Review TRENDS in Cognitive Sciences VoL9 No.5 May2005 The cognitive control of emotion Kevin N.Ochsner1 and James J.Gross2 e,New York,NY 10027,USA The tion is im tant for bu models of the 'cold'control of dantation emotion regu ce.dir glhaegeentwyakeho memory(eg).The aim of this review mp or- ate recent im ext of 9 t in and anima cognitive processes difficult tos ecture draw upon highe cognitive control of emotion. uc have exam c meaningot.em0io 12 ally e evocative stimuli.These two regulation orms of en egu on d upon inter tion mechanisms is characterizing the pro emotions. Curent models posit thatm ns are Taken together,the results suggest a functional archi- mental representations that (i involve cha tecture or the co 1 th research on emotion If you are distressed by anything external,the pain (iii)can be either unlearned responses to stimuli intrins a ve s not di prop an e at any stimuli with acquired emotional value (e.g.a moment onditioned Marcus Aurelius(Meditations) and car the significance of stimuli to curn [11).that (v)depend upon different neura tems3,12,13. 25 initiation ures and los t time e to hrough the a ago,we humans have an extraordinary capacity Box 1.A brief history of psychological research on emotion gely determine regulation the impact dy of the ive control of er will have on our mental and he h motion regulation】 has a long history (Box 1).Past worl stre strategies and the neural systems involved in simple g168g9 of w on emotion regulation has entered a new phase unctional ima ging studies of reg atory ph 、。 tated in but,perhaps more importantl tudy of ld ob d b emotion that are dimcul nt work on the t thend ilds on lescribe when.how
The cognitive control of emotion Kevin N. Ochsner1 and James J. Gross2 1 Department of Psychology, Columbia University, Schermerhorn Hall, 1190 Amsterdam Avenue, New York, NY 10027, USA 2 Department of Psychology, Stanford University, Building 420, Stanford, CA 94305-2130, USA The capacity to control emotion is important for human adaptation. Questions about the neural bases of emotion regulation have recently taken on new importance, as functional imaging studies in humans have permitted direct investigation of control strategies that draw upon higher cognitive processes difficult to study in nonhumans. Such studies have examined (1) controlling attention to, and (2) cognitively changing the meaning of, emotionally evocative stimuli. These two forms of emotion regulation depend upon interactions between prefrontal and cingulate control systems and cortical and subcortical emotion-generative systems. Taken together, the results suggest a functional architecture for the cognitive control of emotion that dovetails with findings from other human and nonhuman research on emotion. If you are distressed by anything external, the pain is not due to the thing itself, but to your estimate of it; and this you have the power to revoke at any moment. Marcus Aurelius (Meditations) Introduction Conflicts, failures, and losses at times seem to conspire to ruin us. Yet, as Marcus Aurelius observed nearly two millennia ago, we humans have an extraordinary capacity to regulate the emotions occasioned by such travails. Importantly, these regulatory efforts largely determine the impact such difficulties will have on our mental and physical well-being [1–3]. Given its importance to adaptive functioning, it is not surprising that research on emotion regulation has a long history (Box 1). Past work has investigated the cellular responses to stress, the behavioral consequences of adopting specific regulatory strategies, and the neural systems involved in simple forms of affective learning and social behavior in rodents and nonhuman primates [1,4–7]. In recent years, research on emotion regulation has entered a new phase as functional imaging studies of regulatory phenomena in humans have developed rapidly. This growth has facilitated investigation of human analogs to affective behaviors studied in animals, but, perhaps more importantly, has allowed study of the emotion regulatory power of higher cognitive control processes that are difficult to study in animal models. In so doing, current work on the ‘hot’ control of emotion draws on rapidly developing cognitive neuroscience models of the ‘cold’ control of attention and memory (e.g. [8,9]). The aim of this review is to evaluate recent imaging studies that, in the context of evidence from allied human and animal work, help to elucidate the functional architecture underlying the cognitive control of emotion. Emotion and emotion regulation An essential part of understanding emotion regulatory mechanisms is characterizing the processes that generate emotions. Current models posit that emotions are valenced responses to external stimuli and/or internal mental representations that (i) involve changes across multiple response systems (e.g. experiential, behavioral, peripheral physiological [10]), (ii) are distinct from moods, in that they often have identifiable objects or triggers, (iii) can be either unlearned responses to stimuli with intrinsic affective properties (e.g. an unconditioned response to an aversive shock) or learned responses to stimuli with acquired emotional value (e.g. a conditioned response or stimulus–reward association), (iv) and can involve multiple types of appraisal processes that assess the significance of stimuli to current goals [11], that (v) depend upon different neural systems [3,12,13]. Emotion regulation involves the initiation of new, or the alteration of ongoing, emotional responses through the Box 1. A brief history of psychological research on emotion regulation Study of the cognitive control of emotion has three major historical antecedents within psychology [1]. The first antecedent is the psychodynamic study of defense, which was initiated by Freud a century ago. This line of work has examined the regulation of anxiety and other negative emotions using clinical descriptions and individual difference studies of so-called perceptual defenses against processing negatively arousing stimuli, and specific defenses such as repressive coping [68,69]. The second antecedent is the stress and coping tradition that grew out of the psychodynamic approach in the 1960s. This line of work has focused on the management of situations that ‘tax or exceed the resources of the person’ ([70], p. 141), and generated an early classic study of reappraisal showing that subjective and physiological responses decreased when a film of a potentially upsetting surgical procedure was viewed in analytical and detached terms [71]. The third antecedent is the developmental study of self-regulation, which had its roots in the study of socioemotional development. This work showed that children could obtain a preferred but delayed reward by thinking about available treats in abstract ways (e.g. putting a mental ‘picture-frame’ around a cookie) that decreased their immediate impulse to eat them [72]. Contemporary research builds on this foundation using both behavioral and neuroscience methods to describe when, how, and with what consequences individuals Corresponding author: Ochsner, K.N. (ochsner@psych.columbia.edu). regulate their emotions. Available online 5 April 2005 Review TRENDS in Cognitive Sciences Vol.9 No.5 May 2005 www.sciencedirect.com 1364-6613/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.tics.2005.03.010
Review TRENDS in Cognitive Science s Vol.9 No.5 May 200 24 Box 2.From basic mechanisms to individual difference and vely re Aany opatholog und failure tive basi re for 13,6.13到日 nd su hus .9.)that might be related yadtnhlerasonsiderableaniabityinthen mot ods like tho his v .78.E dge of d in p appraisal syste date the rs and sugge avenues f e:h he li It is might re自e es in y to coa tively rur emotional events pre ponseasinchndi action of re they generate,when they do so,and how these emotions ving to initiate(amplify)or block(diminish)perception Se mes h ve of our responses to stimul (3)their rela ive reliance on (e.g.141).One distinction su sted by Gross and ntrol and cognitive change,as indicated by their placement along the continuum;and(4)whether emotion ognit (e.g. att ing to ge is heir explicit goal( I want to fee ulation of negative emotions might limit expressive action but ment is correct). ot dampen unpl nt expe e.wo L atio contrast cognitive regulation neutralizes gative Attentional control ence without impairing and might decrease Attention is often referred to as the selective aspect of physiological arous sing,enabling us to focus on goa might be related to both normaland patholorical variation (e.g.loud music next door)information.In ral studie in well-being and social behavior(Box 2). have indicated that behavioral and neural responses ha two types of attend compare ectivel (g 119l)When responses to attended and hypothetical continuum to illustrate ory strateges tapping :(1)thewo type relat automati e conte Cognitive change re 1.Hy coninuumilustratngralatio the forms of cognitive control of em citation
action of regulatory processes. Current work examines the processes that individuals use to influence which emotions they generate, when they do so, and how these emotions are experienced or expressed [1]. Several schemes have been proposed for organizing regulatory strategies (e.g. [14]). One distinction suggested by Gross and colleagues contrasts behavioral (e.g. suppressing expressive behavior) and cognitive (e.g. attending to or interpreting emotion-eliciting situations in ways that limit emotional responding) regulation. Behavioral regulation of negative emotions might limit expressive action but does not dampen unpleasant experience, worsens memory, and increases sympathetic nervous system activation. By contrast, cognitive regulation neutralizes negative experience without impairing memory and might decrease physiological arousal [15,16]. Individual differences in emotional responsivity and/or cognitive control capacity might be related to both normal and pathological variation in well-being and social behavior (Box 2). Recent imaging work has investigated two types of cognitive regulation, attentional control and cognitive change, which are the focus of this review. Figure 1 uses a hypothetical continuum to illustrate relationships between regulatory strategies tapping these two types of control. These strategies might differ in: (1) their targets – impacting different types of emotional appraisal processes and associated neural systems [17,18]; (2) their effects – serving to initiate (amplify) or block (diminish) perception of our responses to stimuli; (3) their relative reliance on the overlapping neural systems supporting attentional control and cognitive change, as indicated by their placement along the continuum; and (4) whether emotion change is their explicit goal (‘I want to feel better!’), or occurs as a by-product of pursuing some other learning or judgment-related goal (e.g. ‘I want to learn which judgment is correct’). Attentional control Attention is often referred to as the selective aspect of information processing, enabling us to focus on goalrelevant (e.g. our writing) and ignore goal-irrelevant (e.g. loud music next door) information. In general, studies have indicated that behavioral and neural responses to attended as compared with unattended stimuli (or stimulus features) are either facilitated or inhibited, respectively (e.g. [19]). When responses to attended and unattended inputs do not differ, processing is considered to be relatively automatic. In the context of emotion, researchers have begun asking how paying less attention Box 2. From basic mechanisms to individual differences Characterizing the nature and operating characteristics of basic emotion regulatory mechanisms in healthy participants might help to establish a normative model for explaining the successful regulation of emotion. It might also lead to a greater understanding of individual differences, clinical conditions and lifespan development, by describing them in terms of variation and change in the function of a basic functional architecture for the cognitive control of emotion. Among healthy adults, there is considerable variability in the nature and strength of emotional responses, and also in the capacity to regulate them. Behavioral studies have begun to explore the experiential and behavioral consequences of these differences [73], and characteristic patterns of resting and/or emotional stimulusrelated neural activity in prefrontal and emotional appraisal systems are now being associated with gender, personality, negative affectivity [3,74] and regulatory ability. For example, Jackson et al. found that greater left PFC electrical activity at rest predicted dampened physiological reactivity to aversive stimuli, which might reflect automatic regulatory processes [75], and Ray et al. [76] found that the tendency to cognitively ruminate about emotional events predicted enhanced ability to increase or decrease amygdala responses through reappraisal, which itself depends upon cognitively reexamining the meaning of emotional events. Many forms of psychopathology revolve around failures to adaptively regulate emotional responses, with consequences ranging from personal distress to socially maladaptive and self-destructive behaviors [2,3,5]. Resting and symptom provocation studies have begun to identify abnormal patterns of neural response in psychiatric illness [3,6,13] and substance abuse (e.g. [77]) that might be related to emotion regulation failures. However, very few studies have examined directly the neural mechanisms mediating successful or unsuccessful regulation in clinical populations using methods like those described in this review (see, however, [78]). Building knowledge of dysregulatory mechanisms from a basic model of effective regulation could elucidate the nature of these disorders and suggest avenues for cognitive and pharmacological treatment. Basic models of emotion regulation might also help to explain the development of regulatory capacities across the lifespan. It is possible, for example, that structural and functional changes in control and appraisal systems underlie normal and abnormal emotional responses in children [79], and the positivity of emotional experience in older adults [80]. TRENDS in Cognitive Sciences Attentional control Cognitive change Selective inattention to emotional stimuli [19–22,25] Performing distracting secondary task [31–35] Attention to and judgement of emotional vs. non-emotional stimulus attributes [23,24,26–28] Anticipatory/ expectancydriven emotion [37–40,42–46] Top-down appraisal [17] Reappraisal [48–54] Placebo [55–57] S-R reversal/ extinction [58–65] Figure 1. Hypothetical continuum illustrating relationships among the forms of cognitive control of emotion described in this review. The left and right anchors for the continuum represent the exclusive use of attentional control or cognitive change, respectively, to modulate emotion perception and/or responses. Red and blue text denote strategies for controlled emotion generation and regulation, respectively. Relevant citations for each strategy are shown in brackets. This continuum is intended to serve a heuristic function, helping the reader to visualize relationships among control strategies (see text). Review TRENDS in Cognitive Sciences Vol.9 No.5 May 2005 243 www.sciencedirect.com
2 Review TRENDS in Cognitive Sciences Vol.9 No.5 May 2005 l ing in emotional appraisal systems such as the amygdala. (i)deliberate attempts to regulate pain in order to e manipulated the amount of attention ional control have sh that limiti on modulation of amygdala responses,have produced but the contexts mechanism activation de when participants attend to and valuate ing than ptual features there has compared with subliminal presentations of negative) Ame hcan faces dging the of conceived 6 happy faces [231, or rating their emotional response to judgments or tasks.For studies of selective attention ther than ing them passively 4 wever, a more important problem might be an over activity to be invariant with res ct to attention to rroborating behavioral or physiological meas & ants judged the gender ort the at en th tion ha ed hous dged the stimuli)has made it difficult to det and/o ppy, and fea [27],judge the ag ure to famous ing highly arousing(painful)stimuli,question people (e.g. sely what processes are being carried out by find clear,but two Summary be w).First,some judgments might impose a Cognitive change ing of e long-ter and me also limits a and reasoning has been a pants might some the primar cognitive i making good/bad evaluations of valenced concepts interactions between prefrontal systems that sup or ion),right atrdlateralpreironta control posterio pants indicated in po ratings that they hade ed (e g visual spatial auditory)information 18 361 In the 22 P activity is also found in ntext lti motio have in a ng how as dis Thes es can be why similar reciprocal PFC-amygdala relationships have can com a nge both to otional response wl en none was ongoing or to regulate an already triggered response emotion uses a distracting ondary task to limit Controlled generation ttention to emotional stimu The use of fcognitive change to generate an emotional e roach has e ined th netral correlate oop task 341,or simply being asked to'think of of anticipatory re that precede expected emotion ve 0 ents ical a implicated in mental state attribution [41],which migh gray orbi ofrontal e orte
to emotional stimuli or their features modulates processing in emotional appraisal systems such as the amygdala. Selective attention Several studies have manipulated the amount of attention paid to emotional stimuli by asking participants to selectively judge either their emotional or their perceptual features. These studies, which have focused particularly on modulation of amygdala responses, have produced strikingly discrepant results. On one hand, some studies have shown that amygdala activation decreases when participants attend to and evaluate emotional features, including matching emotional faces or scenes based on emotional labels rather than perceptual features [20,21], viewing supra- as compared with subliminal presentations of (presumably negative) African American faces [22], judging the expression rather than the gender of fearful, angry, or happy faces [23], or rating their emotional response to aversive scenes rather than viewing them passively [24]. On the other hand, studies have shown amygdala activity to be invariant with respect to attention to emotional features when participants judged the gender of fearful faces rather than judging aspects of simultaneously presented houses [19,25], judged the gender as compared with expression of happy and disgusted [26], or happy, sad, disgusted and fearful faces [27], judged the age or trustworthiness of normatively untrustworthy faces [28], or the age or goodness of normatively ‘bad’ famous people (e.g. Hitler) [29]. The reasons for these discrepant findings are not yet clear, but two possibilities stand out (see [18], and Critical Summary below). First, some judgments might impose a greater attentional load, which more strongly limits processing of perceptual inputs and as a consequence also limits amygdala responses (cf. [30]). Second, participants might in some cases actively regulate their responses. In keeping with the latter suggestion, when making good/bad evaluations of valenced concepts (e.g. abortion), right ventral lateral prefrontal cortex (LPFC) activation was found on trials for which participants indicated in postscan ratings that they had exerted control [22]. Right ventral LPFC activity is also found in combination with amygdala deactivation during cognitive change, as discussed below. These results could explain why similar reciprocal PFC–amygdala relationships have been observed when participants judged emotional compared with perceptual properties of stimuli [20,21]. Attentional distraction A second approach to interactions between attention and emotion uses a distracting secondary task to limit attention to emotional stimuli. These studies have focused primarily on responses to pain (however, see [31]), and have found that performance of a verbal fluency task [32], the Stroop task [33,34], or simply being asked to ‘think of something else’ [35] diminishes the aversiveness of pain, reduces activity in cortical and subcortical pain-related regions, including midcingulate cortex, insula, thalamus and periacqueductal gray, and activates orbitofrontal cortex (OFC), anterior cingulate cortex (ACC) and medial and lateral PFC regions related to cognitive control. It is not yet clear, however, whether these activations reflect (i) deliberate attempts to regulate pain in order to facilitate performance of the distractor task and/or (ii) processes supporting performance of that task directly. Critical summary Studies of attentional control have shown that limiting attention to emotional stimuli can limit responses in appraisal systems, but the contexts and mechanisms governing this regulatory effect are not clear. For example, studies of selective attention have used primarily emotional face stimuli whereas studies of distraction have used painful stimuli, confounding type of attentional control and type of stimulus. Furthermore, there has been lack of clarity concerning the underlying processing demands – whether conceived as attentional load or some other type of cognitive operation – imposed by specific judgments or tasks. For studies of selective attention, however, a more important problem might be an overreliance on brain activation changes – in the absence of corroborating behavioral or physiological measures – to support the inference that emotion regulation has taken place. That fact (coupled with the use of low arousal, face stimuli) has made it difficult to determine whether amygdala modulation reflects regulatory success and/or the failure to elicit a strong response. Although studies of attentional distraction have avoided these pitfalls by using highly arousing (painful) stimuli, questions remain about precisely what processes are being carried out by control systems. Cognitive change The use of higher cognitive abilities such as working memory, long-term memory and mental imagery to support learning, judgment and reasoning has been a primary focus of research in cognitive neuroscience. In general, these abilities have been shown to depend upon interactions between prefrontal systems that support control processes and posterior cortical and subcortical systems that represent different types of modality specific (e.g. visual, spatial, auditory) information [8,36]. In the context of emotion, researchers have begun asking how these abilities can be used to construct expectations for, select alternative interpretations of, and/or make different judgments about emotional stimuli [18,36] that can change both behavioral and neural responses to them. Cognitive change might be used either to generate an emotional response when none was ongoing or to regulate an already triggered response. Controlled generation The use of cognitive change to generate an emotional response has been studied in three ways. The first approach has examined the neural correlates of anticipatory responses that precede expected emotional events. Such anticipation has been associated with activation of dorsal medial PFC (MPFC) regions [37–40] implicated in mental state attribution [41], which might reflect cognitive expectations for pleasant or unpleasant experiences, in combination with activation of regions 244 Review TRENDS in Cognitive Sciences Vol.9 No.5 May 2005 www.sciencedirect.com
Review TRENDS in Cognitive Science Vol9 No.5 May2005 245 important for appraising the aversive or rew and appraisal systems are strikingly similar to those ompared w are 39 sho ate 2nneheoy hich sti tas myg. acc NA 【4 rd type of cognitive regu insula and cingulate 40 ways in which simple stimul ciations are d r expectation formed and Altho the pre syst stimuli are perceived as painful when participants expec avoidance of aversive stimuli 42,exti action of classically ,an thi rostral cingulate regions [461,which might be involved in depend upon interactions between similar cognitiv pain aftect and cognitive expectations about pain, A third approach has directly contrasted top-dow PFC,OFC and/or ACC have been observed consistently, generated by beliets al a stimulus with ing impair. this issue by asking participants either to look at aversiv the appraisal side however,findings have less or to th 818 an dala activa observed in both conditions. Ho ver on top-down extinction.and during reversal learning both striatal 60 8geerao act AC PFC and MPF and amygdala vation h been observed, wit aversive annraisal of an oth wise innocuous image npared with currently reinforced stimuli62.Thes repancies across studies might chan e has also b een studied in the rent Critica a ha as nvo C.O by cingulate contro general.studies have found that rea raisal of neg about,and interpretations of,stimuli,or (ii)by ing to emotion orsal ACC and systems tha late new e onses with stimuli. These and decre trol that in ap raisal systems such as the mygdala or insula in cingulate systems [8,9.The consiste acy of these e oal of reappraisal here ngs (relative to o fact systems recruitedacross studies,however,which migh the use of stimuli that generate strong emotional (see below.and 18.51). said qu ons remain about when and how specific The second type of controlled n is implicate ontrol d appraisa systems int including worki an raisal svstems the tent to which dhavre ho th participante tha different strategies modulate appraisal systems in differ ent ways amygdala and pain- elated cingulate,insula and thalamic Towards a functional architecture of cognitive control of com (ii)incr on of of this re control,includir al cing ate cortex and dorsal and studies whose results can help to elucidate the function yet clo interactions betwee imaging studies of either or
important for appraising the aversive or rewarding (as compared with neutral) properties of stimuli. Thus, anticipating a painful shock [37,42,43], heat [38] or injection [39] activates cingulate, insula and amygdala; anticipating pleasant or aversive tastes activates amygdala, nucleus accumbens (NAcc) and/or OFC [44]; and anticipating monetary reward activates NAcc, amygdala, insula and cingulate [40]. The second approach has examined how expectations about how a stimulus might feel influence neural responses to it. Studies have shown that nonpainful stimuli are perceived as painful when participants expect pain, and that this expectation leads to activation of midcingulate regions [45] as well as medial temporal and rostral cingulate regions [46], which might be involved in pain affect and cognitive expectations about pain, respectively. A third approach has directly contrasted top-down responses generated by beliefs about a stimulus with bottom-up responses driven by direct perception of aversive stimuli. To date, only one study has addressed this issue by asking participants either to look at aversive images (bottom-up) or to think about neutral images in negative ways (top-down). Amygdala activation was observed in both conditions. However, only top-down generation activated ACC, LPFC and MPFC systems [17], which might be involved in cognitively generating an aversive appraisal of an otherwise innocuous image. Controlled regulation The use of cognitive change to regulate an existing or ongoing emotional response has also been studied in the context of three different forms of higher cognition and learning. The first type of cognitive regulation is known as reappraisal, and involves reinterpreting the meaning of a stimulus to change one’s emotional response to it [47]. In general, studies have found that reappraisal of negative emotion activates dorsal ACC and PFC systems that support the selection and application of reappraisal strategies, and decreases, increases or maintains activity in appraisal systems such as the amygdala or insula in accordance with the goal of reappraisal [48–54]. There has been variability in the precise prefrontal and appraisal systems recruited across studies, however, which might be attributable to differences in the nature of the stimuli used and the goal or content of reappraisal strategies (see below, and [18,51]). The second type of controlled regulation is implicated in placebo responses to situations that involve no active drug compounds that could impact appraisal systems. Two studies have shown that if participants believe that placebo creams or drugs blunt pain, then painful stimuli elicit less pain and produce (i) decreased activation of amygdala and pain-related cingulate, insula and thalamic regions in combination, with (ii) increased activation of lateral and medial prefrontal regions related to cognitive control, including rostral cingulate cortex and dorsal and right ventral LPFC [55–57]. Although the precise nature of the cognitive processes mediating placebo effects is not yet clear, placebo-related interactions between prefrontal and appraisal systems are strikingly similar to those supporting reappraisal, suggesting that placebo effects are mediated by the active maintenance of beliefs about placebo compounds that change the way in which stimuli are appraised [57]. The third type of cognitive regulation builds on animal models of emotion regulation (e.g. [6,7]) by examining the ways in which simple stimulus–reinforcer associations are formed and altered. Although the precise systems recruited and the nature of interactions among them have differed across studies and paradigms, instrumental avoidance of aversive stimuli [42], extinction of classically conditioned fear responses [58,59] and reversal of stimulus–reward associations [60–63] have been shown to depend upon interactions between similar cognitive control and emotional appraisal systems. On the control side, findings of activation in ventral lateral and medial PFC, OFC and/or ACC have been observed consistently, supported by neuropsychological studies showing impairments of reversal learning in patients with lesions of ventral and orbital but not dorsolateral PFC [64,65]. On the appraisal side, however, findings have been less consistent. For example, amygdala activation has been reported to either decrease [59] or increase [58] during extinction, and during reversal learning both striatal [60] and amygdala activation have been observed, with separate regions of the amygdala tracking previously as compared with currently reinforced stimuli [62]. These discrepancies across studies might be connected with differences in stimulus characteristics, and also how emotional associations are learned and altered. Critical summary In general, studies of cognitive change have shown consistently that emotional appraisal systems can be modulated by PFC, OFC and cingulate control systems activated either (i) by high-level expectations for beliefs about, and interpretations of, stimuli, or (ii) by learning to associate new emotional responses with stimuli. These findings are strikingly similar to control dynamics observed for ‘cold’ forms of control that involve prefrontal and cingulate systems [8,9]. The consistency of these findings (relative to inconsistent results for studies of attentional control) might be attributable to two factors: the use of stimuli that generate strong emotional responses and the use of regulatory strategies that clearly and strongly engage regulatory processes. That being said, questions remain about when and how specific control and appraisal systems interact, including working out exactly why specific control strategies recruit specific control systems and determining the extent to which different strategies modulate appraisal systems in different ways. Towards a functional architecture of cognitive control of emotion The goal of this review was to evaluate recent imaging studies whose results can help to elucidate the functional architecture underlying the cognitive control of emotion. Work using animal models of affective learning and imaging studies of either cognitive control or emotional Review TRENDS in Cognitive Sciences Vol.9 No.5 May 2005 245 www.sciencedirect.com
Review TRENDS in Cognitive Sciences Vol.9 No.5 May 2005 (c)Act ation key Superior Emoin regulation via reappraisal or placebo -100 -100 -50 (b)Media 间s udies inc plot Later 8,51,52.53,57 9323834,37,3.46 100 100 -50 76066 75880.62.63 d. (al an FC and ventral LPEC an land ve I MPFC emotional appraisal systems,and are used to explicitly sp e about nbe ch s the dala in different t taining repr ntations of these descriptions might pr [3,5-7,13 Current imaging w ork on attentional deploy vide a task context that indirectly an gnitive egulate appraisal system activation systems that represent alternative interpretations of involvement of contro-appraisa ents s a co. cognitive ch ange group into those that recruit only ventral multiple types of control strategies that regulate multiple reve ems praisal.placebo and anticipation).A ke enit of this type of as ative ion scheme is thatitc trol mechanisms and their impact on otion-ger ort studied in animal models to the use of higher systemsFor ample, s betweer cognitive processes to regulate emotion. pes ant towhich th processes(Figure 2).The frst type PFC Future direction nd OFC syst ems used to evaluate the Although current research provides converging for a functiona ehremotioncontrol,iti po limited data reciproc udies make it difficult to draw firm and highly specific TA could also affect ng cont comput at by The involves dorsal to ystems and heed or phys
responding in both healthy and psychiatric populations have implicated regions of PFC, OFC and ACC in specific types of control processes and subcortical regions, such as the amygdala, in different types of emotional appraisal [3,5–7,13]. Current imaging work on attentional deployment and cognitive change builds on this work by examining the ways in which these control systems regulate appraisal system activation. The consistent involvement of control–appraisal system dynamics in various forms of regulation suggests a common functional architecture that might be flexibly deployed to support multiple types of control strategies that regulate multiple types of emotional responses. Furthermore, current imaging work is beginning to identify patterns of functional specificity in cognitive control mechanisms and their impact on emotion-generative systems. For example, it seems that relationships between types of cognitive change might be understood in terms of the extent to which they depend upon two types of control processes (Figure 2). The first type involves ventral PFC and OFC systems used to evaluate the context-appropriate emotional value of stimuli and select actions on the basis of those evaluations. Maintaining representations of these values might directly affect emotional associations through direct reciprocal connections with appraisal systems such as the amygdala and NAcc. Through these reciprocal connections, appraisal systems could also affect representation of goal-relevant information in PFC and OFC regions. The second type involves dorsal PFC systems that have few, if any, direct connections with emotional appraisal systems, and are used to explicitly reason about, and describe, how associations between stimuli and emotional responses can be changed. Maintaining representations of these descriptions might provide a task context that indirectly affects emotional associations by biasing processing either in the ventral control system or in perceptual and associative memory systems that represent alternative interpretations of events, which in turn send inputs to appraisal systems. Against this backdrop, it can be seen that forms of cognitive change group into those that recruit only ventral systems (stimulus–reward reversal learning and extinction) and those that might recruit both ventral and dorsal systems (reappraisal, placebo and anticipation). A key benefit of this type of classification scheme is that it could help to relate simple forms of affective learning – of the sort studied in animal models – to the use of higher cognitive processes to regulate emotion. Future directions Although current research provides converging evidence for a functional architecture for emotion control, it is important to note that for each type of control examined here, limited data and/or variability in activations across studies make it difficult to draw firm and highly specific inferences concerning which control computations are carried out by specific systems, and how they configure for different strategies in different contexts. To address these issues, future work will need to: (1) make use of experiential, behavioral and/or physiological indices that right z = 20 Inferior Superior left (b) Medial –100 –50 0 50 0 right z = 20 left Inferior Superior 50 0 –50 50 0 (a) Lateral (c) Activation key 32 - 48, 51, 52, 53, 57 63 33, 38 40, 42, 44 48, 51, 52, 53, 55, 57 58, 60, 61, 62, 63 32, 37, 38 40, 42, 45 48, 51, 55, 57 60, 61, 62, 63 32, 33, 34, 37, 39, 46 40, 44 51, 53 58, 60, 62, 63 Lateral Medial Superior Inferior (d) Studies in each plot –50 50 0 –50 –100 –50 50 0 –50 50 50 –100 50 0 –50 –100 –50 0 Attentionally distracting secondary task Emotion regulation via reappraisal or placebo Emotion regulation via extinction or reversal Emotion generation via anticipation Figure 2. Activations in (a) LPFC and (b) MPFC associated with different forms of cognitive control over emotional responding located dorsal and ventral to zZ20 (roughly the median z-coordinate). Each point corresponds to an activation focus representing the results of a contrast isolating regions related to control, shape- and color-coded according to the type of strategy used. (c) Activation key indicating which shapes correspond to which types of cognitive control. As described in the text, regulation strategies differ in the extent to which they draw upon dorsal PFC systems supporting redescription of emotional associations or ventral PFC systems supporting alteration of these associations through choice and learning. As is illustrated in (a) and (b) and listed (by reference number) in (d), reappraisal and placebo recruit dorsal MPFC and both dorsal and ventral LPFC whereas extinction and reversal primarily recruit dorsal and ventral MPFC and only ventral LPFC. Fewer studies have examined attentional distraction and emotion generation, which recruit ventral LPFC and both dorsal and ventral MPFC. 246 Review TRENDS in Cognitive Sciences Vol.9 No.5 May 2005 www.sciencedirect.com