ReviewFunctional neuroimaging of reward processing and decision-making: A review of aberrant motivational and affective processing in addiction and mood disorders
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)
- et al.
Prediction error as a linear function of reward probability is coded in human nucleus accumbens
Neuroimage
(2006) - et al.
Anticipation of aversive stimuli activates extended amygdala in unipolar depression
J. Psychiatr. Res.
(2007) - et al.
Decision-making and addiction (part II): myopia for the future or hypersensitivity to reward?
Neuropsychologia
(2002) - et al.
Parsing reward
Trends in Neurosciences
(2003) - et al.
Orbitofrontal cortex dysfunction in abstinent cocaine abusers performing a decision-making task
Neuroimage
(2003) - et al.
Neural substrates of faulty decision-making in abstinent marijuana users
Neuroimage
(2005) - et al.
Neural systems and cue-induced cocaine craving
Neuropsychopharmacology
(2002) - et al.
Functional imaging of neural responses to expectancy and experience of monetary gains and losses
Neuron
(2001) - et al.
Attenuation of cue-induced cigarette craving and anterior cingulate cortex activation in bupropion-treated smokers: a preliminary study
Psychiatry Res.
(2004) - et al.
Neurobiological mechanisms in addictive and psychiatric disorders
The Psychiatric clinics of North America
(2004)