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Interactions Between Attention and Emotion This article was originally published in Brain Mapping: An Encyclopedic Reference, published by Elsevier, and the attached copy is provided by Elsevier for the author's benefit and for the benefit of the author's institution, for non-commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who you know, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier's permissions site at: http://www.elsevier.com/locate/permissionusematerial Reeck C., and Egner T. (2015) Interactions between Attention and Emotion. 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 learning, 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 “affect” and “emotion” are used tively neutral stimuli. During visual search, 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 temperaments, 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 awareness of those stimuli, uli and modulate their capacity to influence perception, 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 distraction 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 cocktail party effect (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: binocular rivalry 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 Brain Mapping: An Encyclopedic Reference http://dx.doi.org/10.1016/B978-0-12-397025-1.00243-8 269 Brain Mapping: An Encyclopedic Reference, (2015), vol. 3, pp. 269-274 Author's personal copy 270 INTRODUCTION TO COGNITIVE NEUROSCIENCE | Interactions between Attention and Emotion via their primary cortical areas, a second ‘low road’ provides Complementing findings from neuroimaging research, the amygdala rapid access to these representations, via a pulvi- damage to the amygdala removes attentional advantages for nar connection to the superior colliculus 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 parietal lobe 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
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