Monetary Reward and Punishment to Response Inhibition Modulate Activation and Synchronization Within the Inhibitory Brain Network

Abstract

A reward or punishment can modulate motivation and emotions, which in turn affect cognitive processing. The present simultaneous functional magnetic resonance imaging-electroencephalography study examines neural mechanisms of response inhibition under the influence of a monetary reward or punishment by implementing a modified stop-signal task in a virtual battlefield scenario. The participants were instructed to play as snipers who open fire at a terrorist target but withhold shooting in the presence of a hostage. The participants performed the task under three different feedback conditions in counterbalanced order: a reward condition where each successfully withheld response added a bonus (i.e., positive feedback) to the startup credit, a punishment condition where each failure in stopping deduced a penalty (i.e., negative feedback), and a no-feedback condition where response outcome had no consequences and served as a control setting. Behaviorally both reward and punishment conditions led to significantly down-regulated inhibitory function in terms of the critical stop-signal delay. As for the neuroimaging results, increased activities were found for the no-feedback condition in regions previously reported to be associated with response inhibition, including the right inferior frontal gyrus and the pre-supplementary motor area. Moreover, higher activation of the lingual gyrus, posterior cingulate gyrus (PCG) and inferior parietal lobule were found in the reward condition, while stronger activation of the precuneus gyrus was found in the punishment condition. The positive feedback was also associated with stronger changes of delta, theta, and alpha synchronization in the PCG than were the negative or no-feedback conditions. These findings depicted the intertwining relationship between response inhibition and motivation networks.

Keywords: electroencephalography; functional magnetic resonance imaging; motivation; no-feedback; posterior cingulate gyrus; punishment; response inhibition; reward.

FIGURE 1

Experimental design. Presentation of stimuli during three conditions including no-feedback, reward, and punishment on the battlefield scene. (A) The no-feedback condition was used as a control condition. (B) In the reward condition, minimum compensation was started from 800 NTD, and each successful withheld response aggregates an additional bonus of 10 NTD (i.e., positive feedback). (C) In the punishment condition, each failure in withholding response aggregates a penalty of 10 NTD (i.e., negative feedback).

FIGURE 2

Different brain regions and related dipole source locations. Pre-SMA, pre-supplementary motor area; rMFG, right middle frontal gyrus; lIFG, left inferior frontal gyrus; PCG, posterior cingulate gyrus; rIPL, right inferior parietal lobe; lMOG, left middle occipital gyrus; rMOG, right middle occipital gyrus. Pre-SMA, lIFG, and rMFG are accomplished for response inhibition. PCG and rIPL are accomplished for emotion and motivation. Bilateral MOGs are accomplished for the analysis of visual stimuli. The small area shows the location of each participant’s dipole, while vast areas display the dipole locations of each cluster.

FIGURE 3

The response inhibition functions for no-feedback (blue), reward (green), and punishment (red) conditions. Error rates are plotted against five different SSDs centered around the cSSD that was adaptively determined for each individual participant and each condition, respectively. Error bars indicate standard error of the mean.

FIGURE 4

Difference of monetary fees in no-feedback, reward, and punishment conditions. Reward (i.e., positive feedback) shows greater fees then punishment (i.e., negative feedback), reward (+270 NTD) > Punishment (–221 NTD) fees. Asterisks indicate pairwise significance (p < 0.05) in t-tests between the no-feedback and reward conditions.

FIGURE 5

Response inhibition associated brain regions. Brain activations associated with the no-feedback (left panel), reward (middle panel), and punishment (right panel) are rendered on the axial slices ranging between 6 and 41 mm along the z-axis (spacing 4 mm between slices). The upper-left number next to each central slice indicates the z-axis, and the same set of slices are illustrated for all conditions. The right hemisphere is on the right side of the figure. The cluster threshold alpha was set at 0.01, and the voxel-wise threshold was fixed at p < 0.001.

FIGURE 6

Brain activation related to response inhibition. Left-panel: horizontal sections under reward–no-feedback; middle-panels: horizontal slices under reward–punishment and punishment–reward; right-panel: horizontal slices during the punishment–no-feedback condition. The upper left-hand number in addition to each segment indicates the z-axis. The voxel-wise threshold statistics were set at p < 0.001, and cluster threshold alpha <0.01. The right-hemisphere is on the right side of the picture.

FIGURE 7

Significant brain activation in the cortical regions, for reward–no-feedback, reward–punishment, the punishment–reward, and punishment–no-feedback condition under response inhibition (R, right hemisphere in the top two rows; L, left hemisphere in the bottom two rows). Please see Table 4 for the abbreviation of all brain regions.

FIGURE 8

The event-related spectral perturbation (ERSP) of the lIFG cluster during response inhibition. The solid red line shows go-stimulus onset. Yellow dashed line reveals stop signal onset. Purple dashed line presents response onset. Statistic at p < 0.01. Color bars indicate the scale of ERSP.

FIGURE 9

The ERSP analysis in the pre-SMA of the brain during response inhibition. Solid red line shows go cue onset. Yellow dashed line displays stop signal onset. Purple dashed line presents response cue onset. Statistic at p < 0.01. Color bars reveal the level of ERSP.

FIGURE 10

The ERSP analysis in the PCG of the brain during response inhibition. Solid red line shows go stimulus onset. Yellow dashed line reveals stop signal onset. Purple dashed line presents response onset. Statistic at p < 0.01. Color bars indicate the magnitude of ERSP.

FIGURE 11

The neural system shows the different brain activation and overlap area of the brain during no-feedback, reward, and punishment conditions under human inhibition. An overlap middle occipital gyrus (MOG) of the brain was investigated in three conditions.