How do emotion and motivation direct executive control?
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. 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. Although the impact of affective significance (see Glossary) on behavioral performance is well documented [1Vuilleumier P. How brains beware: neural mechanisms of emotional attention.Trends Cogn. Sci. 2005; 9: 585-594Abstract Full Text Full Text PDF PubMed Scopus (1524) Google Scholar], in general, the mechanisms by which this impact is manifested remain poorly understood. And, whereas some progress has been made concerning the interactions between emotion and specific cognitive processes [2Phelps E.A. Emotion and cognition: insights from studies of the human amygdala.Annu. Rev. Psychol. 2006; 57: 27-53Crossref PubMed Scopus (1164) Google Scholar, 3Pessoa L. On the relationship between emotion and cognition.Nat. Rev. Neurosci. 2008; 9: 148-158Crossref PubMed Scopus (1419) Google Scholar], important gaps still remain. Crucially, relatively little is known about the role of affective significance in ‘executive control’ functions. Here, our goal is to propose a conceptual framework that describes how affective significance impacts the flow of information processing in the brain, with a particular aim at understating how it can either enhance or impair behavioral performance according to the situation at hand. Items laden with affective significance include those that involve threat (e.g. via pairing with mild shock) and reward (e.g. via pairing with cash). The framework thus attempts to describe how both emotion and motivation interact with executive control to determine behavioral outcome – in contrast with proposals that focus on either threat or reward processing. Here, it is suggested that both emotion and motivation signals are integrated with executive functions so as to effectively incorporate value into the unfolding of behavior. The proposed framework is referred to as the ‘dual competition’ model to reflect the suggestion that affective significance influences competition at both the perceptual and executive levels – and because the impact is caused by both emotion and motivation. According to many proposals of attention, objects compete for limited perceptual processing capacity and control of behavior [4Desimone R. Duncan J. Neural mechanisms of selective attention.Annu. Rev. Neurosci. 1995; 18: 193-222Crossref PubMed Scopus (6035) Google Scholar, 5Pashler H. The Psychology of Attention. MIT Press, 1998Google Scholar]. To understand the flow of information processing more widely, in addition to the role of perceptual competition, it is crucial to understand the impact of executive control functions on item processing. Executive control involves a host of ‘adjustment processes’, including perceptual selection, detection and resolution of conflict, and maintenance of contextual information. Executive control is not unitary, and different mechanisms can have their own limited processing capacities or resources [6Kahneman D. Attention and Effort. Prentice-Hall, 1973Google Scholar, 7Norman D.A. On data-limited and resource-limited processes.Cognit. Psychol. 1975; 7: 44-64Crossref Scopus (1565) Google Scholar]. Neuropsychological research also supports the dissociation of executive functions, consistent with the fractionation of the central executive [8Norman D.A. Shallice T. Attention to action: willed and automatic control of behavior.in: Davidson R.J. Consciousness and Self-Regulation. Plenum, 1986: 1-18Crossref Google Scholar, 9Baddeley A. Working memory: looking back and looking forward.Nat. Rev. Neurosci. 2003; 4: 829-839Crossref PubMed Scopus (3351) Google Scholar, 10Stuss D.T. Knight R.T. Principles of Frontal Lobe Function. Oxford University Press, 2002Crossref Scopus (550) Google Scholar]. The exact fractionation of executive functions is subject to debate, but probably involves at least three functions [11Smith E.E. Jonides J.J. Neurosicence – storage and executive processes in the frontal lobes.Science. 1999; 283: 1657-1661Crossref PubMed Scopus (2255) Google Scholar, 12Miyake A. et al.The unity and diversity of executive functions and their contributions to complex ‘Frontal Lobe’ tasks: a latent variable analysis.Cognit. Psychol. 2000; 41: 49-100Crossref PubMed Scopus (9609) Google Scholar]: inhibition, shifting and updating. Crucially, ample evidence indicates some unity of executive functions as well, consistent with the notion that mechanisms are shared across functions [12Miyake A. et al.The unity and diversity of executive functions and their contributions to complex ‘Frontal Lobe’ tasks: a latent variable analysis.Cognit. Psychol. 2000; 41: 49-100Crossref PubMed Scopus (9609) Google Scholar, 13Duncan J. et al.Intelligence and the frontal lobe: the organization of goal-directed behavior.Cognit. Psychol. 1996; 30: 257-303Crossref PubMed Scopus (682) Google Scholar]. This ‘capacity sharing’ has important implications for the understanding of human information processing – because it leads to ‘executive competition’. Here, it is proposed that subcomponents of executive control are mutually interacting, such that resources devoted to one component will detract from those available to other components. For instance, if resources required to carry out behavioral inhibition are partly shared with those needed during shifting, an individual needing to withhold responding in a trial might exhibit an increased switching cost if she is asked in close temporal succession to switch between tasks (e.g. Ref. [14Verbruggen F. et al.The interaction between stop signal inhibition and distractor interference in the flanker and Stroop task.Acta Psychol. (Amst.). 2004; 116: 21-37Crossref PubMed Scopus (115) Google Scholar]). It is hypothesized that affective significance determines the flow of information processing in at least two general ways: in a ‘stimulus-driven’ and a ‘state-dependent’ manner. Emotion-laden stimuli include those involving emotional expressions or affective scenes, in addition to originally neutral items that might have acquired affective significance by previous pairing with aversive events (e.g. pairing with mild shock). It is hypothesized that affective significance impacts both perceptual competition and executive control (Figure 1a ). Perceptual competition, which takes place in visual cortex, is affected because emotional content enhances sensory representations of emotional items (Figure 1a, arrow 1), which is well documented in human visual cortex [1Vuilleumier P. How brains beware: neural mechanisms of emotional attention.Trends Cogn. Sci. 2005; 9: 585-594Abstract Full Text Full Text PDF PubMed Scopus (1524) Google Scholar]. Such enhancement depends, at least in part, on output connections from the amygdala, which is known to project to multiple levels of visual cortex, including the primary visual cortex [15Amaral D.G. et al.Anatomical organization of the primate amygdaloid complex.in: Aggleton J. The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, 1992: 1-66Google Scholar]. Executive control is affected by emotional content because; firstly, strengthened sensory representations will receive prioritized attention (Figure 1a, arrow 2). For example, items with increased visual responses can direct spatial attention towards those locations – this will occur as long as sufficient processing resources are available [16Pessoa L. To what extent are emotional visual stimuli processed without attention and awareness?.Curr. Opin. Neurobiol. 2005; 15: 188-196Crossref PubMed Scopus (382) Google Scholar]. Secondly, executive control is modulated because affective information might be directly conveyed to control structures (Figure 1a, arrow 3). For instance, amygdala outputs might convey the significance of an item via connections with anterior cingulate cortex (ACC) territories, which might help direct attention towards the location of the emotional item via connections with the dorsolateral prefrontal cortex (PFC) (see later). In this manner, the modulation of executive control eventually affects visual processing [17Egner T. Hirsch J. Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information.Nat. Neurosci. 2005; 8: 1784-1790Crossref PubMed Scopus (818) Google Scholar] (Figure 1a, arrow 4). The impact of an emotion-laden stimulus on behavior crucially depends on how it affects the flow of executive functions. It is hypothesized that this will depend on the level of threat, which, accordingly, will determine if emotional content enhances or impairs behavioral performance. When emotional content is low in threat, processing is biased in favor of the emotional item (Figure 2a ) – this situation also extends to positive stimuli [18Brosch T. et al.Beyond fear: rapid spatial orienting toward positive emotional stimuli.Psychol. Sci. 2008; 19: 362-370Crossref PubMed Scopus (284) Google Scholar] (Box 1). In particular, the spatial locus of the emotional item is privileged, possibly because items that are low in threat are somewhat ambiguous and so might attract further attention as part of additional information gathering [19Whalen P.J. Fear, vigilance, and ambiguity: initial neuroimaging studies of the human amygdala.Curr. Dir. Psychol. Sci. 1998; 7: 177-188Crossref Scopus (678) Google Scholar]. In this manner, emotional content enhances target processing with relatively minor effects on irrelevant stimuli and other executive functions that might be needed (e.g. if task switching is involved). Thus, in the low-threat case, although emotional items are prioritized, the impact on behavior is modest – in this sense, it can be said that a ‘soft’ prioritization occurs. Because the effect on performance is relatively weak, behavioral can be to and might be in (e.g. Ref. et stimuli or visual attention in Psychol. PubMed Scopus Google Scholar]). whereas low-threat emotional stimuli a stimulus their processing is and depends on the of a host of that the neural including attention, task and perceptual A. and the responses to emotional Dir. Psychol. Sci. 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Sci. 2000; 4: Full Text Full Text PDF PubMed Scopus Google Scholar]. The is important for integrating from multiple including affective and et of anterior cingulate cortex to 1995; PubMed Scopus Google Scholar, et organization of the frontal Opin. Neurobiol. PubMed Scopus Google Scholar] – and in this in close with the anterior and H. of interactions in the primate prefrontal Rev. 1995; 19: Scholar]. The has also been suggested to be in conflict processing and and determine the and of It is suggested that during threat will impair executive because resources that are required to threat processing are Secondly, threat also multiple that are in specific executive functions (Figure This is suggested to at least in part, on the signals are known to in other brain and to and responses et of anterior cingulate cortex to 1995; PubMed Scopus Google Scholar]. For instance, the might the which is important in the of other important functions. 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For instance, one is in a of items are and can direct attention in a A. et al.The spatial attention with and to attention 2008; 18: PubMed Scopus Google Scholar]. might be of as an emotional of threat, and leads to effects and mechanisms of evidence from 2008; PubMed Scopus Google Scholar], in general, emotion and motivation are and for focus on threat and reward processing (Box 1). The proposed framework of how emotion and motivation interact with executive functions several in the including biased competition [4Desimone R. Duncan J. Neural mechanisms of selective attention.Annu. Rev. Neurosci. 1995; 18: 193-222Crossref PubMed Scopus (6035) Google Scholar] and [6Kahneman D. Attention and Effort. Prentice-Hall, 1973Google Scholar, 7Norman D.A. On data-limited and resource-limited processes.Cognit. Psychol. 1975; 7: 44-64Crossref Scopus (1565) Google Scholar, et can selective evidence for Psychol. PubMed Scopus Google Scholar, et of selective attention and cognitive Psychol. 2004; PubMed Scopus Google Scholar] – also et et the many of mechanisms of cognitive in Working Oxford University Press, Scholar] and et and modulation and R. PubMed Scopus Google Scholar] for of has how emotional stimuli are prioritized in of processes [1Vuilleumier P. How brains beware: neural mechanisms of emotional attention.Trends Cogn. Sci. 2005; 9: 585-594Abstract Full Text Full Text PDF PubMed Scopus (1524) Google Scholar]. less research has been devoted to understanding the of emotional information and executive a of has the neural of reward reward signals in the Rev. Neurosci. 2000; PubMed Scopus Google Scholar]. less research has to how motivation directly with executive The goal of the competition framework is to propose basic elements of a conceptual framework with which to understand how both emotion and motivation are integrated with executive An important implication of the proposal is that emotion and motivation can either enhance or impair behavioral performance depending on how they interact with control functions. how emotion and motivation can be or to behavior (e.g. as in a for research (Box for the competition framework be to other sensory The to be in the at least for stimuli T. et the of modulation of visual attention by 2008; PubMed Scopus Google positive stimuli to a prioritization of processing that is to that of In at least one case, to effects et and modulation of performance by emotional 2006; PubMed Scopus Google the impact of levels of threat the across executive For instance, an affectively item impair conflict processing and behavioral inhibition to a the model be to a of including and executive functions be as to specific or are they as specific of brain et of Cogn. 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