The Brain Basis of Emotion: a Meta-Analytic Review
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BEHAVIORAL AND BRAIN SCIENCES (2012) 35, 121–202 doi:10.1017/S0140525X11000446 The brain basis of emotion: A meta-analytic review Kristen A. Lindquist Department of Neurology, Harvard Medical School/Massachusetts General Hospital/Martinos Center for Biomedical Imaging, Charlestown, MA 02129, and Department of Psychology, Harvard University, Cambridge, MA 02138 [email protected] http://www.nmr.mgh.harvard.edu/lindqukr/ Tor D. Wager Department of Psychology and Neuroscience, University of Colorado, Boulder, CO 80309 [email protected] http://www.psych.colorado.edu/tor/ Hedy Kober Department of Psychiatry, Yale University School of Medicine, New Haven, CT 06519 [email protected] http://medicine.yale.edu/psychiatry/people/hedy_kober.profile Eliza Bliss-Moreau California National Primate Research Center, University of California, Davis, CA 95616, and Department of Psychiatry and Behavioral Sciences, University of California, Davis, CA 95616 [email protected] http://www.elizablissmoreau.com/EBM/home.html Lisa Feldman Barrett Department of Psychology, Northeastern University, Boston, MA 02115, and Departments of Radiology and Psychiatry, Harvard Medical School/ Massachusetts General Hospital/Martinos Center for Biomedical Imaging, Charlestown, MA 02129 [email protected] http://www.affective-science.org/ Abstract: Researchers have wondered how the brain creates emotions since the early days of psychological science. With a surge of studies in affective neuroscience in recent decades, scientists are poised to answer this question. In this target article, we present a meta-analytic summary of the neuroimaging literature on human emotion. We compare the locationist approach (i.e., the hypothesis that discrete emotion categories consistently and specifically correspond to distinct brain regions) with the psychological constructionist approach (i.e., the hypothesis that discrete emotion categories are constructed of more general brain networks not specific to those categories) to better understand the brain basis of emotion. We review both locationist and psychological constructionist hypotheses of brain–emotion correspondence and report meta-analytic findings bearing on these hypotheses. Overall, we found little evidence that discrete emotion categories can be consistently and specifically localized to distinct brain regions. Instead, we found evidence that is consistent with a psychological constructionist approach to the mind: A set of interacting brain regions commonly involved in basic psychological operations of both an emotional and non-emotional nature are active during emotion experience and perception across a range of discrete emotion categories. Keywords: Discrete emotion; emotion experience; emotion perception; meta-analysis; neuroimaging; psychological construction 1. Introduction and sensory centres already assigned” (James 1890/1998, p. 473). In this target article, we statistically summarize William James framed the question of emotion–brain cor- the last 15 years of neuroimaging research on emotion in respondence when he wrote, “of two things concerning the an attempt to determine which of these alternatives is emotions, one must be true. Either separate and special correct. We examine the utility of two different models centres, affected to them alone, are their brain-seat, or of emotion that have each existed since the beginning of else they correspond to processes occurring in the motor psychology. # Cambridge University Press 2012 0140-525X/12 $40.00 Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 30 May 2017 at 18:25:29, subject to the Cambridge Core terms of use, available at 121 https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0140525X11001531 Lindquist et al.: The brain basis of emotion 2. A locationist account of the brain basis of KRISTEN A. LINDQUIST is a Postdoctoral Fellow at the emotion Harvard University Mind/Brain/Behavior Initiative and is affiliated with the Departments of Neurology A locationist account of emotion assumes that the category / (Harvard Medical School Massachusetts General emotion and individual categories such as anger, disgust, Hospital) and Psychology (Harvard University). She received her A.B. in 2004 and her Ph.D. in 2010 fear, happiness, sadness (and perhaps a few others) are from Boston College. Her interdisciplinary research respected by the body and brain (see Barrett [2006a] for uses social cognitive, psychophysiological, neuropsy- a discussion). The guiding hypothesis of this natural kind chological, and neuroimaging methods to understand model (Barrett 2006a) or modal model (Barrett et al. how emotions emerge from the combination of more 2007d) of emotion is that different emotion categories basic psychological operations. refer to states with endowed motivational characteristics that drive cognition and behavior. It is assumed that TOR D. WAGER is the director of the Cognitive and these states are biologically basic and inherited, and Affective Neuroscience Laboratory at the University cannot be broken down into more basic psychological of Colorado, Boulder. He received his Ph.D. in cogni- components (Ekman & Cordaro 2011; Izard 2011; Pank- tive psychology, with a focus in cognitive neuroscience, sepp & Watt 2011). Despite these common assumptions, from the University of Michigan in 2003. He joined the there is variability in how different researchers define faculty of Columbia University as an Assistant Professor emotions as natural kinds. Some theorists emphasize the of Psychology in 2004, and was appointed Associate Professor in 2009. In 2010, he joined the faculty of universal characteristics of emotion categories, suggesting the Department of Psychology and Neuroscience at that each emotion category (e.g., anger) refers to a “family” the University of Colorado, Boulder. His research of states that share a distinctive universal signal (e.g., facial focuses on how expectations shape responses to pain behavior), physiology, antecedent events, subjective and emotional cues in the brain and body. Peer- experience, and accompanying thoughts and memories reviewed publications include work on brain mechan- (e.g., Ekman & Cordaro 2011). In this view, emotions isms of placebo analgesia and the cognitive regulation can be shaped by culture and learning, but all humans of emotion and attention. possess the capacity to experience and perceive the same core set of emotion categories. HEDY KOBER is an Assistant Professor in Psychiatry, Other theorists take a developmental approach and Psychology, and Cognitive Science at Yale University argue that all infants are born with a set of “first order and Director of the Clinical and Affective Neuro- emotions” that are evolutionarily given reactions (includ- science Laboratory and Director of Research at Yale’s ing feelings, motivations and behaviors) to specific Therapeutic Neuroscience Clinic. She received her B.A., M.A., and M.Phil. in Psychology from Columbia stimuli (e.g., Izard 2011). First order emotions form the University. She completed her Ph.D. in Psychology core of the more elaborate “emotion schemas” that with a focus on Cognitive and Affective Neuroscience develop with age and learning and consist of complex com- at Columbia University in 2009. Her research focuses binations of emotions, cognitions, and behaviors. Still on neural mechanisms of psychological change, regu- other theorists emphasize the evolutionary aspect of lation of craving, and regulation of emotion more emotion categories, and argue that emotions are specific generally. behavioral adaptations that are shared with other mamma- lian species and passed down through phylogeny (e.g., ELIZA BLISS-MOREAU is a Postdoctoral Researcher at Panksepp 1998; 2007; Panksepp & Watt 2011). Some the University of California, Davis and the California models taking an “appraisal” approach to emotion also National Primate Research Center. She received her draw on natural kind assumptions about emotions (cf. S.B. in biology and psychology in 2002 and her Ph.D. Barrett 2006a) by hypothesizing that dedicated cognitive in psychology in 2008 from Boston College. Her mechanisms automatically make meaning of a stimulus research focuses on the neurobiological and physiologi- cal underpinnings of individual differences in affect and trigger the corresponding discrete emotion (e.g., and emotion. She adopts a translational approach by Roseman 1984; Ellsworth & Scherer 2003). Relatively modeling affective processing in both humans and non- little work from an appraisal perspective has investigated human primates. the brain basis of emotion (although see Sander et al. 2003; 2007). Therefore, we do not discuss appraisal LISA FELDMAN BARRETT is Distinguished Professor models further in this article. of Psychology and Director of the Interdisciplinary All natural kind models share the assumption that differ- Affective Science Laboratory (IASLab) at Northeast- ent emotion categories have their roots in distinct mechan- ern University, with research appointments at isms in the brain and body. The mechanisms underlying Harvard Medical School and Massachusetts General discrete emotion categories have been discussed as resid- Hospital. Dr. Barrett received her B.Sc. from the Uni- ing within particular gross anatomical locations (e.g., versity of Toronto in 1986, and her Ph.D. in clinical Calder 2003; Ekman 1999) or networks (e.g., Izard 2011; psychology from the University of Waterloo in 1992. Panksepp 1998) in the brain. These models constitute