Elsevier

Neuropsychologia

Volume 50, Issue 7, June 2012, Pages 1252-1266
Neuropsychologia

The role of the human ventral striatum and the medial orbitofrontal cortex in the representation of reward magnitude – An activation likelihood estimation meta-analysis of neuroimaging studies of passive reward expectancy and outcome processing

https://doi.org/10.1016/j.neuropsychologia.2012.02.007Get rights and content

Abstract

Reward maximization is a core motivation of every organism. In humans, several brain regions have been implicated in the representation of reward magnitude. Still, it is unclear whether identical brain regions consistently play a role in reward prediction and its consumption. In this study we used coordinate-based ALE meta-analysis to determine the individual roles of the ventral striatum (vSTR) and the medial orbitofrontal cortex (mOFC/VMPFC) in the representation of reward in general and of reward magnitude in particular. Specifically, we wanted to assess commonalities and differences in regional brain activation during the passive anticipation and consumption of rewards. Two independent meta-analyses of neuroimaging data from the past decade revealed a general role for the vSTR in reward anticipation and consumption. This was the case particularly when the consumed rewards occurred unexpectedly or were uncertain. In contrast, for the mOFC/VMPFC the present meta-analytic data suggested a rather specific function in reward consumption as opposed to passive anticipation. Importantly, when considering only coordinates that compared different reward magnitudes, the same parts of the vSTR and the mOFC/VMPFC showed concordant responses across studies, although areas of coherence were regionally more confined. These meta-analytic data suggest that the vSTR may be involved in both prediction and consumption of salient rewards, and may also be sensitive to different reward magnitudes, while the mOFC/VMPFC may rather process the magnitude during reward receipt. Collectively, our meta-analytic data conform with the notion that these two brain regions may subserve different roles in processing of reward magnitude.

Highlights

► ALE meta-analysis revealed regional differences for reward anticipation and consumption. ► Ventral striatum was generally activated by passive anticipation and receipt of reward. ► mOFC/VMPFC was specifically activated by reward receipt, but not by its prediction. ► Both ventral striatum and mOFC/VMPFC represent passive reward magnitude.

Introduction

Organisms preferentially seek out locations or initiate motor actions that promise the highest amount of reward. Animal studies have shown that expectations of different reward magnitudes significantly impact on behavioral choice (e.g., Flaherty & Mitchall, 1999). For example, animals performed more accurately in trials with larger rewards and consistently chose larger over smaller incentives (e.g., Cromwell & Schultz, 2003), also when being in a food-deprived state (Collier, 1982). In the same way, the expectancy for higher rewards improved tactile performance in humans and enhanced discrimination accuracy in subsequent trials (Pleger, Blankenburg, Ruff, Driver, & Dolan, 2008). Even when reward predictors were presented subliminally, the magnitude of the available reward influenced the physical effort exerted during the current trial (Pessiglione et al., 2007). These data thus suggest that reward magnitude may be one important driving source that energizes behavior.

Behavioral optimization in terms of reward maximization strongly depends on the neural capacity to represent the expected magnitude of each reward option and to compare the size of all available rewards (Kable & Glimcher, 2009). Reward magnitude is an objective property of reward value that refers to the invariant ratio of different reward sizes (i.e., “less versus more”; see Peters and Büchel, 2010, Schultz, 2006). The present meta-analysis was intended to further dip into the neural substrates involved in the representation of reward magnitude. Neuroimaging research from the past decade identified two functionally related brain regions that probably form the core network for processing of reward magnitude. One of these neural structures is the human ventral striatum (vSTR) (i.e., the brain region comprising the nucleus accumbens, ventral caudate nucleus and ventral putamen; Haber and Knutson, 2009, Haber and McFarland, 1999). Abundant neuroimaging evidence suggests that this brain region is preferentially activated by reliable predictors of reward (e.g., Cohen et al., 2005, Knutson et al., 2001b, Rademacher et al., 2010). Activity changes in the vSTR thereby specifically scaled with the magnitude of expected reward in both humans (e.g., Abler et al., 2009, Knutson et al., 2001a, Tobler et al., 2007, Yacubian et al., 2007) and non-human primates (Cromwell & Schultz, 2003), and ventral striatal activity was further predictive of subsequent behavioral performance (Cromwell and Schultz, 2003, Pleger et al., 2008). Apart from that, some studies that were interested in outcome-related brain activation also reported increased ventral striatal activation during reward consumption (e.g., Yacubian et al., 2006), whereby the observed increase also scaled with the magnitude of the currently received reward (e.g., Elliott, Friston, & Dolan, 2000). However, the consummatory response of the vSTR was more pronounced in situations in which reward was uncertain, namely when a reward occurred either unpredictably after a risky gamble (e.g., Cohen et al., 2005) or was presented randomly in a sequence of rewards and neutral stimuli (e.g., Berns, McClure, Pagnoni, & Montague, 2001). Finally, studies that tested for both anticipatory and outcome-related activation in the vSTR within the same experiment produced rather heterogeneous results. While some of these studies demonstrated a specific function for the vSTR in the anticipation of reward (e.g., Knutson, Fong, Bennett, Adams, & Hommer, 2003), others observed phase-independent activation in this brain region during both anticipatory and consummatory periods (e.g., Breiter et al., 2001, Kim et al., 2010). It therefore remains unclear whether activation in the vSTR can be consistently associated with the representation of reward magnitude across neuroimaging studies during both reward expectancy and its consumption.

The second brain region that has been implicated in reward valuation and in the representation of reward magnitude encompasses the medial orbitofrontal cortex and adjacent parts of the ventromedial prefrontal cortex (i.e., the mOFC/VMPFC). The majority of previous studies found increased activation in this brain region during the consummatory phase of reward processing (e.g., Cohen et al., 2005, Knutson et al., 2003). Activity in the medial OFC was thereby significantly enhanced for larger amounts of reward (e.g., Grabenhorst et al., 2010, O’Doherty et al., 2003a). In addition, a much small number of previous studies also reported medial orbitofrontal activation in response to passive reward predictors (Tobler, O’Doherty, Dolan, & Schultz, 2006) or during the anticipatory period in general (e.g., Rolls, McCabe, & Redoute, 2008), whereby activation scaled with the anticipated reward size (Smith et al., 2009). Yet, anticipatory reward-related activation during passive evaluation was by far more common in the lateral orbitofrontal cortex (e.g., Gottfried et al., 2003, Koeneke et al., 2008, O’Doherty et al., 2002, Schienle et al., 2009). In addition, more complex forms of reward valuation that require an integration of multiple dimensions including various decision costs (e.g., behavioral effort or temporal delay) and expected benefits (e.g., expected reward size) have been shown to activate the mOFC/VMPFC in numerous studies (see Peters & Büchel, 2010 and Grabenhorst & Rolls, 2011 for overview). For example Plassmann, O’Doherty, & Rangel (2007) found that the mOFC/VMPFC represented predicted reward value in a Becker–DeGroot–Marschak (BDM) auction during active decision making rather than during forced choice control trials. Finally, a positive deflection of medial orbitofrontal activity could also be observed during the relative down-regulation of negative affect (e.g., Diekhof et al., 2011a, Diekhof et al., 2011b) and during the evaluation of simulated or hypothetical rewards (e.g., Bray et al., 2010, Coricelli et al., 2005).1 In sum, the mOFC/VMPFC may thus contribute to the hedonic experience (and/or current mood) associated with processing of highly valued rewards (see Grabenhorst and Rolls, 2011, Kringelbach, 2005, Kringelbach and Rolls, 2004, Peters and Büchel, 2010).

Taken together, these previous neuroimaging findings suggest that the human vSTR and the mOFC/VMPFC represent the core system for the processing of reward in general, and of reward magnitude in particular. Still, the heterogeneity of previous findings to some extent precludes a conclusive judgment on the particular roles of these brain regions in either the passive anticipation or the consumption of rewards with different sizes. For this reason, it needs to be determined (1.) whether the vSTR was indeed consistently activated during passive reward prediction and also during reward receipt, (2.) whether its response also represents reward magnitude, and (3.) whether the medial OFC is activated during both passive reward prediction and outcome processing. Coordinate-based quantitative meta-analysis offers a useful tool to answer these questions by assessing the convergence of existing neuroimaging findings that used different reward tasks (Eickhoff et al., 2009, Laird et al., 2005a, Turkeltaub et al., 2002). The identification of the specific role of these brain regions in reward anticipation and consumption – independent of the disadvantages of study-specific characteristics (e.g., experimental design, stimulus modality, or data analysis technique) – may thereby further our understanding of the neural mechanisms underlying motivational drive.

Section snippets

Materials and methods

We performed a coordinate-based quantitative meta-analysis using the activation likelihood estimation (ALE) method (Eickhoff et al., 2009, Laird et al., 2005a, Turkeltaub et al., 2002 available at http://brainmap.org/ale/index.html). This analysis assessed the voxelwise correspondence of neuroimaging results from studies of reward processing. In particular, we wanted to examine the functional role of the vSTR and the medial OFC/VMPFC in the representation of reward magnitude during reward

Results

A systematic search of the PubMed database and application of the inclusion and exclusion criteria yielded a total of 24 relevant research articles (326 coordinates) for the anticipation phase and 46 relevant neuroimaging studies (549 coordinates) that reported reward-related hyperactivations from relevant contrasts during the outcome phase (see Table 1, Table 2). After exclusion of all coordinates that were derived from ROI analyses, 21 studies (307 coordinates) from the anticipation phase and

Discussion

In this study we used coordinate-based ALE meta-analysis to determine the individual roles of the vSTR and the mOFC/VMPFC in the passive representation of reward in general and of reward magnitude in particular. Specifically, we wanted to assess commonalities and differences in regional brain activation during the passive anticipation and consumption of rewards. A systematic search of the existing neuroimaging literature yielded a total of 875 relevant coordinates of which 768 coordinates

Conclusions

Taken together, the present meta-analytic findings demonstrate the important role of the human vSTR and the mOFC/VMPFC in the representation of reward during its passive prediction and consumption, and highlight the complementary functions of these brain regions that have close anatomical connections. In particular, our data underscore that different reward sizes (i.e., reward magnitude) may be represented by the vSTR during both passive anticipation and receipt of reward, while the mOFC/VMPFC,

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