How do emotion and motivation direct executive control?

Abstract

Emotion and motivation have crucial roles in determining human behavior. Yet, how they interact with cognitive control functions is less understood. Here, the basic elements of a conceptual framework for understanding how they interact are introduced. More broadly, the 'dual competition' framework proposes that emotion and motivation affect both perceptual and executive competition. In particular, the anterior cingulate cortex is hypothesized to be engaged in attentional/effortful control mechanisms and to interact with several other brain structures, including the amygdala and nucleus accumbens, in integrating affectively significant signals with control signals in prefrontal cortex. An implication of the proposal is that emotion and motivation can either enhance or impair behavioral performance depending on how they interact with control functions.

Figures

Figure 1

Dual competition model framework. Affective significance impacts the flow of information processing both in a (a) `stimulus-driven' (note fearful face paired with shock as input) and a (b) `state-dependent' fashion based on motivational manipulations (note neutral face input). In both cases competition is suggested to occur at the perceptual and executive levels. Arrows denote functional pathways that do not necessarily map one-to-one to specific anatomical connections. Individual differences in state and/or trait anxiety and sensitivity to reward are expected to modulate the impact of affective significance on information processing.

Figure 2

Executive control and competition are viewed as involving multiple mechanisms, or resources. Larger unfilled ellipses represent executive control; smaller shapes represent processing resources. (a) When threat level is low, affective significance enhances the processing of the item. Other executive functions are not strongly impacted (smaller ellipses). (b-d) Processes are hypothesized to share resources, here called common-pool resources (smaller ellipses in bright blue), such that the engagement of one will detract from the processing of the other. Common-pool resources are proposed to be necessary for general functions of attentional/effortful control. (b) High-threat emotion-laden stimuli will typically recruit common-pool resources that allow their processing to be prioritized, which will detract from other mechanisms sharing those resources (see intersections indicated in bright blue). (c) High threat will also trigger specific executive functions to handle the challenges to the organism, as indicated by the arrows emanating from attentional/effortful control. For instance, `updating' might be needed to refresh the contents of working memory, `shifting' might be recruited to switch the current task set and `inhibition' could be called for to cancel previously planned actions. (d) State-dependent affective significance, such as reward, is hypothesized to have two main effects on executive function. Firstly, motivation fine-tunes executive functions that are important for the task at hand (represented by the change of shape of the updating function; see green arrow). Secondly, motivation can rearrange the allocation of common-pool resources (bright blue ellipse; see orange arrow), thereby affecting other executive resources.

Figure 3

Processing resources and threat. Summary of results from 34 positron emission tomography (PET) and fMRI studies of conditioning from 1995 to 2008, illustrating the coordinates provided for the contrast of threat (CS+) versus safe (CS−). (a) Activation peaks that were observed in the ACC, or nearby cortex, are shown in green for right hemisphere results and red for left hemisphere results (all coordinates were projected onto a midline view for display purposes). (b) Results for the right lateral surface are shown on an inflated surface to reveal multiple PFC sites, including ones that are not on the surface. These included the middle frontal gyrus, inferior frontal gyrus and anterior insula (note that the surface inflation `pushed up' some of the activation sites relative to their standard anatomical positions). (c) Subjects viewed an array of letters superimposed on task-irrelevant faces and were asked to report whether or not the target letter X was present [33]. During the low attentional load condition shown here, the target appeared among a uniform array of distractors (`pop-out' condition). During the high attentional load condition (not shown), a non-uniform array of letters was employed (search condition). During the threat condition, faces were previously paired with mild electrical shock, whereas safe stimuli were never paired with shock. (d) Differential responses to task-irrelevant threat and safe faces were inversely correlated with behavioral performance, suggesting that the processing of threat captured processing resources needed for task execution as a function of threat-related responses. Results are shown for a region of interest in the ACC that was defined in terms of a separate contrast of high versus low attentional load (shown in the inset). Data reanalyzed from Ref. [33].

Figure 4

Effects of threat and motivation on executive function. Key brain regions mediating the interactions between emotion and/or motivation with executive control function. Both types of interaction are hypothesized to depend on the anterior cingulate cortex (ACC). Abbreviations: DLPFC, dorsolateral PFC; IFG, inferior frontal gyrus; LC, locus coeruleus; Nacc, nucleus accumbens; OFC, orbitofrontal cortex; VTA, ventral tegmental area.