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Reeck C., and Egner T. (2015) Interactions between Attention and . In: Arthur W. Toga, editor. Brain Mapping: An Encyclopedic Reference, vol. 3, pp. 269-274. Academic Press: Elsevier. Author's personal copy

Interactions between Attention and Emotion

C Reeck, Columbia University, New York, NY, USA T Egner, Duke University, Durham, NC, USA

ã 2015 Elsevier Inc. All rights reserved.

Authors’ note: Portions of this work were completed as part of the requirements for Crystal Reeck’s doctorate.

Cognitive resources are inherently limited, such that individuals representations of stimuli that have previously (in either the cannot fully process all aspects of their environment at the same species’ or the individual’s history) been associated with time. Attention allocates processing resources to stimuli that are rewarding or aversive consequences. deemed most relevant to an individual’s goals and well-being, In addition to (and partly as a consequence of) their prior- facilitating adaptive behavior. As emotional stimuli have inher- itization in early sensory processing, affective stimuli are more ent value and biological or personal relevance to an individual, likely to hold attention and drive higher-level , by their very nature, they have a unique relationship with atten- decision-making, and response selection processes than affec- tion. (In this article, the terms “” and “emotion” are used tively neutral stimuli. During , affectively salient interchangeably. However, it should be noted that the term targets are more rapidly detected (Fox, 2002; Hansen &

“affect” is generally employed to refer to a broader class of states, Hansen, 1994; Ohman, Flykt, & Esteves, 2001a; Ohman, including moods, motivations, and , than “emo- Lundqvist, & Esteves, 2001b). This advantage appears to be tion” typically encompasses.) Due to space limitations, this supported by speeded serial search (Eastwood, Smilek, & Meri- article primarily addresses interactions between attention and kle, 2001; Notebaert, Crombez, Van Damme, De Houwer, & the processing of negative affective stimuli, the latter having Theeuwes, 2011), and individuals are more likely both to been the main focus of the research literature and affording orient initially to affective stimuli in the environment and to the closest link to animal studies and the clinical domain. return their attention to those stimuli while sampling the Affective stimuli often gain privileged access to neural processing environment (Knight et al., 2007; LaBar, Mesulam, Gitelman, resources, making them both more likely to capture attention & Weintraub, 2000). Moreover, affective stimuli can also and more difficult to filter out if they are irrelevant to the current attract attention and improve processing of neutral stimuli goals. In addition to emotional stimuli exerting a strong exoge- presented at the same spatial locations (Phelps, Ling, & Car- nous (‘bottom-up’) pull on attention, endogenous (‘top-down’) rasco, 2006). Orienting to affectively salient stimuli can occur attentional settings can also shape affective responding to stim- even in the absence of conscious of those stimuli, uli and modulate their capacity to influence , particularly for highly anxious individuals (Mogg & Bradley, decision making, and response selection. This article examines 1998). Emotional stimuli are also more likely to break through both of these aspects of the relationship between emotion and sources of or interference to achieve awareness. attention and highlights the neural systems supporting their Perhaps one of the most famous examples of this phenome- interaction. non is the (Cherry, 1953), wherein people are perfectly capable of ignoring other conversations at a cock- tail party while socializing but will end up orienting to one of Emotional Stimuli Engage Attention those background conversations if something emotionally rel-

evant is uttered, such as their name. Similar affective intrusion Emotion alters neural representations of stimuli at early sen- effects have been observed using visual stimuli, with emotional sory processing stages, with emotional stimuli evoking greater images dominating awareness compared to neutral images in activation than neutral stimuli in relevant sensory regions: paradigms (Alpers & Gerdes, 2007; Alpers & emotional images evoke greater activation in visual cortical Pauli, 2006; Alpers, Ruhleder, Walz, Muhlberger, & Pauli, regions (Lane, Chua, & Dolan, 1999; Morris et al., 1998; 2005) and breaking through interference generated during Sabatinelli, Bradley, Fitzsimmons, & Lang, 2005; Vuilleumier, continuous flash presentations (Yang, Zald, & Blake, 2007). Armony, Driver, & Dolan, 2001), emotional sounds elicit With respect to the attentional blink (wherein targets presented greater activation in auditory processing areas (Grandjean immediately following the detection of a previous target are et al., 2005; Mitchell, Elliott, Barry, Cruttenden, & Woodruff, less likely to be reported), affectively salient stimuli are more

2003), and both pleasant and unpleasant tastes increase resistant to interference from previous targets and are more activation in gustatory processing regions (O’Doherty, Rolls, likely to be reported (Anderson, 2005; Lim, Padmala, & Pessoa, Francis, Bowtell, & McGlone, 2001). These biases can occur 2009). Representations of emotional stimuli in the environ- very early in sensory processing, emerging within 100 millisec- ment, therefore, appear to benefit from enhanced attentional onds after stimulus onset (Halgren, Raij, Marinkovic, access compared to neutral stimuli.

Jousmaki, & Hari, 2000; Pizzagalli, Regard, & Lehmann, Several neural mechanisms appear to contribute to the

1999). Under biased-competition models (Desimone & potent influence that emotional stimuli exert on attention. Duncan, 1995; Miller & Cohen, 2001), external stimuli com- The amygdala plays a core role in processing affective stimuli. pete for representational processing resources. Thus, the Research involving animal models identifies two main proces- observed heightened activation in sensory regions likely sing routes for affective sensory inputs (LeDoux, 1994, 2000). reflects a competitive advantage that is granted to the sensory In addition to sensory inputs to the amygdala being channeled

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270 INTRODUCTION TO COGNITIVE | Interactions between Attention and Emotion

via their primary cortical areas, a second ‘low road’ provides Complementing findings from research, the amygdala rapid access to these representations, via a pulvi- damage to the amygdala removes attentional advantages for nar connection to the that bypasses cortical emotional stimuli (Phelps & LeDoux, 2005), including abol- sensory regions, enabling speeded processing of incoming ishing the ability of emotional stimuli to resist the attentional representations and facilitating rapid behavioral adjustments blink (Anderson & Phelps, 2001). Strikingly, attentional (LeDoux, 1994, 2000). There is some neuroimaging evidence advantages for emotional stimuli are observed even when neu- supporting a role for this direct amygdala input, such as the ral regions related to perceptual processing are damaged if the finding that the amygdala, pulvinar, and superior colliculus all amygdala remains intact. For instance, spatial neglect patients exhibit enhanced activation to fearful compared to neutral face have difficulty orienting their attention to the contralesional images of low spatial frequency (Vuilleumier, Armony, Driver, hemifield due to damage. However, these patients & Dolan, 2003), consistent with the notion that coarse repre- can still detect emotionally expressive faces in the neglected sentations of visual stimuli are rapidly conveyed along this hemifield (Fox, 2002; Vuilleumier & Schwartz, 2001), and processing route. However, recent theories have called into these faces still evoke heightened activations in sensory proces- question whether this pathway is critical in human affective sing regions compared to neutral faces even when they are visual processing (Pessoa & Adolphs, 2010). Nevertheless, the neglected (Vuilleumier et al., 2002). Converging evidence highly interconnected nature of the amygdala (LeDoux, 2000; from blindsight patients (who have lesions to the primary Young, Scannell, Burns, & Blakemore, 1994) makes it well visual cortex, removing one visual hemifield from awareness) suited to serve as a hub for the integration of affective infor- demonstrates that these individuals remain able to discrimi- mation (Pessoa, 2008) and a node that could bias processing nate emotional stimuli presented in the blinded hemifield, in other neural networks. despite difficulty judging nonemotional stimuli (Morris, The amygdala has reciprocal, topographically organized con- DeGelder, Weiskrantz, & Dolan, 2001; Pegna, Khateb, nections with sensory cortices (Amaral, Behniea, & Kelly, 2003) Lazeyras, & Seghier, 2005). This affective discrimination is through which it may amplify neural processing of affectively associated with enhanced activation in the amygdala (Pegna salient stimuli across multiple stages of sensory processing. et al., 2005), consistent with the notion of a ‘low-road’ proces- Increases in amygdala and cortical activations to affectively sing pathway for affective stimuli that bypasses cortical sensory salient stimuli are correlated (Morris et al., 1998; Pessoa, regions (LeDoux, 2000). Generally speaking, perceptual and McKenna, Gutierrez, & Ungerleider, 2002; Sabatinelli et al., attentional processing advantages for emotional stimuli appear 2005), and lesions to the amygdala abolish enhanced cortical to be most pronounced for negatively valenced (Vuilleumier, activations to affectively salient stimuli (Vuilleumier, Richard- 2005) or biologically prepared (Ohman & Mineka, 2001) son, Armony, Driver, & Dolan, 2004), suggesting that the amyg- stimuli, although similar effects are also observed with positive dala plays a role in instantiating heightened sensory processing stimuli or stimuli that acquire affective through of affectively salient inputs. Activation in the amygdala is also learning. associated with enhanced attentional orienting to emotionally salient stimuli (Armony & Dolan, 2002) or cases where emo- Attention Modulates Affective Processing tional stimuli resist the attentional blink (Lim et al., 2009). Evidence from multiple neuroimaging experiments indicates Although amygdala activation is commonly observed in that the amygdala partly guides orienting via connections with response to affective stimuli, the extent to which this activation the frontoparietal attention network. When emotional stimuli is dependent on attention remains contentious. Enhanced spatially cue attention, they activate intraparietal sulcus, the amygdala responses to affective stimuli have been observed , and (Armony & in the absence of conscious awareness of emotional stimuli Dolan, 2002; Pourtois, Schwartz, Seghier, Lazeyras, & Vuilleu- (Morris et al., 1998; Whalen et al., 1998, 2004) and when mier, 2006; Reeck, LaBar, & Egner, 2012). Moreover, investiga- emotional stimuli are unattended (Anderson, Christoff, Panitz, tions of the attentional blink demonstrate that although the De Rosa, & Gabrieli, 2003; Vuilleumier et al., 2001), leading amygdala directly interacts with sensory regions to enhance many to theorize that amygdala activation is largely automatic representations, its influence is at least partially mediated by and occurs independent of attention. However, others have activations in medial prefrontal regions and lateral parietal found that differential amygdala responding to affective stim- regions implicated in attention (Lim et al., 2009). One possibil- uli is diminished or abolished under high attentional load ity then is that, in addition to direct amygdala contributions to (Hsu & Pessoa, 2007; Pessoa, Padmala, & Morland, 2005; the perceptual prioritization of emotional stimuli, the dorsal Pessoa et al., 2002), providing competing evidence that atten- attention system may coordinate inputs of affective processing tion does influence affective neural processing. Investigations regions to construct a top-down salience map (Mohanty, Egner, examining individual differences suggest that may Monti, & Mesulam, 2009; Mohanty & Sussman, 2013)that moderate the effects of attention on amygdala responses to subsequently guides attention and directs processing resources. affective stimuli (Bishop, Duncan, & Lawrence, 2004b), pro- Parallel mechanisms are likely at work when attention is guided viding one potential reconciliation of these disparate findings by rewarding stimulus properties, though these may addition- in the literature. ally involve the modulation of frontoparietal attention systems The manner in which emotional stimuli are interpreted or by subcortical regions specialized in appraising appetitive stim- ‘appraised’ also contributes to their impact on neural proces- ulus value, like the ventral striatum (Krebs, Boehler, Egner, & sing. For instance, a surprised face presented in conjunction Woldorff, 2011) and dopaminergic (Mohanty, Gitel- with a positive context (e.g., “This person just won the lottery”) man, Small, & Mesulam, 2008). is less likely to evoke neural activation in the amygdala than if

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INTRODUCTION TO | Interactions between Attention and Emotion 271

it was associated with a negative context (e.g., “This person just employing magnetic resonance diffusion tractography have lost $200”; Kim et al., 2004). The interpreted affective source of supported this distinction in connectivity, revealing that both the expression, either elation or distress, shapes the neural the pregenual and subgenual subdivisions of the rostral anterior response to the elicitor, even though it was perceptually iden- cingulate cortex maintain connections with regions critical to tical in both cases. Similarly, gustatory stimuli are perceived as affective processing (Beckmann, Johansen-Berg, & Rushworth, more pleasant and generate greater activation in the ventral 2009) and placing the rostral anterior cingulate cortex in striatum and orbitofrontal cortex when presented with the optimal position to exert influence during affective control. label ‘Rich’ instead of ‘Basic’ (Grabenhorst, Rolls, & Bilderbeck, However, these early Stroop adaptations have been criti- 2008). Identical olfactory stimuli are also rated more pleasant cized on a range of issues (Algom, Chajut, & Lev, 2004; Reeck & when labeled as ‘cheddar cheese’ than when presented as ‘body Egner, 2011), including that emotional distracters rarely gen- odor,’ with differential activation in the orbitofrontal cortex erated behavioral effects of interference (such as lengthened tracking this difference in perceived pleasantness (de Araujo, response times) and often did not directly compete with the

Rolls, Velazco, Margot, & Cayeux, 2005). Thus, interpretations task at hand (e.g., the negative semantic meaning of a word and appraisals may alter neural and affective responses by does not necessarily prompt a different font color response in modifying how attention to a stimulus is allocated, enhancing the emotional color-word Stroop). Recent Stroop adaptations processing of features consistent with the presented interpreta- attempting to address these concerns have included the face- tion. This phenomenon is closely related to the emerging field word emotional Stroop, in which individuals state the affective of emotion regulation research, where altering the interpreta- expression displayed in a photograph of a face while ignoring tion of the emotional elicitor has been shown to diminish the a competing affective word printed over the image (Egner, subjective experience of negative , as well as the neu- Etkin, Gale, & Hirsch, 2008; Etkin, Egner, Peraza, Kandel, & ral activation associated with those elicitors in the amygdala, Hirsch, 2006). Findings from these studies suggest that activa- with prefrontal control regions exhibiting heightened activa- tion in the amygdala and dorsal anterior cingulate cortex tion during regulation (Delgado, Nearing, LeDoux, & Phelps, tracks affective conflict and that activation in the rostral ante-

2008; Ochsner, Bunge, Gross, & Gabrieli, 2002). Top-down rior cingulate cortex helps resolve that conflict through inhib- factors therefore appear to exert influence on emotional signals itory interactions with the amygdala (Egner et al., 2008; Etkin in order to shape subjective experience and responses. et al., 2006), a neural signature that has been found to be disrupted in generalized anxiety disorder (Etkin, Prater, Hoeft, Menon, & Schatzberg, 2010). Consideration of the dor-

Affective Salience and Executive Control sal anterior cingulate cortex activation by emotional conflict, as well as during classic conditioning and instructed fear Emotional stimuli often gain prioritized access to attentional learning, has led some researchers to reconceptualize the ante- resources, and when they compete with other ongoing mental rior cingulate cortex’s role in emotional processing, whereby processing, control mechanisms (which regulate the allocation the dorsal/caudal aspect of this region is to be of top-down attention) may mobilize to reduce their involved in the appraisal and expression of negative emotion interference. Several neuroimaging studies examining the neu- and the more ventral/rostral aspect to be involved in regulating ral regions involved in mitigating distraction from emotional emotional responses (Etkin, Egner, & Kalisch, 2011; Shackman sources adapted Stroop paradigms to include affectively salient et al., 2011). distracters. Popular variants, such as the emotional counting Several neurocognitive theories of emotion–

Stroop (wherein participants indicate how many times an interactions have emerged out of the selective attention litera- affective word is printed on a screen) and the emotional ture. In contrast to early theoretical approaches that delineated color-word Stroop (in which participants name the ink color a sharp boundary between pure emotion and pure cognition an affective word is printed in), were developed to examine (Lazarus, 1984; Zajonc, 1984), recent theories emphasize the how ignoring emotional information (particularly negative integration of emotion and cognition. One such approach is content) impacted attention. Neuroimaging studies involving the dual-competition model proposed by Luiz Pessoa (Pessoa, emotional Stroop paradigms implicated the rostral anterior 2009). This theory builds on biased-competition models of cingulate cortex in emotional interference (Mohanty et al., attention and control (Desimone & Duncan, 1995; Miller & 2007; Whalen et al., 1998), consistent with other studies Cohen, 2001), proposing that emotion may alter cognition at utilizing emotional stimuli as distracters (Bishop, Duncan, & multiple stages of processing, including gaining prioritized Lawrence, 2004a; Vuilleumier et al., 2001). Early meta- access to perceptual processing and modulating executive con- analyses of these investigations supported a dissociation in trol functions (Pessoa, 2009). This executive processing mod- anterior cingulate cortex, positing that the dorsal anterior cin- ulation is based on theories that posit that certain mechanisms gulate cortex was involved in nonaffective selective attention and resources are shared across multiple control functions and the rostral anterior cingulate cortex was involved in affec- (Duncan, Emslie, Williams, Johnson, & Freer, 1996; Miyake tive selective attention (Bush, Luu, & Posner, 2000). This dis- & Friedman, 2012) and proposes that emotional stimuli are tinction dovetails well with the evidence that dorsal anterior more likely to gain access to this pool of shared executive cingulate cortex is connected with the dorsolateral prefrontal resources when they are not already fully absorbed by other cortex, parietal cortex, and motor areas, while the rostral extent processing demands. At the neural level, this theory empha- is connected with the amygdala, the nucleus accumbens, the sizes the integration of emotional and nonemotional proces- hippocampus, the anterior insula, and the orbitofrontal cortex sing streams, highlighting the role of neural processing hubs (Devinsky, Morrell, & Vogt, 1995). Recent investigations (e.g., the anterior cingulate cortex, amygdala, and dorsolateral

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272 INTRODUCTION TO COGNITIVE NEUROSCIENCE | Interactions between Attention and Emotion

) in integrating information from multiple instead emphasizing interdependence between these con- sources and regulating processing in other neural regions structs in both neural processing and cognitive processing.

(Pessoa, 2008). In contrast to the dual-competition model, Not only can emotion bias attention, but attention can also others have placed more emphasis on the modularity of certain alter emotional responding and mitigate distraction caused by aspects of emotional and nonemotional processing. For emotional stimuli. The precise mechanisms underlying inter- instance, drawing on executive control frameworks that distin- actions between emotion and attention remain an exciting guish between the detection and the resolution of competing endeavor for future research, with high relevance to many stimulus representations, action tendencies, or response rules prevalent clinical conditions including anxiety and addiction. (Botvinick, Braver, Barch, Carter, & Cohen, 2001), some recent work suggests that conflict resolution processes are modular and distinct for emotional and nonemotional sources of con- See also: INTRODUCTION TO ANATOMY AND PHYSIOLOGY: flict (Egner, 2008). Evidence from neuroimaging investigations Amygdala; INTRODUCTION TO COGNITIVE NEUROSCIENCE:

(Egner et al., 2008; Etkin et al., 2006), research involving lesion Attentional Capacity and Limitations; Salience/Bottom-Up Attention; patients (Maier & di Pellegrino, 2012), and behavioral investi- Top-Down Suppression; INTRODUCTION TO SOCIAL COGNITIVE gations (Kunde, Augst, & Kleinsorge, 2012; Soutschek & NEUROSCIENCE: and Elicitation; Emotion Schubert, 2013) support this potential modularity. Regulation; INTRODUCTION TO SYSTEMS: Brain Mapping of Another perspective on emotion–control interactions has Control Processes; Emotion. emerged from the literature on frontostriatal mechanisms for regulating the contents of working or ongoing task- representations (e.g., Braver & Cohen, 2000; Frank, Loughry, & O’Reilly, 2001). One influential proposition derived from this References work is based on the close link between rewarding stimuli and Algom, D., Chajut, E., & Lev, S. (2004). A rational look at the emotional Stroop striatal dopamine release and the latter’s assumed role in gating phenomenon: A generic slowdown, not a . Journal of Experimental information into . Specifically, it has been Psychology: General, 133(3), 323–338. http://dx.doi.org/10.1037/0096- proposed that positive stimuli (by eliciting striatal dopamine 3445.133.3.323. release) facilitate the gating of new information into prefrontal Alpers, G. W., & Gerdes, A. B.M (2007). Here is looking at you: Emotional faces predominate in binocular rivalry. Emotion, 7(3), 495–506. http://dx.doi.org/ working memory representations, which would be associated 10.1037/1528-3542.7.3.495. with a broad and flexible attentional state; by contrast, a neg- Alpers, G. W., & Pauli, P. (2006). Emotional pictures predominate in binocular rivalry.

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