Reward reduces conflict by enhancing attentional control and biasing visual cortical processing

Abstract

How does motivation interact with cognitive control during challenging behavioral conditions? Here, we investigated the interactions between motivation and cognition during a response conflict task and tested a specific model of the effect of reward on cognitive processing. Behaviorally, participants exhibited reduced conflict during the reward versus no-reward condition. Brain imaging results revealed that a group of subcortical and fronto-parietal regions was robustly influenced by reward at cue processing and, importantly, that cue-related responses in fronto-parietal attentional regions were predictive of reduced conflict-related signals in the medial pFC (MPFC)/ACC during the upcoming target phase. Path analysis revealed that the relationship between cue responses in the right intraparietal sulcus (IPS) and interference-related responses in the MPFC during the subsequent target phase was mediated via signals in the left fusiform gyrus, which we linked to distractor-related processing. Finally, reward increased functional connectivity between the right IPS and both bilateral putamen and bilateral nucleus accumbens during the cue phase, a relationship that covaried with across-individual sensitivity to reward in the case of the right nucleus accumbens. Taken together, our findings are consistent with a model in which motivationally salient cues are employed to upregulate top-down control processes that bias the selection of visual information, thereby leading to more efficient stimulus processing during conflict conditions.

Figure 1

Response-conflict paradigm and behavioral data. Subjects performed a response conflict task under two motivational contexts: (A) during the reward condition (shown here), a cue stimulus (“$20”) signaled that participants would be rewarded for fast and correct performance; during the control condition (not shown here), a cue stimulus (“$00”) signaled that no reward was involved. Following a variable-length delay, a target stimulus containing a picture of a house or building was shown together with a task-irrelevant word (an incongruent condition is illustrated here). After the target stimulus, subjects were informed about the potential reward and about the total number of points accrued. Finally, a variable-length delay ended the trial. (B) Plot of interference (incongruent vs. neutral) and facilitation (congruent vs. neutral) reaction time scores illustrating the interaction patterns. C, congruent trials; I, incongruent trials; N, neutral trials. Error bars represent the standard error of the mean.

Figure 2

Hypothesized network interactions. (A) The relationship between attentional control implemented in fronto-parietal cortex during the cue phase, and conflict-related activity in medial PFC during the subsequent target phase was hypothesized to be mediated via the amount of target/distractor processing in visual cortex. (B) We also hypothesized that the functional coupling between fronto-parietal cortex and subcortical regions involved in reward processing would be affected by motivational context. PFC, prefrontal cortex.

Figure 3

Cue-related responses. Increased evoked responses to reward relative to no-reward were observed across fronto-parietal cortex and subcortical regions. MPFC, medial prefrontal cortex; FEF, frontal eye field; IPS, intraparietal sulcus; MFG, middle frontal gyrus; SMA/pre-SMA, supplementary motor area/ pre-supplementary motor area. The color scale represents p-values corrected for multiple comparisons via false discovery rate.

Figure 4

Target-related responses. (A) Regions that showed significant motivation (reward, no-reward) x interference (incongruent, neutral) interactions. MPFC, medial prefrontal cortex; IPS, intraparietal sulcus; MFG, middle frontal gyrus; AI, anterior insula. (B) Plot of interference (incongruent vs. neutral) and facilitation (congruent vs. neutral) effects in the medial prefrontal cortex ROI illustrating the interaction patterns. (C) Plot of interference (incongruent vs. neutral) and facilitation (congruent vs. neutral) effects in the left fusiform gyrus ROI illustrating the interaction patterns. C, congruent trials; I, incongruent trials; N, neutral trials. Error bars in panels B and C represent the standard error of the mean.

Figure 5

Relationship between cue- and target-phase responses. The scatter plot illustrates the relationship between cue-related responses in the right IPS ROI and conflict-related responses in the medial prefrontal cortex ROI. Increased differential responses during the cue phase were linked to decreased conflict-related responses during the subsequent target phase. The linear fit is shown for illustration purposes. IPS, intraparietal sulcus; MPFC, medial prefrontal cortex; Rewd, reward condition; No-Rewd, no-reward condition.

Figure 6

Network analysis. The relationship between cue-related responses in the right IPS (X: initial variable) and target-related responses in the medial prefrontal cortex (Y: outcome variable) was mediated via the left fusiform gyrus (M: mediator/intervening variable). The X, Y, and M variables employed in the analysis involved contrast or interaction terms, as indicated in red font. The letters a, b, c, c’, refer to estimated path coefficients (see SI Text). FG, fusiform gyrus; IPS, intraparietal sulcus; MPFC, medial prefrontal cortex; Rewd, reward condition; No-Rewd, no-reward condition; I, incongruent trial; N, neutral trial. *P < .05, **P < .01, ***P < .005, two-tailed. The dotted line indicates a path that was not statistically significant after the mediator was taken into account.

Figure 7

Functional connectivity. (A) Regions exhibiting stronger functional connectivity with the right IPS ROI during the cue-phase (reward vs. no-reward). (B) The scatter plot illustrates the trial-by-trial relationship between right IPS and right nucleus accumbens signals during the reward (red dots and line) and no-reward (green dots and line) conditions. Data are illustrated for one individual. The lines are included for illustration purposes and are linear fits to the data. IPS, intraparietal sulcus; NAcc, nucleus accumbens. (C) The scatter plot illustrates the relationship between BAS-drive scores and functional connectivity between right IPS and right nucleus accumbens. Participants with higher BAS-drive scores exhibited increased functional coupling. The linear fit to the data is included for illustration purposes.