Influence of motivation on control hierarchy in the human frontal cortex

Abstract

The frontal cortex mediates cognitive control and motivation to shape human behavior. It is generally observed that medial frontal areas are involved in motivational aspects of behavior, whereas lateral frontal regions are involved in cognitive control. Recent models of cognitive control suggest a rostro-caudal gradient in lateral frontal regions, such that progressively more rostral (anterior) regions process more complex aspects of cognitive control. How motivation influences such a control hierarchy is still under debate. Although some researchers argue that both systems work in parallel, others argue in favor of an interaction between motivation and cognitive control. In the latter case it is yet unclear how motivation would affect the different levels of the control hierarchy. This was investigated in the present functional MRI study applying different levels of cognitive control under different motivational states (low vs high reward anticipation). Three levels of cognitive control were tested by varying rule complexity: stimulus-response mapping (low-level), flexible task updating (mid-level), and sustained cue-task associations (high-level). We found an interaction between levels of cognitive control and motivation in medial and lateral frontal subregions. Specifically, flexible updating (mid-level of control) showed the strongest beneficial effect of reward and only this level exhibited functional coupling between dopamine-rich midbrain regions and the lateral frontal cortex. These findings suggest that motivation differentially affects the levels of a control hierarchy, influencing recruitment of frontal cortical control regions depending on specific task demands.

Keywords: cognitive control; control hierarchy; fMRI; lateral frontal cortex; motivation; reward.

Figure 1.

Experimental design. A, Rule structure of the experiment. Digits were judged according to one of two tasks: Magnitude (>5?) and parity (odd or even?). Judgment was given with the index or middle finger. Low-level control: one task (e.g., Magnitude) was conducted in several blocks. Mid-level control: type of task was triggered by the color of the digit. Color 1 = magnitude and color 2 = parity. High-level control: An additional cue (triangle) determined the type of color-cue task association. Triangle with upward-tip: Color 1 = magnitude and color 2 = parity. Triangle with downward-tip: Color 1 = parity and color 2 = magnitude. Three levels of cognitive control were combined with low reward (left) and high reward (right). Low reward: participants earned 1 cent per correctly executed task. High reward: participants earned 15 cents. B, Examples for each of the six experimental conditions: In each condition, mini-blocks (MB) consisting of four consecutive trials were presented. Motivation cues (“1 cent” or “15 cents”) were always shown throughout the mini-block. Cognitive control level 1: Each MB comprised four magnitude (M) or four parity (P) tasks. Cognitive control level 2: M and P tasks were presented in random order in each MB. Digit-color (blue or yellow) determined the type of task. Cognitive control level 3: A triangle in front of the MB triggered the type of cue-task association. Upward-tip: green = P and red = M. Downward-tip: green = M and red = M.

Figure 2.

Reaction times analysis. Analysis of reaction times revealed a Cognition × Motivation interaction. A, Reaction times separately for the six conditions. LL = low reward low level, HL = high reward low level, LM = low reward middle level, HM = high reward middle level, LH = low reward high level, HH = high reward high level. B, Shown here is the beneficial effect of motivation separately for the three levels of cognitive control. High reaction times differences (low minus high motivation trials) indicate faster responses for high motivation trials and thus a benefit from reward.

Figure 3.

Activation pattern of whole brain analyses. A, Left, Main effect of Cognition. Each cognitive control condition collapsed across low and high motivation conditions. Middle, Main effect of Motivation. High versus low motivation collapsed across cognitive control conditions. Right, Interaction of Cognition and Motivation. Shown here and in subsequent figures are active clusters that surpassed a threshold of p < 0.001 (uncorrected) and 10 consecutive voxels per cluster. FWE-corrected values and coordinates are shown in the tables below. B, Motivation comparisons (i.e., high reward versus low reward) separately for the three levels of cognitive control. Left, Motivation effect in low-level cognitive control. Middle, Motivation effect in mid-level cognitive control. Right, Motivation effect in high-level cognitive control (no significant activation). C, Cognition comparisons collapsed across low and high motivation conditions. High-level versus mid-level (red) and mid-level versus low-level (blue) conditions are shown.

Figure 4.

ROI analyses. Percentage of BOLD signal change of ROIs in lateral frontal cortex: vPM, mIFS, aIFS, and SMA. Left, Cognition effects. Analysis of BOLD signal change for the three levels of cognitive control collapsed across low and high motivation conditions. Middle column, Motivation effects. Analysis of BOLD signal change for low and high motivation collapsed across three levels of cognitive control. Right column, Interaction of Cognition and Motivation. Difference between high and low motivation BOLD signal change separately for the three levels of cognitive control.

Figure 5.

Correlation and PPI analysis. A, Correlation between individual behavioral and BOLD signal change in mid-level of cognitive control. The x-axis shows individual (i.e., for each participant) behavioral difference between high and low motivation conditions separately for the mid-level control condition. High values relate to strong behavioral effects of motivation. The y-zxis shows individual BOLD signal difference between high and low motivation conditions separately for the mid-level control condition. High values relate to higher activity for motivation. B, PPI analysis. Left, Results of the PPI analysis on mid-level cognitive control condition (high vs low motivation) with midbrain as seed region. Note that we found no significant effect on the analysis in low-level and high-level cognitive control conditions. Right, Correlation between individual connectivity values of IFJ and individual behavioral values (i.e., reaction time differences between high and low motivation conditions in mid-level cognitive control condition).