Neuroscience and Biobehavioral Reviews

Neuroscience and Biobehavioral Reviews

Contents lists available at ScienceDirect Neuroscience and Biobehavioral Reviews journal homepage: www.elsevier.com/locate/neubiorev Review article Neural correlates of emotion-attention interactions: From perception, learning, and memory to social cognition, individual differences, and training interventions Florin Dolcosa,b,*, Yuta Katsumia,b, Matthew Moorea,b, Nick Berggrenc, Beatrice de Gelderd, Nazanin Derakshanc, Alfons O. Hamme, Ernst H.W. Kosterf, Cecile D. Ladouceurg, Hadas Okon-Singerh, Alan J. Pegnai, Thalia Richterh, Susanne Schweizerj, Jan Van den Stockk, Carlos Ventura-Bortl, Mathias Weymarl,SandaDolcosa,b,* a Department of Psychology, University of Illinois at Urbana-Champaign, Champaign, IL, USA b Beckman Institute for Advanced Science & Technology, University of Illinois at Urbana-Champaign, Urbana, IL, USA c Department of Psychological Sciences, Birkbeck, University of London, London, England, United Kingdom d Department of Psychology and Neuroscience, Maastricht University, Maastricht, Netherlands e Department of Biological and Clinical Psychology/Psychotherapy, University of Greifswald, Greifswald, Germany f Department of Experimental-Clinical and Health Psychology, Ghent University, Ghent, Belgium g Department of Psychiatry, Western Psychiatric Institute and Clinic, University of Pittsburgh Medical Center, University of Pittsburgh, Pittsburgh, PA, USA h Department of Psychology, University of Haifa, Haifa, Israel i School of Psychology, University of Queensland, Saint Lucia, Queensland, Australia j Institute of Cognitive Neuroscience (Developmental Cognitive Neuroscience Group), University College London, London, England, United Kingdom k Laboratory for Translational Neuropsychiatry, Research Group Psychiatry, Department of Neurosciences, KU Leuven, Leuven, Belgium l Department of Psychology, University of Potsdam, Potsdam, Germany ARTICLE INFO ABSTRACT Keywords: Due to their ability to capture attention, emotional stimuli tend to benefit from enhanced perceptual processing, Emotion which can be helpful when such stimuli are task-relevant but hindering when they are task-irrelevant. Altered Attention emotion-attention interactions have been associated with symptoms of affective disturbances, and emerging Perception research focuses on improving emotion-attention interactions to prevent or treat affective disorders. In line with Learning and memory the Human Affectome Project’s emphasis on linguistic components, we also analyzed the language used to de- Individual differences Training interventions scribe attention-related aspects of emotion, and highlighted terms related to domains such as conscious Psychophysiology awareness, motivational effects of attention, social attention, and emotion regulation. These terms were dis- Neuroimaging cussed within a broader review of available evidence regarding the neural correlates of (1) Emotion-Attention Affective neuroscience Interactions in Perception,(2)Emotion-Attention Interactions in Learning and Memory,(3)Individual Differences in Health and well-being Emotion-Attention Interactions,and(4)Training and Interventions to Optimize Emotion-Attention Interactions. This Linguistics comprehensive approach enabled an integrative overview of the current knowledge regarding the mechanisms of emotion-attention interactions at multiple levels of analysis, and identification of emerging directions for future investigations. Abbreviations: ABC, arousal-biased competition; ABM, attentional bias modification; ACC, anterior cingulate cortex; ACT, attentional control theory; AMs, auto- biographical memories; AMY, amygdala; BA, Brodmann area; CS, conditioned stimulus; DES, dorsal executive system; dlPFC, dorsolateral prefrontal cortex; Dm, Difference due to memory; EBA, extra-striate body area; EEG, electroencephalography; EM, episodic memory; ERP, event-related potentials; FA, focused attention; FBA, fusiform body area; FFA, fusiform face area; FG, fusiform gyrus; fMRI, functional magnetic resonance imaging; HC, hippocampus; IPL, inferior parietal lobule; IPS, intraparietal sulcus; LPC, lateral parietal cortex; LPP, late positive potential; MEG, magnetoencephalography; mPFC, medial prefrontal cortex; MTL, medial temporal lobe; NE, norepinephrine; OFA, occipital face area; PMv, ventral premotor area; pSTS, posterior superior temporal sulcus; PTSD, post-traumatic stress disorder; RT, reaction time; STS, superior temporal sulcus; TEC, trauma exposed control; TMS, transcranial magnetic stimulation; TPJ, temporo-parietal junction; UCS, unconditioned stimulus; VAS, ventral affective system; vmPFC, ventromedial prefrontal cortex; vlPFC, ventrolateral prefrontal cortex; WM, working memory ⁎ Corresponding authors at: Beckman Institute for Advanced Science & Technology, University of Illinois at Urbana-Champaign, 405 North Mathews Avenue, Urbana, IL 61801, USA. E-mail addresses: fdolcos@illinois.edu (F. Dolcos), sdolcos@illinois.edu (S. Dolcos). https://doi.org/10.1016/j.neubiorev.2019.08.017 Received 1 January 2019; Received in revised form 2 July 2019; Accepted 21 August 2019 F. Dolcos, et al. 1. Introduction and basic notions general consensus that affective phenomena (the more comprehensive term) consist of multiple subcomponents including physiological, ap- Decades of research have shown that emotional stimuli can benefit praisals, expressions, and behaviors that define the relation between the from enhanced perceptual processing due to their ability to capture individual and environment. From a practical standpoint, a simplistic attention, and through such prioritized processing they also impact dissociation between emotions and feelings that is typically used in other cognitive processes. For instance, emotional stimuli are better neuroscientific approaches is in terms of physiological vs. psychological encoded and remembered and can also be powerful distracters when aspects of affective processing (Iversen et al., 2000; LeDoux and Brown, task-irrelevant. Moreover, altered processing of emotional material has 2017). Namely, while emotions have more to do with bodily responses been associated with individual differences in various domains of (e.g., increased heart rate in a frightening situation), feelings refer to healthy functioning (sex, personality, age), as well as with symptoms of the associated psychological aspects (e.g., experiencing the feeling of affective disturbances, including anxiety and depression. The linguistic being afraid) produced by the specific circumstances. Feelings might search that builds the foundation of this special issue reflects the cen- therefore be best understood as subjective interpretations of physiolo- trality of attentional processes in affective experiences. The identified gical responses (Siddharthan et al., 2018). Studies of emotion-attention terms (Supplementary Table 1) can be broadly categorized into do- interactions have investigated both emotions (including unconscious/ mains relating to conscious awareness, motivational effects of attention, automatic bodily responses) and feelings (relatively more conscious social attention, and emotion regulation. We integrate the discussion of aspects of emotional responses), which are discussed throughout all these terms within a broader review of emerging scientific evidence sections of the current review. regarding emotion-attention interactions. We review evidence in healthy functioning and alterations observed in clinical conditions, with 1.2. Transient vs. long-term responses a particular emphasis on the associated neural mechanisms. This work brings together evidence based on various approaches, spanning from In addition to differentiating between emotions and feelings, it is behavioral and lesion to brain imaging and interventions, which are also important to consider the duration of affective experiences. What is grouped around the following four main themes: (1) Emotion-Attention commonly referred to as an occurrence of an emotion is transient and Interactions in Perception,(2)Emotion-Attention Interactions in Learning usually concerned with a specific object or situation (Russell and and Memory,(3)Individual Differences in Emotion-Attention Interactions, Barrett, 1999), whereas mood is considered to be much longer-lasting, and (4) Training and Interventions to Optimize Emotion-Attention diffuse, and less specific (Frijda, 2009). Furthermore, although emo- Interactions (Fig. 1). A detailed discussion of evidence regarding these tions tend to follow the emotion-eliciting stimuli closely or in- four themes is followed by a brief discussion of related linguistic aspects stantaneously, a mood might be temporally remote from its cause, (5). Such a comprehensive approach allows for an integrative under- making the cause of a mood difficult to identify (Morris, 1992). standing of the available evidence and identification of concrete ave- Moreover, prolonged emotional responses and moods are also com- nues for future investigations. In the remainder of this introductory monly observed as symptoms of anxiety, depression, or trauma- and section, we briefly introduce basic concepts that are relevant stress-related disorders, which are characterized by recurrent and in- throughout the review. trusive thoughts about previous or anticipated distressing or potentially traumatic events (Dalgleish and Power, 2004). Of particular relevance for the present review, such symptoms of affective dysregulation have 1.1. Emotions vs. feelings been associated with deficits in top-down attentional control (Schäfer et al., 2018). These and

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