making: A review of aberrant motivational and affective processing in addiction and mood disorders

https://doi.org/10.1016/j.brainresrev.2008.07.004Get rights and content

Abstract

The adequate integration of reward- and decision-related information provided by the environment is critical for behavioral success and subjective well being in everyday life. Functional neuroimaging research has already presented a comprehensive picture on affective and motivational processing in the healthy human brain and has recently also turned its interest to the assessment of impaired brain function in psychiatric patients. This article presents an overview on neuroimaging studies dealing with reward processing and decision-making by combining most recent findings from fundamental and clinical research. It provides an outline on the neural mechanisms guiding context-adequate reward processing and decision-making processes in the healthy brain, and also addresses pathophysiological alterations in the brain's reward system that have been observed in substance abuse and mood disorders, two highly prevalent classes of psychiatric disorders. The overall goal is to critically evaluate the specificity of neurophysiological alterations identified in these psychiatric disorders and associated symptoms, and to make suggestions concerning future research.

Introduction

Reward is no unitary concept, but subsumes several components including learning-related, motivational, affective and decisional aspects (Chau et al., 2004). Organisms form predictions, compare different reward opportunities with regard to their relative value and balance immediate reward with long-term utility to guarantee overall behavioral success. In the healthy brain the integration of reward-related information is ensured by several cortical and subcortical regions that form the brain's reward circuit, which is also involved in the selection and initiation of goal-directed behavior (O'Doherty, 2004). Adaptive decision-making further relies on regions that represent higher-order cognitive control processes (e.g., planning) and help to balance affectively guided impulsive choice and rational future-oriented considerations in order to maximize long-term behavioral success (Trepel et al., 2005).

Disturbances within the reward system have detrimental effects on behavior. Especially mood disorders and substance abuse disorders have already been reported to involve overt behavioral deficits in emotional processing leading to abnormal motivational and affective processing. Recent neuroimaging studies have provided a useful means that allowed to relate these overt deficits to their underlying neural substrates and to identify specific regional disturbances within the reward system of psychiatric patients. Nevertheless, to completely understand pathophysiological alterations it is also necessary to be aware of the neurophysiology of reward processing and decision-making in the healthy brain. This review will therefore provide a brief outline on brain regions that in the healthy brain predict rewards, sense rewarding outcomes, process them in a context-sensitive way and finally decide upon the actions that lead to the direct acquisition of reward by also balancing it with long-term reward utility. We will thereby briefly address recent functional neuroimaging studies on healthy human subjects, before in a second step we will deal with their relevance for the pathophysiology of psychiatric disorders. The focus will be on substance abuse disorders and mood disorders, two highly prevalent classes of psychiatric disorders, which can be characterized by overt motivational deficits, disordered affective processing and impairments in decision-making. The aim of this article is to review and evaluate neuroimaging findings from the last decade with regard to their contribution to the understanding of pathophysiological processes and their disorder-related specificity regarding alterations in the reward system. From this, we will be able to derive useful suggestions for future neuroimaging research by also pointing to potential interconnections with other experimental approaches (e.g., psychopharmacological research).

Section snippets

Learning to predict reward

The prospective organization of goal-directed behavior requires the correct prediction of when and where rewards will occur. Decisive information for the formation of such predictions has thereby been assumed to be mainly derived from the observation of environmental regularities (e.g., the contingency between a certain action and its outcome; O'Doherty, 2004). As the major source for the release of a neural teaching signal providing the organism with important information on changing reward

Representation of reward and punishment—‘relevance detectors’ in the brain

Besides the establishment of predictions of when and where rewards will occur, adaptive behavior requires the ability to represent the current motivational value of available rewards, which permits context-sensitive behavioral choices between different rewards. Within the human brain's reward circuit, the OFC has thereby been most consistently found to represent the rewarding outcomes and the relative value of reinforcers (O'Doherty, 2004). Particularly, activations in posterior parts of the

Parsing reward—Affective value and motivational significance

The existence of valence-independent ‘relevance detectors’ implies that it may be critical to make a clear distinction between the affective value of a stimulus (i.e., positive or negative) and its actual motivational significance for the organism. Although these two components usually occur collectively in the environment, at least in animals there is evidence that they recur on different neural substrates. Dopamine has been assumed to represent the motivational ‘wanting’ component of reward

Deciding advantageously—Reversal-learning, prospective planning and impulsive choice

Decision-making refers to the process of forming preferences, selecting and executing actions, as well as evaluating (possible or anticipated) outcomes (Ernst and Paulus, 2005). It requires the ability to accurately evaluate elements of outcome, including motivational value, outcome predictability, and risk. On the most basic level, organisms base their behavioral decisions on simple stimulus–response–outcome associations. Significant changes in the motivational value of environmental stimuli

Implications for psychiatric disorders

Overt behavioral impairments of motivational and affective processing like an overvaluing of some reward categories (e.g., drugs in patients with substance use disorders) at the expense of others or a mood-congruent bias towards a certain category of affective stimuli (e.g., sad faces in depressives) have been reported to significantly compromise everyday life of psychiatric patients. Despite small sample sizes and obvious confounds in clinical populations in comparison to healthy control

Substance (ab)use disorders

Addiction may be best described as a pathology of incentive motivation and behavioral control. As the most prominent behavioral feature, patients commonly exhibit a decreased ability to control the desire to obtain drugs, despite knowledge about the aversive consequences following drug intake or the low expectation of actual pleasure expected from the drug (see Schoenbaum et al., 2006). The compulsive character of drug seeking, the obvious lack of inhibitory control and the lacking ability to

Mood disorders—Changes in motivational relevance and affective processing

Mood disorders like major depressive and bipolar disorder (BD) have been characterized by significant changes in both motivational and affective processing (see Davidson et al., 2003a, Davidson et al., 2003b, Leppänen, 2006). Dominated by persistent dysphoric emotions and thoughts (e.g., anhedonia) – even in the absence of acute stressors – depressive patients have been reported to exhibit a decreased motivation to seek and a reduced ability to experience reward (Drevets, 2001, Chau et al., 2004

General conclusion

Context-sensitive reward processing and adaptive decision-making require the intact interplay between various cortical and subcortical regions that form the brain's reward circuit. Disturbances within this network have been reported in all of the psychiatric disorders reviewed above, even in patients without overt behavioral deficits. Both patients with substance dependence and mood disorders thereby showed a more or less consistent motivational bias towards certain stimulus categories (in mood

Limitations of ALE

ALE provides a useful tool that has many advantages over label-based reviews (see Laird et al., 2005b for a detailed discussion), but nevertheless suffers from some potential limitations that have not been overcome yet. For instance, ALE neither provides a weighting factor for the number of subjects in each study nor for the different voxel heights (z-values) and spatial extents of clusters in the studies included as data basis. In addition, this method does not account for the proportion of

References (166)

  • ChenC.H. et al.

    Explicit and implicit facial affect recognition in manic and depressed States of bipolar disorder: a functional magnetic resonance imaging study

    Biol. Psychiatry

    (2006)
  • ChristodoulouT. et al.

    The relationship of impulsivity to response inhibition and decision-making in remitted patients with bipolar disorder

    Eur. Psychiatr.

    (2006)
  • DavidsonM.C. et al.

    Differential cingulate and caudate activation following unexpected nonrewarding stimuli

    Neuroimage

    (2004)
  • DrevetsW.C.

    Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders

    Curr. Opi. Neurobiol.

    (2001)
  • DrevetsW.C. et al.

    Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria

    Biol. Psychiatry

    (2001)
  • ElliottR. et al.

    Abnormal ventral frontal response during performance of an affective go/no go task in patients with mania

    Biol. Psychiatry

    (2004)
  • ElliottR. et al.

    Role of the orbitofrontal cortex in reinforcement processing and inhibitory control: evidence from functional magnetic resonance imaging studies in healthy human subjects

    Int. Rev. Neurobiol.

    (2005)
  • ErnstM. et al.

    Neurobiology of decision making: a selective review from a neurocognitive and clinical perspective

    Biol. Psychiatry

    (2005)
  • FitzgeraldD.A. et al.

    Beyond threat: amygdala reactivity across multiple expressions of facial affect

    Neuroimage

    (2006)
  • GlascherJ. et al.

    Formal learning theory dissociates brain regions with different temporal integration

    Neuron

    (2005)
  • GoldsteinR.Z. et al.

    Subjective sensitivity to monetary gradients is associated with frontolimbic activation to reward in cocaine abusers

    Drug and Alcohol Dependence

    (2007)
  • HorvitzJ.C.

    Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events

    Neuroscience

    (2000)
  • JensenJ. et al.

    Direct activation of the ventral striatum in anticipation of aversive stimuli

    Neuron

    (2003)
  • JuckelG. et al.

    Dysfunction of ventral striatal reward prediction in schizophrenia

    Neuroimage

    (2006)
  • KeedwellP.A. et al.

    The neural correlates of anhedonia in major depressive disorder

    Biol. Psychiatry

    (2005)
  • KeedwellP.A. et al.

    A double dissociation of ventromedial prefrontal cortical responses to sad and happy stimuli in depressed and healthy individuals

    Biol. Psychiatry

    (2005)
  • KirschP. et al.

    Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study

    Neuroimage

    (2003)
  • KnutsonB. et al.

    A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI

    Neuroimage

    (2003)
  • KringelbachM.L. et al.

    Neural correlates of rapid reversal learning in a simple model of human social interaction

    Neuroimage

    (2003)
  • KumariV. et al.

    Neural abnormalities during cognitive generation of affect in treatment-resistant depression

    Biol. Psychiatry

    (2003)
  • LawrenceN.S. et al.

    Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression

    Biol. Psychiatry

    (2004)
  • LeppänenJ.M. et al.

    Depression biases the recognition of emotionally neutral faces

    Psychiatry Res.

    (2004)
  • MalhiG.S. et al.

    Reduced activation to implicit affect induction in euthymic bipolar patients: an fMRI study

    J. Affect. Disord.

    (2007)
  • Abler, B., Greenhouse, I., Ongur, D., Walter, H., Heckers, S., 2007b. Abnormal Reward System Activation in Mania....
  • AdinoffB. et al.

    Resting regional cerebral blood flow and gambling task performance in cocaine-dependent subjects and healthy comparison subjects

    Am. J. Psychiatr.

    (2003)
  • AhmedS.H.

    Addiction as compulsive reward prediction

    Science

    (2004)
  • AltshulerL. et al.

    Increased amygdala activation during mania: a functional magnetic resonance imaging study

    Am. J. Psychiatr.

    (2005)
  • AranaF.S. et al.

    Dissociable contributions of the human amygdala and orbitofrontal cortex to incentive motivation and goal selection

    J. Neurosci.

    (2003)
  • BalleineB.W. et al.

    The role of the dorsal striatum in reward and decision-making

    J. Neurosci.

    (2007)
  • BecharaA. et al.

    Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex

    Cerebral Cortex

    (1996)
  • BernsG.S. et al.

    Predictability modulates human brain response to reward

    J. Neurosci.

    (2001)
  • BrodyA.L. et al.

    Brain metabolic changes during cigarette craving

    Arch. Gen. Psychiatry

    (2002)
  • BushG. et al.

    Dorsal anterior cingulate cortex: a role in reward-based decision making

    Proc. Natl. Acad. Sci., U S A

    (2002)
  • CalderA.J. et al.

    Neuropsychology of fear and loathing

    Nat. Rev. Neurosci.

    (2001)
  • CanliT. et al.

    Brain activation to emotional words in depressed vs healthy subjects

    Neuroreport

    (2004)
  • ChangL. et al.

    Insights from recent positron emission tomographic studies of drug abuse and dependence

    Curr. Opin. Psychiatry

    (2006)
  • ChauD.T. et al.

    The neural circuitry of reward and its relevance to psychiatric disorders

    Curr. Psychiatry Rep.

    (2004)
  • CoffeyS.F. et al.

    Impulsivity and rapid discounting of delayed hypothetical rewards in cocaine-dependent individuals

    Exp. Clin. Psychopharmacol.

    (2003)
  • CoolsR. et al.

    Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging

    J. Neurosci.

    (2002)
  • CoxS.M. et al.

    Learning to like: a role for human orbitofrontal cortex in conditioned reward

    J. Neurosci.

    (2005)
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