The anterior cingulate gyrus signals the net value of others' rewards

Abstract

Evaluating the costs and benefits of our own choices is central to most forms of decision-making and its mechanisms in the brain are becoming increasingly well understood. To interact successfully in social environments, it is also essential to monitor the rewards that others receive. Previous studies in nonhuman primates have found neurons in the anterior cingulate cortex (ACC) that signal the net value (benefit minus cost) of rewards that will be received oneself and also neurons that signal when a reward will be received by someone else. However, little is understood about the way in which the human brain engages in cost-benefit analyses during social interactions. Does the ACC signal the net value (the benefits minus the costs) of rewards that others will receive? Here, using fMRI, we examined activity time locked to cues that signaled the anticipated reward magnitude (benefit) to be gained and the level of effort (cost) to be incurred either by a subject themselves or by a social confederate. We investigated whether activity in the ACC covaries with the net value of rewards that someone else will receive when that person is required to exert effort for the reward. We show that, although activation in the sulcus of the ACC signaled the costs on all trials, gyral ACC (ACC(g)) activity varied parametrically only with the net value of rewards gained by others. These results suggest that the ACC(g) plays an important role in signaling cost-benefit information by signaling the value of others' rewards during social interactions.

Keywords: cingulate; effort; empathy; reward; social; value.

Figure 1.

A, Trial structure. Participants performed trials that began with a color-coded instruction cue. Blue indicated that the subjects (first person) would perform button presses to receive a financial reward and brown indicated that the button presses would be performed by a confederate (third person). The position of crosshairs on these stimuli indicated the level of reward available (16 or 4 p) and the number of button presses required for reward receipt (2, 3, 8, or 12). After this was the effort period, in which the required button presses were made by cancelling out highlighted squares that each corresponded to one button on a keypad. After this was a cue that indicated the number of button presses (“cancellation cue”) and then a trigger cue. At the time of the trigger cue, on the third-person trials, the subjects were required to indicate how much reward the third person would receive (16, 4, or 0 p if they made the incorrect number of button presses). After this, there was feedback for performance on this judgment task and, finally, there was feedback for the individual who performed the effort task. The instruction cue onsets were jittered over the first two scans (TRs) of each trial to sample evoked hemodynamic responses time locked to these events evenly and independently from the other elements in the trials. The dotted lines indicate the cue that was jittered over the first two TRs. B, Experimental design displayed in a table showing the 16 different conditions in the experiment. Net value was calculated as the level of reward divided by the level of effort. These were then log transformed to create the parameters used for the parametric analysis.

Figure 2.

Behavioral results. A, Behavioral results for the performance of the effort task by the subjects themselves. Behavioral performance was high for each effort level and showed no significant differences between effort conditions. B, Performance at judging the level of reward that was being received by the confederate for each of the six net value levels. A repeated-measures ANOVA showed no difference in performance by net value. There was also no effect of effort or reward on the task accuracy.

Figure 3.

fMRI results. Activity shown in the ACC_g (A) covaried with the net value of the rewards. B, C, β-coefficients (parameter estimates) (B) from the parametric analysis and perstimulus time histogram plots (C) of activity from the peak ACC_g voxel. It is important to note that the β-coefficients from the parametric analysis reflect only the unique variance of a regressor. Therefore, the absence of a significant β-coefficient for the effort parameter in the ACC_g suggests that activity in this region cannot be explained by the unique variance of the effort parameter. However, as can be seen in the PSTH plot, ACC_g activity is modulated by both the effort level and the reward level. This supports the notion that activity in this portion of the ACC_g covaries with the net value of another's reward. D, Activity shown in the ACC_s that covaried with the effort level on both the first-person and third-person trials. E, Parameter estimates from the peak ACC_s voxel. F, Activity shown in the NA that covaried with the net-value on the first-person trials only. G, Parameter estimates from the peak NA voxel. All error bars reflect SEM.