Love is analogous to money in human brain: Coordinate-based and functional connectivity meta-analyses of social and monetary reward anticipation

Abstract

Both social and material rewards play a crucial role in daily life and function as strong incentives for various goal-directed behaviors. However, it remains unclear whether the incentive effects of social and material reward are supported by common or distinct neural circuits. Here, we have addressed this issue by quantitatively synthesizing and comparing neural signatures underlying social (21 contrasts, 207 foci, 696 subjects) and monetary (94 contrasts, 1083 foci, 2060 subjects) reward anticipation. We demonstrated that social and monetary reward anticipation engaged a common neural circuit consisting of the ventral tegmental area, ventral striatum, anterior insula, and supplementary motor area, which are intensively connected during both task and resting states. Functional decoding findings indicate that this generic neural pathway mediates positive value, motivational relevance, and action preparation during reward anticipation, which together motivate individuals to prepare well for the response to the upcoming target. Our findings support the common neural currency hypothesis by providing the first meta-analytic evidence to quantitatively show the common involvement of brain regions in both social and material reward anticipation.

Keywords: Functional decoding; Meta-analysis; Meta-analytic connectivity modeling; Monetary incentive delay task; Resting-state functional connectivity; Reward anticipation; Social reward.

Fig. 1.

Flow chart of the study selection process for the meta-analysis. SID, social incentive delay task; MID, monetary incentive delay task; fMRI, functional magnetic resonance imaging; PET, positron emission tomography.

Fig. 2.

Significant clusters from the main coordinate-based activation likelihood estimation meta-analysis (cluster-level family-wise error correction [P < 0.05] with a cluster-forming threshold of P < 0.001 using 10,000 permutations) for social reward anticipation, monetary reward anticipation, and their conjunction and contrasts. Consistent maximum for: (A) social reward anticipatation; (B) monetary reward anticipation; (C) the conjunction of social and monetary reward anticipation; (D) the contrasts of social and monetary reward anticipation. Brain regions showing higher activation in the anticipation of social reward are illustrated in red, whereas regions showing higher activation in the anticipation of monetary reward are illustrated in green. L, left; R, right.

Fig. 3.

Quantitative forward and reverse inference on each region identified in the conjunction analysis. Quantitative forward and reverse inference for: (A) left VS; (B) right VS; (C) VTA; (D) left AI; and (E) SMA.

Fig. 4.

Results for the task-based meta-analytic connectivity modeling (MACM) analyses, task-free resting-state functional connectivity (RSFC) analyses, and their conjunctions for the regions commonly involved in the social and monetary reward anticipation. (A) task-based connectivity; (B) task-free connectivity; (C) conjunction across all MACM maps; (D) conjunction across all RSFC maps; (E) conjunction across all MACM and RSFC maps. L, left; R, right; VS, ventral striatum; AI, anterior insula; VTA, ventral tegmental area; SMA, supplementary motor area.

Fig. 5.

Clustering on functional connectivity between regions identified in the contrast analyses. Full (below the diagonal) and partial (above the diagonal) correlation matrices were illustrated, with warmer colors denoting positive correlations and cooler colors denoting negative correlations. The location of each region was displayed at the top of each column. The background color of region label indicates the contrast of each region (blue = social > monetary; red = monetary > social). The spatial map of each subcluster is illustrated at the bottom. L, left; R, right; AI, anterior insula; SMA, supplementary motor area; dACC, dorsal anterior cingulate cortex; Thal, thalamus; Puta, putamen; Caud, caudate; MOG, middle occipital gyrus.

Fig. 6.

Quantitative forward and reverse inference on each subcluster identified in the hierarchical clustering. Quantitative forward and reverse inference for: (A) subcluster 1; (B) subcluster 2; (C) subcluster 3; and (D) subcluster 4.