Common and distinct networks underlying reward valence and processing stages: a meta-analysis of functional neuroimaging studies

Abstract

To better understand the reward circuitry in human brain, we conducted activation likelihood estimation (ALE) and parametric voxel-based meta-analyses (PVM) on 142 neuroimaging studies that examined brain activation in reward-related tasks in healthy adults. We observed several core brain areas that participated in reward-related decision making, including the nucleus accumbens (NAcc), caudate, putamen, thalamus, orbitofrontal cortex (OFC), bilateral anterior insula, anterior cingulate cortex (ACC) and posterior cingulate cortex (PCC), as well as cognitive control regions in the inferior parietal lobule and prefrontal cortex (PFC). The NAcc was commonly activated by both positive and negative rewards across various stages of reward processing (e.g., anticipation, outcome, and evaluation). In addition, the medial OFC and PCC preferentially responded to positive rewards, whereas the ACC, bilateral anterior insula, and lateral PFC selectively responded to negative rewards. Reward anticipation activated the ACC, bilateral anterior insula, and brain stem, whereas reward outcome more significantly activated the NAcc, medial OFC, and amygdala. Neurobiological theories of reward-related decision making should therefore take distributed and interrelated representations of reward valuation and valence assessment into account.

Figure 1

Concordance of brain activation from the ALE analyses. A. Core network activated by all contrasts/experiments. B. Overlay of brain areas separately involved in positive versus negative reward processing. C. Overlay of brain areas individually activated by different reward processing stages, anticipation, outcome, and evaluation. D. Direct contrast of brain activation between positive and negative reward processing. E. Direct contrast of brain activation between reward anticipation and outcome.

Figure 2

Concordance of brain activation from the PVM analyses. A. Core network activated by all contrasts/experiments. B. Overlay of brain areas separately involved in positive versus negative reward processing. C. Overlay of brain areas individually activated by different reward processing stages, anticipation, outcome, and evaluation. D. Direct contrast of brain activation between positive and negative reward processing. E. Direct contrast of brain activation between reward anticipation and outcome.

Figure 3

A schematic framework illustrates the roles of core brain areas involved in different aspects of reward-related decision making. The grid pattern denotes the medial orbitofrontal cortex encoding positive valence; the dash pattern denotes the anterior insula, lateral orbitofrontal cortex, anterior cingulate cortex, and amygdala encoding negative valence; the wave pattern denotes the ventral striatum encoding both positive and negative valence; the diamond pattern denotes the frontoparietal network being involved in information integration.